Advances in MARINE BIOLOGY Series Editor
DAVID W. SIMS Marine Biological Association of the United Kingdom, The Laboratory Citadel Hill, Plymouth, United Kingdom Editors Emeritus
LEE A. FUIMAN University of Texas at Austin
CRAIG M. YOUNG Oregon Institute of Marine Biology Advisory Editorial Board
ANDREW J. GOODAY Southampton Oceanography Centre
GRAEME C. HAYS University of Wales Swansea
SANDRA E. SHUMWAY University of Connecticut
ROBERT B. WHITLATCH University of Connecticut
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Harborne, A. R., Mumby, P. J., Micheli, F., Perry, C. T., Dahlgren, C. P., Holmes, K. E., and Brumbaugh, D. R. The functional value of Caribbean coral reef, seagrass and mangrove habitats to ecosystem processes. pp. 57–189. Collins, M. A. and Rodhouse, P. G. K. Southern ocean cephalopods. pp. 191–265. Tarasov, V. G. EVects of shallow-water hydrothermal venting on biological communities of coastal marine ecosystems of the western Pacific. pp. 267–410. Volume 51, 2006. Elena Guijarro Garcia. The fishery for Iceland scallop (Chlamys islandica) in the Northeast Atlantic. pp. 1–55. JeVrey, M. Leis. Are larvae of demersal fishes plankton or nekton? pp. 57–141. John C. Montgomery, Andrew Jeffs, Stephen D. Simpson, Mark Meekan and Chris Tindle. Sound as an orientation cue for the pelagic larvae of reef fishes and decapod crustaceans. pp. 143–196. Carolin E. Arndt and Kerrie M. Swadling. Crustacea in Arctic and Antarctic sea ice: Distribution, diet and life history strategies. pp. 197–315. Volume 52, 2007. Leys, S. P., Mackie, G. O. and Reiswig, H. M. The Biology of Glass Sponges. pp. 1–145. Garcia E. G. The Northern Shrimp (Pandalus borealis) Offshore Fishery in the Northeast Atlantic. pp. 147–266. Fraser K. P. P. and Rogers A. D. Protein Metabolism in Marine Animals: The underlying Mechanism of Growth. pp. 267–362. Volume 53, 2008. Dustin J. Marshall and Michael J. Keough. The Evolutionary Ecology of Offspring Size in Marine Invertebrates. pp. 1–60. Kerry A. Naish, Joseph E. Taylor III, Phillip S. Levin, Thomas P. Quinn, James R. Winton, Daniel Huppert, and Ray Hilborn. An Evaluation of the Effects of Conservation and Fishery Enhancement Hatcheries on Wild Populations of Salmon. pp. 61–194. Shannon Gowans, Bernd Wu¨rsig, and Leszek Karczmarski. The Social Structure and Strategies of Delphinids: Predictions Based on an Ecological Framework. pp. 195–294.
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Volume 54, 2008. Bridget S. Green. Maternal Effects in Fish Populations. pp. 1–105. Victoria J. Wearmouth and David W. Sims. Sexual Segregation in Marine Fish, Reptiles, Birds and Mammals: Behaviour Patterns, Mechanisms and Conservation Implications. pp. 107–170. David W. Sims. Sieving a Living: A Review of the Biology, Ecology and Conservation Status of the Plankton-Feeding Basking Shark Cetorhinus Maximus. pp. 171–220. Charles H. Peterson, Kenneth W. Able, Christin Frieswyk DeJong, Michael F. Piehler, Charles A. Simenstad, and Joy B. Zedler. Practical Proxies for Tidal Marsh Ecosystem Services: Application to Injury and Restoration. pp. 221–226.
PREFACE
Echinoderms are fascinating creatures that display a rich array of reproductive modes and strategies. As members of the invertebrate deuterostomes, the closest extant relatives of vertebrates, they also occupy a very significant phylogenetic position. For this reason, echinoderms have received considerable attention over the past decades from researchers in various fields. This has allowed particularly significant advances to be made in the areas of gamete biology, developmental processes, and genomics. With the advent of new biochemical and molecular tools, the recent discovery of species dwelling in deep-sea habitats (presumably far removed from the direct influence of familiar environmental fluctuations) and the growing number of aquaculture initiatives, studies on the reproduction of echinoderms have entered a new era. Nevertheless, fundamental questions such as the respective, and possibly, synergistic contributions of biological, chemical, and physical factors to successful breeding events and the recruitment of new generations remain incompletely understood. To draw a comprehensive portrait of our current understanding of the endogenous and exogenous mediation of gamete synthesis and spawning in echinoderms, we have endeavored in this review to compile and assimilate a large body of literature, including work dating back over a century. Early and recent studies provide a wide blend of approaches and exhibit various degrees of reliability and completeness. We have tried to present the data as objectively as possible, outlining the proposed hypotheses and leaving the reader to weigh opposing arguments. In the concluding chapter, we provide a personal analysis, contrasting, and sometimes questioning both the traditional paradigms and novel theories, and identifying the main gaps in our knowledge. It goes without saying that this contribution relies entirely on the collective effort of innumerable colleagues, which form a vast and rich research community dedicated to the study of echinoderm ecology and reproduction. They are too numerous to acknowledge fully here; however, we would like to highlight in this context the pioneering work of Arthur C. Giese, Haruo Kanatani, Fu-Shiang Chia, John M. Lawrence, and John S. Pearse who have paved the way for generations of enthusiastic echinodermologists around the world. We would also like to extend our warmest and most sincere thanks to John S. Pearse (University of California, Santa Cruz) and Raymond J. Thompson (Memorial University) for their valuable input and comments. xi
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Owing to the apparent complexity and diversity of reproductive strategies displayed by echinoderms of all shapes and origins, and the likely absence of universal patterns, we wholeheartedly admit that this work is by no means definitive. It is our sincere hope that it will, however, provide solid framework for those wishing to push our understanding yet further, and fuel our never-ending fascination with this exceptional Phylum. ANNIE MERCIER JEAN-FRANC¸OIS HAMEL
C H A P T E R
O N E
Introduction Abstract Most echinoderms display seasonal or other temporal cycles of reproduction that presumably result from the complex interplay of endogenous and exogenous signals. Various environmental, chemical and hormonal factors, acting directly or indirectly, individually or in combination, have been proposed to cue, favour or modulate a suite of reproductive functions from the onset of gametogenesis to gamete release. From as early as the nineteenth century, an astonishing array of studies has been published on topics related to the control of reproduction in echinoderms, ranging from fortuitous behavioural observations to complex experimental demonstrations and molecular analyses. Although the exact pathways involved in the perception of external signals and their transduction into coordinated spawning events remain obscure for most species, significant advances have been made that shed new light on the information gathered over decades of research. By compiling the existing literature (over 1000 references), interpreting the main results, critically assessing the methodologies used and reviewing the emerging hypotheses, we endeavour to draw a clearer picture of the existing knowledge and to provide a framework for future investigation of the mechanisms that underlie reproductive strategies in echinoderms and, by extension, in other marine invertebrates.
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1. Terminology 2. Brief Overview of Reproductive Features
The regulation of reproductive processes in marine invertebrates has been discussed in the literature since the end of the nineteenth century. Echinoderms were initially studied in this context because they were abundant and fairly easy to collect and maintain in captivity. More recently, they have become models for the study of gamete biology and some species of echinoids and holothuroids have been reared in captivity as part of aquaculture or restocking programmes, yielding a larger body of knowledge on their reproductive processes. Except for a small number of mammals, including humans, most animals show distinct reproductive seasons or cycles (Cloudsley-Thompson, 1961; Rusak and Zucker, 1975). Both timing and duration of breeding periods are crucial elements of the overall life history strategy of an organism Advances in Marine Biology, Volume 55 ISSN 0065-2881, DOI: 10.1016/S0065-2881(09)55001-8
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(Boolootian, 1966; Giese et al., 1991). Reproductive activity is usually timed to coincide with optimal environmental conditions for offspring survival, including food availability. Breeding success in echinoderms, as in other marine invertebrates, depends on highly synchronized processes between individuals of a population at the level of gamete synthesis and spawning. This synchronization is generally believed to be mediated by external cues (i.e., environmental factors) which may act either directly or indirectly, alone or in synergy, to reset or maintain biological clocks. Increasing evidence is pointing to the transduction of environmental signals via the endocrine system, but we are only beginning to understand the depth and complexity of the pathways and mechanisms involved and the possible role of chemical communication in this scheme. Indeed, different species may exhibit markedly different breeding strategies and periodicities, based largely on their specific life history, social arrangement, type of gonad and gamete development, endocrine system, and response to environmental fluctuations/stimuli. Furthermore, different populations of the same species often breed at different, locally suitable times while using the same suite of synchronizing cues. Reviews of echinoderm biology which either focused on or included various aspects of their reproduction were published between 1955 and 1991 (e.g., Binyon, 1972; Boolootian, 1966; Giese and Pearse, 1974; Giese et al., 1991; Hyman, 1955; Kanatani and Nagahama, 1983; Shirai and Walker, 1988). These publications considered what was known at the time about gametogenesis, spawning, gonad morphology and environmental cues related to the reproductive cycle. Interest in these concepts has flourished over the past two decades following the study of species from new locations (e.g., Antarctica, deep-sea habitats) or within aquaculture programmes and the use of novel techniques to probe the neurological and hormonal reactions involved in the synthesis and release of gametes. Apart from reproductive aspects discussed within reviews of specific groups [e.g., edible sea urchins (Lawrence, 2007)], there has been no comprehensive synthesis of the abundant data published on the control of reproduction in echinoderms since the early 1990s. The objective of this review is to update this wealth of information and discuss the control of reproduction in echinoderms in light of a more complete understanding of the interactions and processes involved. In so doing, we present a comprehensive account that integrates the early ground-breaking work on the influence of external factors (e.g., temperature, photoperiod, lunar cycle, phytoplankton) with recent results on chemical ecology, endocrine systems, entrained biological clocks and social behaviours. Evidence has been compiled for coastal and deep-sea species within the five conventional classes of extant echinoderms (Crinoidea, Ophiuroidea, Holothuroidea, Asteroidea and Echinoidea). The enigmatic class Concentricyloidea is not included as it currently contains only three
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little known species of Xyloplax and is the subject of taxonomic controversy ( Janies and Mooi, 1998; Mah, 2006; Pearse and Pearse, 1994; Rowe, 1988). We hope that the concepts emerging from the analysis of this large body of literature will provide a framework for further investigation of the mechanisms underlying reproductive behaviour, and be used as a guide for manipulating reproductive processes to gain insights into the proximate and ultimate triggers of the observed breeding strategies and periodicities. Understanding how exogenous and endogenous factors interact to ensure gamete competence at the proper time of year is important not only from an ecological standpoint but also for developing sustainable fisheries and aquaculture programmes, and for assessing how echinoderm populations may be affected by, and respond to, natural and man-made disturbances (e.g., fisheries, climate change, endocrine-disrupting chemicals). Through its appraisal and discussion of the presumed and confirmed paradigms, we trust that this review will provide a clearer picture of the existing knowledge and identify the areas in need of further investigation.
1. Terminology Regulation of the reproductive cycle is not only concerned with the timing of spawn-out, for this is merely the climax of considerable preparatory activity, but encompasses all aspects of the organism’s physiology and behaviour. The overall length of the breeding cycle can be looked upon as a function of the rate of growth, development, and maturation of gonadal tissues, ending in a spawning or a series of spawning events, followed by a period of germinal redevelopment (Giese, 1959a). Boolootian (1966) indicated that the reproductive cycle refers to the total course of events, regardless of the time period over which gamete production occurs (daily, weekly, monthly, annually, etc.) and Holland (1991) rightly pointed out that defining a beginning and an end in the annual reproductive cycle is arbitrary. The breeding season of a species, usually delineated in terms of months, is generally defined as the period of the year when most individuals in a population have numerous ripe gametes available for release (Giese and Pearse, 1974). In some species there is only one gametogenic cycle in each individual during each breeding season. The gametes may be released simultaneously or intermittently during the season (Giese and Pearse, 1974). In this review the breeding season will be discussed as a part of the gametogenic cycle, whereas spawning events will be addressed in a separate chapter, as years of research on the specific stimuli resulting in gamete release have identified it as a clearly distinct step in the reproductive process. There exists an important distinction between proximate factors, which serve as cues to maintain synchronous breeding within a population, and
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ultimate factors, which serve as selective forces that give survival value to the adaptation. In other words, the adaptive significance of spawning under certain conditions at a certain time can be distinguished from the mechanism by which this is achieved. The initial definitions of ultimate and proximate factors in the control of reproduction were first outlined by Baker (1938); however, Clark (1979) later suggested a further distinction between necessary environmental conditions (i.e., those allowing the completion of some cellular process essential for gamete maturation and breeding) and specific environmental signals that control the timing of reproductive events (Olive, 1995). According to Baker (1938), ultimate factors select individuals that produce young at the optimum time for survival; these factors do not, however, regulate the precise timing of breeding each year, which is controlled by proximate factors acting on gonad development well in advance of spawning. Proximate factors have been subdivided by Wingfield (1980) into two different types of information. The primary sources of initial predictive information for many animals are the large annual cycles such as photoperiod and temperature. Complete gonad development, mating (if any), and spawning are stimulated by supplementary information, for instance social cues and availability of particular foods. These factors vary from year to year and between locations, and they determine the exact timing of breeding each year. In echinoderms and other marine invertebrates, reproductive cycles are usually cyclic with annual, seasonal or monthly periodicities involving most individuals within a given population. This cyclic pattern is generally associated with habitats where environmental factors (e.g., photoperiod, temperature) fluctuate according to a predictable regime. However, a ‘‘continuous’’ reproductive pattern has been proposed for a growing number of species, mainly those found along the equator (e.g., Muthiga, 2005; Ramofafia et al., 2003) and in deep-water habitats (reviewed by Young, 2003). Like many of our colleagues, we recommend the use of the term ‘‘aperiodic’’, which refers to the absence of any detectable pattern. It is still unclear whether these species synthesize gametes and spawn opportunistically (or continuously) or whether part of the population follows a cyclic pattern (e.g., monthly) that is not detectable by conventional sampling techniques and analyses. Traditional gonad analysis of the equatorial sea cucumber Isostichopus fuscus from Ecuador suggested an aperiodic pattern of reproduction (Mercier et al., 2007), but direct observations over several years revealed a clear and predictable monthly periodicity, with <40% of individuals involved in a given spawning event. Hence, periodicities may easily be masked. Another example is the deep-sea asteroid Henricia lisa in which no periodicity in gonad maturation was found in serial samplings of the population. Nevertheless, laboratory monitoring over nearly 2 years showed a biannual periodicity (Mercier and Hamel, 2008). Furthermore,
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some species can complete the gametogenic cycle within periods as short as 2 weeks, which can remain unnoticed when individuals are collected from different locations or when sampling frequency is inadequate (Baillon, Hamel and Mercier, unpublished data). These results suggest that the term ‘‘continuous’’ is not appropriate, that ‘‘aperiodic’’ is more accurate, and that both should be used cautiously pending more refined sampling and analytical methods.
2. Brief Overview of Reproductive Features The Crinoidea, or feather stars, can be informally subdivided based on adult anatomy into stalked and stalkless species. Stalked crinoids are also referred to as sea lilies, whereas stalkless crinoids are commonly called feather stars or comatulids. The gonads of most species are located in the genital cavity of the arms and pinnules. The gonoduct, when present, is a small evagination of the inner epithelium of the ripe gonad. All crinoids are gonochoric, and hermaphroditism is rare and inconsistent (Dan and Dan, 1941; Holland, 1991; Mladenov, 1986; Vail, 1987). The sex ratio did not differ significantly from unity in the species studied and reviewed by Holland (1991). The class Ophiuroidea is composed of mostly unbranched species of brittle stars with a few, generally larger, species called basket stars, which possess prehensile, intricately branching arms. Most ophiuroids are gonochoric, bearing a set of paired gonads in each interradial area of the central disc. Many species display some form of hermaphroditism, in which case the paired gonads are either differentiated into a set of paired ovarian and testicular portions (Fell, 1946) or occur as ovotestes (Hyman, 1955). Confined to the Ophiuroidea are the bursae which function in reproduction, serving among other things as a common outlet for multiple gonoducts and as brood chambers in brooding species; fused bursae can be found in broadcast spawning species, more rarely in brooding species (Hendler, 1991). Most ophiuroids have two bursae at the base of each arm. The disposition of the gonads is variable, but in most species they are closely associated with the coelomic surface of the bursae, which may bear one or more gonads (Hendler, 1991). In the Holothuroidea, or sea cucumbers, the gonad is a single organ composed of multiple gonadal tubules, a gonad basis and a gonoduct leading to the gonopore(s). The sex ratio is usually close to 1:1 and hermaphroditic species are rare (Hyman, 1955; Smiley et al., 1991). Direct development is especially common in the order Dendrochirotida, whether the embryos are brooded or become motile vitellariae, whereas indirect development
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(i.e., occurrence of an auricularia stage which metamorphoses into a juvenile) is limited to the Aspidochirotida and Apodida (Smiley et al., 1991). The Asteroidea, or sea stars, exhibit a reproductive system which is organized either as a single proximal tuft of tubules with one gonoduct and gonopore (e.g., Asterina gibbosa, Ctenodiscus crispatus) or as multiple tufts distributed along the axis of each arm (Chia and Walker, 1991), in which case either each tuft has its own gonoduct and gonopore or a common gonoduct unites them all, leading to a single gonopore (e.g., Acanthaster planci, Astropecten irregularis, Linckia multifora and Luidia clathrata). Alternatively, some asteroids (e.g., Asterias rubens and other forcipulates) exhibit elongated gonads, or branched sacs, that enlarge during gametogenesis to fill the length of each ray (Chia and Walker, 1991). Aseroids exhibit a wide variety of reproductive modes, including common ones such as broadcast spawning and external brooding and uncommon highly derived ones such as internal fertilization, intra-gonadal incubation of progeny and live birth of juveniles (viviparity) (e.g., Byrne et al., 2003). Both gonochoristic and hermaphroditic species are known. In the Echinoidea, or sea urchins, branches of the genital coelomic and haemal sinuses interconnect the five gonads (Walker et al., 2007). A single gonoduct emerges from each gonad and extends within the branches of the aboral coelomic sinus before exiting the test through a pentagonal array of gonopores in the genital plates surrounding the anus (Walker et al., 2007). The echinoid gonad is essentially composed of tubules which ramify and anastomose extensively to form discrete organs suspended by the mesenteries in the perivisceral coelom. Gonads can be elongated well-formed structures or resemble clusters of grapes, depending on the season and the species (Pearse and Cameron, 1991). The majority of echinoids described so far broadcast their gametes and most instances of brooding are observed in Antarctic and deep-sea species. Although hermaphroditism seems to be rare, occurring in only a few individuals within certain species, it can take the form of either male or female-biased gonads (Pearse and Cameron, 1991). However, Moore et al. (1963a,b) noted that up to 27% of Tripneustes esculentus and 8% of Lytechinus variegatus were hermaphrodites at certain periods of the year and that this condition may easily be underestimated by not examining all the gonads.
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Gametogenesis Contents 7 9 9 10 11 11 12 13 14 34 35 58 65 66 66 66 67 70
1. General Note 1.1. Crinoidea 1.2. Ophiuroidea 1.3. Holothuroidea 1.4. Asteroidea 1.5. Echinoidea 1.6. Deep-sea echinoderms 2. Correlation with Exogenous Factors 2.1. Photoperiod and temperature 2.2. Lunar cycle 2.3. Food availability and nutrient storage 2.4. Inter-population and inter-individual communication 3. Endogenous Mediation 3.1. Crinoidea 3.2. Ophiuroidea 3.3. Holothuroidea 3.4. Asteroidea 3.5. Echinoidea
1. General Note Gametes are formed through gametogenesis, a process which is markedly similar among most animals (Giese and Pearse, 1974; Wourms, 1987). An individual gametogenic cycle usually includes the accumulation of nutrients to be utilized during gametogenesis, the proliferation of gonial cells and their differentiation into gametes, and a reproductively quiescent or spent period when residual gametes are absorbed or the adult dies. There is often little activity in the gonads following the release of the gametes, a period sometimes termed the resting phase. As first outlined by Giese and Pearse (1974), two main hypotheses have been proposed to explain the control of the gametogenic cycle within individuals: (1) it may be intrinsic, its timing being regulated by endogenous Advances in Marine Biology, Volume 55 ISSN 0065-2881, DOI: 10.1016/S0065-2881(09)55002-X
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2009 Elsevier Ltd. All rights reserved.
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(internal) factors (e.g., accumulation of nutrients and interplay of hormones between the controlling centers and the gonads); (2) it may be extrinsic or under exogenous (external) control (e.g., mediated via environmental changes). It has been postulated that whenever individual gametogenic cycles are synchronized within a species population, exogenous regulation is almost certainly involved (Giese and Pearse, 1974; Giese et al., 1991). The timing of reproduction in populations of different species of marine invertebrates evokes many patterns. Reproduction may occur rhythmically or sporadically during part or all of the year, or it may occur without any obvious periodicity. When rhythmic, the period of breeding may be daily, semi-monthly, monthly, semi-annual, annual, or biennial (Giese and Pearse, 1974). So-called continuous production of gametes (see Section 1 in Chapter 1) throughout the year is probably rare in an individual, inasmuch as successive gametogenic cycles usually have at least some pause between them. Gametogenesis may be staggered among different individuals during the year, so that reproduction appears to occur continuously throughout the year for the entire population (Giese and Pearse, 1974). A clear example of this has been provided by a recent study of the holothuroid Isostichopus fuscus that monitored gamete shedding for several years and tried to reconcile the data with the serial analysis of gonad maturity (Mercier et al., 2007). Although monthly spawnings followed predictable lunar and diel cycles, they were observed in only a portion of the population, therefore no clear periodicity was detectable in gonad samples. The overall length of the reproductive cycle can be regarded as a function of the rate of growth, development, and maturation of gonadal tissues, ending in a spawning or series of spawnings, followed by a period of germinal redevelopment (Giese, 1959a). In this process, a series of sequential events such as feeding activity, storage/translocation of nutrients and migrations may be involved, as well as gametogenesis and gonad growth. Each of these may be a cause or an effect of several exogenous or endogenous factors. If the timing of the reproductive cycle were regulated only endogenously (i.e., time necessary for completion of one set of biological events in the cycle), continuous breeding or breeding unaffected by geographical location would be expected (Giese and Pearse, 1974). However, this is seldom the case; environmental factors vary with time and season, and it is not surprising to find periodic reproductive processes, presumably timed to take advantage of favourable conditions, especially in terms of larval survival. Several factors are known to control some of the phases of the reproductive cycle (growth, maturation, spawning). These factors are of two types: (1) neuro-hormonal induction of maturation and shedding; (2) environmental factors such as biological stimuli triggering gametogenesis, and physical factors that probably control the neuro-hormonal system.
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1.1. Crinoidea Reproductive cycles in crinoids have been studied less than in other echinoderm classes (Nichols, 1991) and are still receiving little attention. Earlier reviews reported that most crinoids have short breeding seasons of 1–2 months (Boolootian, 1966; Clark, 1921; Hyman, 1955), although most of these conclusions were based on rather slim evidence from single or sporadic observations of spawning, the occurrence of large oocytes in the gonads, or the presence of juveniles on the adults. More thorough studies, especially on Oxycomanthus japonicus (formerly Comanthus japonica) (Dan and Kubota, 1960; Holland, 1981a; Holland et al., 1975), Florometra serratissima (Mladenov, 1986) and Promachocrinus kerguelensis (McClintock and Pearse, 1987), have shed more light on the reproductive cycles of crinoids, although studies have remained scarce over the last 20 years. In the most recent review available, Holland (1991) stated that germinal cell populations of several crinoids undergo annual gametogenic cycles, with few exceptions. The level of synchrony reported in gonad development varies considerably and discrepancies exist even for the same species studied in different localities. At the time Holland (1991) wrote his review on crinoids, nothing definite was known about the regulation of gametogenic cycles, and little has changed since. No rigorous experimental evidence has ever been presented on the control of gametogenesis in crinoids. However, a few hypotheses have been proposed, strictly based on correlations (Appendix A1). A significant portion of the evidence to date has been obtained from the Japanese species Oxycomanthus japonicus.
1.2. Ophiuroidea Reproductive patterns and timing of gametogenic activity in ophiuroids were last reviewed several years ago (Hendler, 1991; Rumrill, 1984). Gametogenesis has been studied in a number of species since the late 1800s (reviewed by Hendler, 1991) and more recently (e.g., Chao and Tsai, 1995; Falkner and Byrne, 2003; Gage et al., 2004; Gould et al., 2001; Gounin and Richard, 1992; Grange et al., 2004; Hendler and Tran, 2001; McClintock et al., 1993; McGovern, 2002; Morgan and Jangoux, 2002; Selvakumaraswamy and Byrne, 1995, 2000; Stewart and Mladenov, 1995; Sumida et al., 2000; Tominaga et al., 2004; Valentine, 1991a,b). Reproductive activity may occur throughout the year, or there may be distinct reproductive seasons. In many species with an annual cycle of gametogenic development, reproduction seems to extend over a period of several months. The influence of environmental factors on gametogenesis in ophiuroids is not well understood. Several investigators have tried to determine
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whether gamete synthesis and breeding periods are correlated with seasonal variations of physical or chemical parameters, but most correlations have been weak, comparing the reproductive cycle with only one of the many factors that act within a natural environment. Temperature and photoperiod are proximate factors that may directly regulate reproductive periodicity in ophiuroids (e.g., Hendler, 1979, 1991; Hendler and Tyler, 1986; Appendix A3). Other factors that may ultimately explain the adaptive significance of reproductive periodicity in this class include seasonal variation of food availability for either adults or larvae and habitat availability (Hendler, 1979; Rumrill and Pearse, 1985; Appendix A3).
1.3. Holothuroidea During the past 50 years, annual reproductive cycles and the factors that may control them have been investigated in many holothuroid species with varying precision and success (Catalan and Yamamoto, 1994; Conand, 1981, 1982, 1993a,b; Costelloe, 1985; Drumm and Loneragan, 2005; Engstrom, 1980; Green, 1978; Guzma´n et al., 2003; Hamel and Mercier, 1996a,b; Hamel et al., 1993; Krishnaswamy and Krishnan, 1967; Kubota, 2000; Morgan, 2000a,b; Ong Che, 1990; Ramofafia et al., 2000, 2001, 2003; Rasolofonirina et al., 2005; Sewell and Chia, 1994; Tanaka, 1958). An early review by Boolootian (1966) stated that specific breeding seasons had been noted or established for a number of holothuroids, and suggested that these patterns were largely determined by environmental factors. A later review indicated that, apart from general correlations between environmental factors and gonad maturity, the mechanisms controlling gametogenesis in holothuroids remained unknown (Smiley et al., 1991). These authors mentioned that correlations alone cannot properly demonstrate causality, and also noted methodological problems associated with experiments designed to analyse the role of single or multiple factors in the control of gametogenesis. Since then, few studies have succeeded in identifying experimentally the proximal factors responsible for the onset and progression of gametogenesis in holothuroids. The main factors that appear to be correlated with gametogenic development in holothuroids are: temperature, light intensity, photoperiod, lunar cycle, tidal flux, food availability, change in food type and diffusible chemical signals (e.g., Conand, 1993b; Hamel and Mercier, 1996b, 1999, 2004; Ramofafia et al., 2000; Smiley et al., 1991; Tan and Zulfigar, 2001; Appendix A5). Gamete maturation appears to be influenced by several physical and chemical factors that act either together, successively or independently of one another, and this may be particularly evident in species displaying a single, discrete annual spawning season.
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1.4. Asteroidea The reproductive cycles of sea stars are among the most studied within the Echinodermata. Several publications have outlined more or less robust correlations with environmental factors, while others have elegantly demonstrated the specific impacts of isolated mediators (Appendix A7). Photoperiod is probably the most widely proposed factor to control reproduction, based on correlations between global annual trends in temperature or day length and reproductive cycles in various asteroids (e.g., Byrne et al., 1997; Georgiades et al., 2006; Pastor-de-Ward et al., 2007; Stewart and Mladenov, 1995). The influence of photoperiod has been corroborated by experimental manipulations in a number of species (Bouland and Jangoux, 1988; Pearse and Beauchamp, 1986; Pearse and Bosch, 2002; Pearse and Eernisse, 1982; Pearse and Walker, 1986; Pearse et al., 1986a). The role of food and/or nutritional status has been documented mainly in terms of the relationship between gonad and pyloric caecum indices, which often, but not always, follow an inverse trend (e.g., Barker and Xu, 1991a,b; Byrne, 1992; Chen and Chen, 1992; Farmanfarmaian et al., 1958; Grange et al., 2007; Rubilar et al., 2005), whereas the direct influence of feeding remains unclear (e.g., Bouland and Jangoux, 1988; Worley et al., 1977). Finally, the role of sinking phytodetritus in stimulating gametogenesis has been evoked, although reports are sometimes contradictory (Benitez-Villalobos et al., 2007; Pearse, 1966; Ramirez-Llodra et al., 2002).
1.5. Echinoidea It should be noted at the outset that gonad growth in echinoids is not solely due to gamete synthesis. Somatic cells within the germinal epithelium (i.e., nutritive phagocytes) store extensive nutrient reserves before gametogenesis begins (Walker et al., 2007). Sea urchin reproduction is therefore generally characterized by cycles of gametogenesis and nutritive phagocyte growth and depletion (Walker et al., 2007). It is often defined as displaying two major phases: storage of nutrients and production of gametes (Scheibling and Hatcher, 2007). The seasonality of gametogenesis observed in several species of echinoids (Pearse, 1981; Pearse and Cameron, 1991) has raised questions regarding the role of environmental factors in the control of reproduction. Gametogenesis in temperate species of echinoids characteristically follows an annual cycle (King et al., 1994; Meidel and Scheibling, 1998; Pearse and Cameron, 1991; Walker et al., 2007), with seasonal changes in photoperiod (Bay-Schmith and Pearse, 1987; James et al., 2007; McClintock and Watts, 1990; Pearse et al., 1986b) and seawater temperature (Byrne, 1990;
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Guillou and Michel, 1993; Pearse and Cameron, 1991) proposed as the main controlling factors (Appendix A9). However, evidence that the nutritional status of the individual influences gonad production has come from both field studies (e.g., Harrington et al., 2007; Meidel and Scheibling, 1998; Pearse, 1969a,b) and laboratory experiments (e.g., Garrido and Barber, 2001; Meidel and Scheibling, 1999). Sea urchins use the gonad and gut as storage organs, meaning that gonads may be re-absorbed and gametogenesis may be altered or arrested during periods of stress (see reviews by Guillou et al., 2000; Lawrence and Lane, 1982). Despite the numerous papers correlating reproductive events with environmental parameters, the evidence for exogenous control of echinoid reproduction remains equivocal (Byrne, 1990; King et al., 1994; Pearse and Cameron, 1991). No single mediator can be consistently correlated with the reproductive cycles of all sea urchins (Appendix A9). It is likely that several factors are involved, or that different sea urchins respond to different stimuli (Piatigorsky, 1975). The major events during gametogenesis in echinoids have been well studied (Pearse and Cameron, 1991), and reproductive cycles have been delineated for many species, although the factors influencing gametogenesis, especially those that regulate the timing of events, remain poorly understood.
1.6. Deep-sea echinoderms In the marine environment, the timing of reproduction is usually controlled on two different temporal scales: a long scale associated with initiation and progression of gametogenesis, and a shorter scale associated with spawning. Factors that entrain seasonal cycles of gametogenesis in sublittoral areas include cyclic changes in the natural light regime (e.g., sunrise, sunset, changing day length, lunar cycle), and predictable variability in salinity, diet and energy availability (Giese and Pearse, 1974). Most of these periodic cues are not believed to operate at deeper depths, although reproductive periodicities have been observed in deep-sea species. James Orton (1920) was the first to propose the hypothesis that reproduction should not follow any periodical pattern in the constant thermal conditions of the deep sea. This view was not questioned until deep-sea seasonality and reproductive periodicity were documented after the 1960s (reviewed by Tyler, 1988). While echinoderms were among the first deepsea animals shown conclusively to display seasonal reproductive periodicity (Lightfoot et al., 1979; Schoener, 1968; Tyler et al., 1982a,b), it was later found that seasonal breeding is the exception in this group rather than the rule (see Table 12.6 in Young, 2003). Few seasonal breeders have been found in the Rockall Trough (NE Atlantic), where numerous species have been examined over many years, whereas the majority of species studied at bathyal depths on the Bahamian Slope breed seasonally (Young, 2003).
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Deep-water species with seasonal reproductive cycles presumably produce planktotrophic larvae, while continuous breeders produce non-planktotrophic larvae (Tyler and Young, 1992). Gametogenesis follows the same pattern as in shallow-water echinoderms, although species such as Echinus affinis with semi-continuous reproduction possess gonads with multiple cohorts of gametes, and the cycle spans over more than a year (Tyler and Gage, 1984a). Pain et al. (1982a) studied several asteroids from 2200 m depth and found that mature males remained in a state of constant ripeness, ready to shed sperm at any chance encounter with a female releasing ripe oocytes. Similar observations were made on Hymenaster membranaceus (Pain et al., 1982b), with no evidence of reproductive synchrony between or within female samples and males apparently ready to release sperm at any time. It appears that only a small number of oocytes reach maximum size at any one time; these are probably spawned intermittently, making room in the tubule for the further development of other oocytes. This pattern of reproduction, involving large egg size, low fecundity, and lack of seasonality is often presumed to be a function of the stable low temperature environment of the deep sea that has led to efficiency of reproduction (Clarke, 1979; Sanders, 1979; Southwood, 1977; Tyler et al., 1982b). Nevertheless, Tyler et al. (1982a) mentioned that preliminary observations of gametogenesis in a variety of deep-sea asteroids suggest that there is a distinct but variable pattern of oocyte growth in the main families represented. Although there is considerable habitat variation at great depths, some regions such as abyssal plains are presumably more uniform than most shallow-water habitats (Young, 2003). Nevertheless, seasonal changes that could possibly entrain reproductive cycles occur even at these depths, such as eddy kinetic energy, spring or summer falls of phytodetritus, and turbulence during benthic storms, though they remain untested as controllers of gametogenesis or spawning (Young, 2003). Aside from environmental stability, selective pressures that may influence life-history traits in the deep sea include low population densities, spatially uniform habitats, food limitation and extreme conditions associated with hydrothermal vents (Young, 2003).
2. Correlation with Exogenous Factors It is often stated that reproduction is timed according to environmental factors in order to maximize fertilization success and/or survival of the offspring. For this to happen, the individual should initiate gametogenesis before conditions become optimal, and be able to detect
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environmental changes that act as cues or zeitgebers which synchronize reproduction with the subsequent favourable conditions. These environmental changes could exert proximate exogenous control on reproduction, and need not be restricted to only one factor, but may consist of several factors which interact in synchronizing reproductive activities, although one factor may be dominant, at least under some circumstances (Giese and Pearse, 1974). Much effort has been expended in the search for those environmental factors that exert proximate control over discrete breeding periods in marine invertebrates. In spite of such effort, possible environmental factors controlling reproduction are poorly understood and their identification largely speculative, partly due to our incomplete understanding of how multiple and often overlapping environmental cycles can produce definite temporal patterns. Ideally, to determine the proximate and ultimate mediators of reproductive periodicities requires an independent analysis of each of the cycles (e.g., diel, tidal, semi-lunar, lunar, seasonal) to evaluate their respective roles in producing speciesspecific or population-specific patterns of reproduction (Yamahira, 2004). However, such complex studies are rarely undertaken and we are forced to stitch many small incomplete pieces of information together to obtain the best possible approximation. Appendixes A1, A3, A5, A7 and A9 summarize the exogenous factors that have been more or less convincingly correlated with gametogenesis in the five main extant classes of echinoderms.
2.1. Photoperiod and temperature Photoperiod and temperature are considered within the same section because they have been identified as the most probable proximate mediators of reproduction in echinoderms. However, they are often examined concurrently and sometimes not separated, since day length directly influences sea surface temperatures. Despite this intrinsic interrelationship, we have tried to distinguish between evidence of control via photoperiod/day length and via temperature whenever possible, especially for holothuroids and echinoids, on which most of the studies have been conducted. The inherent challenge was suitably summed up by Chia and Walker (1991), who stated that when natural populations are observed, investigators can only record seasonal variations in factors such as food supply, temperature, light intensity and salinity and try to find correlations with changes in the reproductive status of the specimens studied. Whether positive or negative, these relationships remain suggestive and the underlying causes are often unclear (Chia and Walker, 1991). Temperature has long been considered to be of major importance in the timing of the reproductive cycles of marine invertebrates. Living in the
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ocean with its tremendous specific heat, marine organisms are essentially buffered against the acute and unpredictable variations found in smaller bodies of water or in terrestrial environments. Orton’s (1920) classic paper pointed to seasonal changes of seawater temperature as the major environmental factor determining the timing of reproductive activity of marine animals. Sufficient correlative evidence was gathered over the following decades for Thorson (1946) to propose that Orton’s suggestion become a general rule. Orton (1920) showed that seasonally changing sea temperatures probably regulate the reproductive periodicities of many temperate species, leading him to postulate that in more stenothermal areas like the polar seas, animals would breed more or less continuously. In recent years, this statement has been proven inadequate for temperate and polar areas where clear seasonal patterns of reproduction can be observed, whereas there are many examples of aperiodic reproductive cycles closer to the equator. Pearse et al. (1986a) indicated that seasonally changing seawater temperatures are not likely to be very influential in controlling the timing of reproduction in species that live in areas where these temperatures undergo little seasonal change. Moreover, they noted that in areas submitted to substantial seasonal changes of temperature, the sequence of events involved in gamete production often seemed synchronized too precisely from place to place and year to year to be determined solely by changing seawater temperature. Nevertheless, convincing evidence of the influence of temperature on gametogenesis has recently been brought to light. Photoperiodic control of reproductive activities has been demonstrated in several species of echinoderms, though the mechanisms involved remain far from clear. Such timing has been observed in the sea urchins Strongylocentrotus purpuratus (Bay-Schmith and Pearse, 1987; Pearse et al., 1986b) and Eucidaris tribuloides (McClintock and Watts, 1990), as well as in several species of sea stars, including Pisaster ochraceus (Pearse and Eernisse, 1982; Pearse et al., 1986a), Asterias rubens (¼vulgaris) (Pearse and Walker, 1986) and many others (e.g., Pearse and Beauchamp, 1986; Pearse and Bosch, 2002; Xu and Barker, 1990a). Nonetheless, as will be shown below, most of the evidence to date is circumstantial or speculative at best, and convincing experimental work is still limited to a few asteroids and echinoids. 2.1.1. Crinoidea Only correlative data have been presented for crinoids. Holland et al. (1975) and Holland (1991) proposed that the early stages of gametogenesis in Oxycomanthus japonicus could be linked with shortening day length and decreasing sea surface temperature. A schematic model representation of the gametogenesis in this species suggested a correlation between the lowest winter temperature and the initiation of oocyte growth (Holland, 1981a). Similarly, Mladenov and Brady (1987) indicated that the re-initiation of
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gametogenesis in the Jamaican population of Nemaster rubiginosa in early fall may be correlated with shortening day length and increased seawater temperature. Nichols (1994) also stated that a decrease in seawater temperature and day length in August might influence the gametogenic cycle of Antedon bifida in the English Channel (UK). 2.1.2. Ophiuroidea Many studies of the reproductive cycle in ophiuroids have reported that breeding seasons may be influenced by ambient seawater temperature (reviewed by Hendler, 1991; McClintock et al., 1993), but the evidence remains tentative and somewhat ambiguous. Thorson (1934) studied Ophiocten sericeum in east Greenland, and suggested that the earlier maturation of inner-fjord populations may be correlated with the fact that ice breaks up earlier in spring and forms earlier in autumn in these locations than in the outer areas. However, Thorson’s conclusions with respect to the time course of reproduction in O. sericeum was later questioned by Pearse (1965) who re-interpreted the data to indicate that gametogenesis would take over a year, as observed in the asteroid Odontaster validus. Fenaux (1970) studied the timing of gametogenesis and spawning in the Mediterranean ophiuroid Amphiura chiajei. According to her work, the growth of the gonads appears to be correlated with increasing summer sea temperatures; however, changing thermal regimes were not identified as a possible regulating factor. A similar correlation was made by Bowmer (1982) who indicated that the onset of oocyte growth in Amphiura filiformis population coincided closely with the annual rise in seawater temperature in Galway (Ireland) (Fig. 2.1). He further suggested that the higher maturity index observed in 1980 could be due in part to slightly higher temperatures in August/September in concert with a massive plankton bloom reported that year. Tyler (1977) noted that Ophiura albida in the Bristol Channel (UK) had a short period of gamete production and spawned when the temperature exceeded 12.5 C. Yamashita and Iwata (1983) provided experimental evidence supporting the observation that gonadal growth in Amphipholis kochii from Japan could be initiated during periods of low temperature. They also found that gonadal growth was higher in individuals held at higher temperatures. A field study in Massachusetts (USA) revealed that Ophioderma brevispinum initiated slow gonadal growth in fall despite stable temperatures before and after this initiation (Hendler and Tyler, 1986). Similar observations were reported for O. brevispinum at Cedar Key (Florida, USA) when temperatures were at their lowest (Stancyk, 1974) and for Microphiopholis atra and Hemipholis elongata in Mississippi Sound, USA (Valentine, 1991a). The latter investigator added that a mean increase in gonad index was closely followed by an increase in mean near-bottom temperatures after gonadal growth was initiated. Temperature was also the only environmental variable to correlate
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Control of Reproduction in Echinoderms
Temperature
A
OC
15
S B
5 0
M J
A S O N D J 1979
F
M A
M J 1980
J
A
S O
Salinity
B B S
‰
30
J
10 0
Oxygen
C 10 ml/L
S B 0
Ml
D
Maturity index
6 5 4 3 2 1
Figure 2.1 Amphiura filiformis (Ophiuroidea). Relation of temperature, salinity and dissolved oxygen at surface (S) and bottom (B) of Galway Bay (Ireland) with the maturity index in males and females. Reprinted with permission from Bowmer (1982).
significantly with oocyte size in a study of the Antarctic brittle star, Ophionotus victoriae (Grange et al., 2004). Gounin and Richard (1992) suggested that temperature and food supply were the principal factors influencing gonad maturation in Ophiothrix fragilis from the Pas-de-Calais (France). According to Davoult et al. (1990), differences in gonad weight and index between populations of O. fragilis (Cap Gris-Nez and Roscoff, France), and between years in the population of the
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Dover Strait (UK), were linked to difference in environmental conditions, higher gonad index values being observed in June–July when the temperature was ca. 17 C. Moreover, in the Netherlands, Morgan and Jangoux (2002) found that increasing temperature seemed to influence gonadal growth in O. fragilis, specifically the maturation period, although they also believed that photoperiod might be important. Shirai and Walker (1988) proposed that the difference between lower winter and higher summer values of temperature may cause the release of a gonado-stimulating factor in O. fragilis. In the southern hemisphere, the only record of temperature-related gonad development is that of Astrobrachion constrictum in the Fiordland (New Zealand) which follows the progressive increase of seawater temperature and peaks in April–May (Stewart and Mladenov, 1995). In Monterey Bay (USA), different species of ophiuroids displayed maximal gonad maturity during periods of increasing (Ophiothrix spiculata, Amphiodia occidentalis) or decreasing (Ophiopteris papillosa) seawater temperatures (Rumrill, 1984). Rumrill (1984) suggested that the gametogenesis and gonadal growth of O. papillosa that begin in November in California (USA) may rely on increasing day length. Species of ophiuroids that exhibit seasonal reproductive patterns, such as those found along the north-eastern Pacific where seasonal temperature changes are minor, also may respond to day length (Rumrill and Pearse, 1985). 2.1.3. Holothuroidea The vast majority of investigations have made basic correlations with one or more environmental factors that seem to be fluctuating synchronously with gonad growth and gametogenesis. Some of the best correlative data have been gathered from temperate and polar regions, where marked seasonal regimes in temperature and photoperiod occur. The influence of temperature on gonad maturation has been observed in Apostichopus (=Stichopus) japonicus in Hokkaido, Japan (Tanaka, 1958). Furthermore, the more mature gametogenic stages in the sea cucumber Aslia lefevrei from Ireland coincide with low temperatures, high oxygen concentrations and reduced feeding activity, suggesting nutrient build up over the warmer months and use of these food reserves for general metabolism and gametogenic activity during the winter (Costelloe, 1985). A study of Stichopus mollis in New Zealand during a temperature anomaly revealed that lower seawater temperatures associated with the 1987 El Nin˜o extended the duration of the reproductive season and the size of the gonads, spawning occurring 2–3 months later than in 1986 (Sewell and Bergquist, 1990). Similar reasons were evoked to explain a delay in the reproductive period of Pseudechinus spp. between successive years in 1990–1991 (McClary and Barker, 1998).
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In eastern Canada, the active phase of gametogenesis in the phytoplankton-feeding species Psolus fabricii begins in January when seawater temperatures are near the freezing point and phytoplankton abundance is minimal (Hamel et al., 1993). Hence, the only notable environmental change occurring during the mid-winter onset of gametogenesis is increasing photoperiod. In fact, almost the entire active gametogenic cycle coincides with increasing day length and daily bright sunshine, peak maturity occurring when photoperiod is maximal (Hamel et al., 1993). After the onset of gamete synthesis, which is presumably in response to increasing day length, the major growth in gonadal tubule diameter and mass observed in March– April suggests that phytoplankton production and vernal warming control the level of gametogenic activity (Hamel et al., 1993). Similarly, gamete synthesis in the sea cucumber Cucumaria frondosa, which also occurs in eastern Canada, is initiated in early winter after the first increase in day length when food availability is low and temperature and salinity are constant, while the most intense phase of gametogenesis is associated with the abundance of food and rising temperature in early summer (Hamel and Mercier, 1995a, 1996a). The roles played by photoperiod, day length and temperature in holothuroid gametogenesis are less clearly established in the lower latitudes, where such environmental factors are usually assumed to be less variable, although this assumption is not always valid. According to Conand (1989), gonad maturation in several species of aspidochirotids from New Caledonia (Holothuria scabra, H. scabra versicolor, H. fuscopunctata, Actinopyga echinites, Thelenota ananas and Stichopus variegatus) is correlated with a rise in seawater temperature between September and November. The shift observed between some of the species could be due to local thermal variations (Conand, 1989). In the Philippines, gamete synthesis in H. scabra increases with temperature during summer and decreases at the end of the year when the temperature falls (Ong Che and Gomez, 1985). While an early study conducted in India implied that the annual reproductive cycle of H. scabra was best explained by salinity variation (Krishnaswamy and Krishnan, 1967), Conand (1989, 1993b) did not find any such correlation in New Caledonia, whereas temperature showed a plausible correlation during the warmest and coolest periods. Tuwo (1999) concurred that gametogenesis of H. scabra in Sulawesi (Indonesia) was under temperature control after observing two main periods of activity, the first one directly correlated with the increase of seawater temperature during the dry season and the second during the decrease of seawater temperature in the rainy season. However, the peak of the reproductive season (September–October) occurred towards the end of the dry season in the Solomon Islands, implying that both salinity and temperature fluctuations may regulate the seasonal reproductive cycle of H. scabra (Battaglene, 1999a). It has also been suggested that both factors act as proximal cues responsible for synchronization
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and regulation of the seasonal reproductive pulses in H. scabra in the Philippines (Ong Che and Gomez, 1985). Recently, the possible influence of temperature on oogenesis of this species has also been noted in the south-western Indian Ocean (Rasolofonirina et al., 2005). Peak values of the gonad index in Actinopyga mauritiana occurred during different months in 2 consecutive years in Guam, being 2–3 months later in 1988 than in 1989 (Hopper et al., 1998). Although the investigators did not measure seawater temperatures and relied on global data, 1988 was a La Nin˜a year (i.e., cold water event), which they suggested could explain the reproductive lag ( June–July) compared with 1989 (March–April). In the Solomon Islands, A. mauritiana displays an annual cycle during which the initiation of gametogenesis is correlated with decreasing photoperiod (Ramofafia et al., 2001). The onset of gametogenesis in Holothuria fuscogilva in the same location coincided with the inflection point in March when the light period became shorter than the dark period, also implying that photoperiod may entrain gonad development (Ramofafia et al., 2000). The same assumption was made by Tehranifard et al. (2006) for Stichopus herrmanni in Kish Island (Iran). Gametogenesis of Holothuria leucospilota in the Cook Islands was synchronous and appeared to be related to changes in photoperiod and sea temperature, as spawning conditions were reached during maximal values for both variables (Drumm and Loneragan, 2005). A severe El Nin˜o event in 1997/1998 resulted in a 3–4 C increase in sea temperature in Rarotonga in October 1998, causing spawning to occur 2 months earlier (November– February) than in previous years ( January–April) (Drumm and Loneragan, 2005). Previously, Ong Che (1990) had noted that the rising seawater temperature may be the factor responsible for the initiation of gametogenesis in the same species in Hong Kong. 2.1.4. Asteroidea While most studies in this class provide correlative evidence, a few convincing experimental investigations have been published that lend credence to the influence of photoperiod on the gametogenesis of asteroids. In a basic study of Pisaster ochraceus on the West coast of the USA, Feder (1956) simply reported that a decline in temperature was accompanied by growth of the gonads. Smith (1971) demonstrated experimentally the role played by temperature and illumination on the reproduction of Leptasterias pusilla from Monterey Bay (USA). Low numbers of individuals were admittedly used for the experiment but a direct temperature effect was not apparent, suggesting that the lengthening photoperiod may play some role in either inducing spawning or lowering the threshold of the stimulus necessary for spawning. Dehn (1980b) combined laboratory and field studies of Luidia clathrata in Florida (USA) to show that both temperature and food supply seemed to be
Control of Reproduction in Echinoderms
21
correlated with the reproductive activity of this species. She noted that the gametogenic activity began in fall when temperatures were rapidly decreasing from their summer maxima, and suggested that this decrease may trigger metabolic processes associated with activation of gametogenesis. Rumrill (1989) studied Patiria (as Asterina) miniata in Barkley Sound (BC, Canada) and observed that the population exhibited seasonal cycles in pyloric and gonad indices. Seasonal breeding in Barkley Sound differs substantially from the breeding cycle found in populations in Monterey Bay (CA, USA) (Davis, 1985; Farmanfarmaian et al., 1958; Gerard, 1976; Nimitz, 1971). Cyclic growth of gonads in P. miniata from Barkley Sound corresponded with seasonal changes in temperature and with changes in the abundance of prey (Rumrill, 1989). Aseasonal organ indices observed in populations of P. miniata from California (USA) may reflect a more constant food supply and a poorly defined annual temperature cycle (Gerard, 1976; Harrold and Pearse, 1980). The sea star Cosmasterias lurida exhibited a long spawning period in Argentina when seawater temperature reached high values and photoperiod started to decrease (Pastor-de-Ward et al., 2007). However, seawater temperature was not significantly correlated with gonad index, suggesting that it was not directly related to gametogenesis and spawning. In contrast, photoperiod did show a significant correlation to gonad indices, indicating an influence on reproductive processes (Pastor-de-Ward et al., 2007). Pearse and several collaborators demonstrated experimentally that the photoperiod cycle played a major role in the timing of the annual reproductive cycle in several species of asteroids. Pearse and Eernisse (1982) showed that longer day lengths in the spring and summer in California (USA) entrained the initiation of gametogenesis and gonadal growth to begin in the fall in Pisaster ochraceus. Furthermore, oogenesis in P. ochraceus was initiated 6 months earlier, in mid-winter, following laboratory exposure to long day lengths (>12 h) (Fig. 2.2). However, the out-of-phase oogenic cycle was not sustained for more than a few months in specimens exposed to long day lengths, indicating that short day lengths may be required as well to maintain later phases of oogenesis. On the other hand, a fixed photoperiod (either short, neutral or long) had no effect on gametogenesis, implying that the gametogenic cycle is under the control of an endogenous annual rhythm (Pearse et al., 1986a). Pearse and Beauchamp (1986) found that individuals of Leptasterias sp. maintained for almost 3 years under two different photoperiod regimes under controlled laboratory settings shifted out-of-phase with respect to in-phase animals. Pearse and Walker (1986) demonstrated a major role for photoperiod on the reproduction of another species of sea star, Asterias rubens (¼vulgaris), in this case on the north-eastern coast of the USA. They mentioned that it was tempting to conclude that control of reproduction by photoperiod is a general phenomenon, at least for shallow-water species.
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Annie Mercier and Jean-Franc¸ois Hamel
Laboratory photoperiod
Field
6 Mo out of phase
Ambient Hours
16
Daylength
12
Gonad index
20
Body wet wt (kg)
15
Pyloric cecum index
8 +++ ∗∗∗
∗
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∗∗
++
10 5 0
Pyloric ceca
15 10 5 0
1.0
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0.5 0 1979
1980
1979
1980
1979
1980
Figure 2.2 Pisaster ochraceus (Asteroidea). Changes in day length, gonad index, pyloric caecum index, and total wet body weight in field and laboratory populations held under ambient (in-phase) and 6-month out-of-phase photoperiod (mean SE). There were no differences between values for males and females in any of the samples. Continuous lines: individuals collected in and maintained from December 1978. Dashed lines: individuals collected in and maintained from June 1979. Asterisks and crosses: laboratory observations of spawning in individuals collected in December 1978 and June 1979, respectively. Reprinted with permission from Pearse and Eernisse (1982).
Regulation of oogenesis in Sclerasterias mollis was studied by Xu and Barker (1990a) in New Zealand using an experimental design similar to that of Pearse and Eernisse (1982). Well-fed individuals maintained 6 months out-of-phase of the ambient photoperiod underwent a gradual shift in the breeding periodicity that was apparent in the gonad index, the size of oocytes and the steroid levels after a few months. Interestingly, individuals maintained in-phase did not entirely follow the field population, exhibiting differences in gonad index and oocyte size, possibly because of the different
Control of Reproduction in Echinoderms
23
light, temperature and feeding regimes (Xu and Barker, 1990a). Nevertheless, the two experimental groups displayed clear out-of-phase reproductive rhythms in response to the photoperiod regime, while their feeding, body size and pyloric caecum index remained unaffected. Pearse and Bosch (2002) worked with the sea star Odontaster validus in McMurdo Sound (Antarctica) and demonstrated the photoperiodic control of gametogenesis in this species with a well-defined gametogenic cycle throughout its circumantarctic distribution (Grange et al., 2007; Pearse, 1965, 1966). Gametogenesis in specimens kept on a photoperiod 6 months out-of-phase with ambient (constant light in winter, constant dark in summer) switched within a year to the out-of-phase regime, unlike sea stars kept on an ambient photoperiod or collected from the field. Gametogenesis in sea stars kept in constant light or on a 12L:12D photoperiod appeared to be maintained more or less continuously, whereas day lengths >12 h apparently stimulated gametogenesis. In contrast, gametogenesis in sea stars kept in constant darkness was comparable to that in sea stars kept under ambient photoperiod or collected from the field, suggesting an underlying circannual rhythm (Pearse and Bosch, 2002). Bouland and Jangoux (1988) used a comparative investigation of gonad cycles in Asterias rubens under laboratory controlled conditions and in the field in the Netherlands to show that the sensitivity of gonad synthesis to environmental factors differs according to whether the gonads are initiating their gametogenesis or are at the pre-spawning stage. Gametogenesis initiation and spawning were either suppressed or delayed when individuals were held in static seawater for at least 2 months. Bouland and Jangoux (1988) suggested that the effect of these manipulations was more marked when asteroids were initiating gametogenesis. In contrast, individuals in which gametogenesis had begun showed no difference between natural field conditions and laboratory conditions. Byrne et al. (1997) have shown that the reproductive cycle of Asterias amurensis introduced in Tasmania, Australia (Byrne et al., 1997) is analogous to that of this species in Japan (Hatanaka and Kosaka, 1959; Ino et al., 1955), populations occurring at similar latitudes on either side of the equator (42–43 S and 35–41 N, respectively). Patterns of gametogenesis and spawning exhibited correlations with temperature and photoperiod cycles in both regions, though reproductive timings were 6 months out-of-phase. In Japan, gonads were mature in winter ( January) and spawning occurred between late winter and early spring (February–May) when temperatures ranged from 5 to 12 C (Hatanaka and Kosaka, 1959; Ino et al., 1955; Kim, 1968). In Tasmania, gonads were fully developed in the austral winter ( June–July) and spawning occurred between late winter and spring ( July– October) at seawater temperatures of 10–13 C (Byrne et al., 1997). It has been suggested that although temperature would be expected to have an influence given the correspondence of northern and southern seawater
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Annie Mercier and Jean-Franc¸ois Hamel
temperature regimes, gametogenic events would be most reliably entrained by the seasonally varying photoperiod, since recovery and spawning coincided with the longest and shortest days of the year, respectively (Byrne et al., 1997). A study of Coscinasterias muricata at Governor’s Reef (Australia) revealed that significant events in the gametogenic cycle of females were associated with changes in photoperiod (Georgiades et al., 2006). A peak in pyloric caecum index coincided with the March equinox, while the gonad index was low, whereas a nearly opposite pattern occurred at the September equinox. The pyloric caecum and gonad indices were almost equal around the solstices. The summer solstice was proposed as an environmental cue for the onset of spawning as specimens appeared to spawn or be ready to spawn around this period both in 1999 and 2000 (Georgiades et al., 2006). Noticeable peaks in progesterone concentration in the pyloric caeca of the females were observed in the months immediately following the March and September equinoxes, suggesting a possible relationship (Georgiades et al., 2006). The authors also stated that gametogenesis appeared to start with the highest seawater temperatures (March), and that the spawning event coincided with the coldest seawater temperatures (September). 2.1.5. Echinoidea Pearse and Cameron (1991) suggested that temperature and photoperiod greatly influence gonad development in sea urchins. Photoperiod is the most frequent factor correlated with initiation of gametogenesis and nutritive phagocyte utilization in echinoid species (Pearse et al., 1986b; Walker and Lesser, 1998), though the specific action of the photoperiodic cue remains unclear (Walker et al., 2007). Nevertheless, evidence for the role of temperature is rapidly accumulating (Agatsuma, 2007; Agatsuma and Nakata, 2004; Cochran and Engelmann, 1975; Ito et al., 1989; Sakairi et al., 1989; Viktorovskaya and Matveev, 2000; Yamamoto et al., 1988; Yatsuya and Nakahara, 2004). Given the abundance and possibly confusing nature of the data on the photoperiodic and/or temperature control of gametogenic cycles in sea urchins, for the sake of clarity this section has been further subdivided into three sub-sections (‘‘Temperature’’, ‘‘Photoperiod’’, ‘‘Uncertain influence of temperature vs photoperiod’’). (a) Temperature Populations of Strongylocentrotus purpuratus along a latitudinal gradient exhibited very low correlation coefficients between seawater temperature and gonad development at 18 stations sampled along the west coast of the USA (Boolootian, 1966). In Oregon, gonad growth of S. purpuratus began in July, when temperature was high but variable due
Control of Reproduction in Echinoderms
25
to upwelling, and continued as temperature declined in autumn; spawning occurred at the time of lowest temperature, but did not coincide with either a particular temperature or an abrupt change (Gonor, 1973a). Similarly, Pearse (1981) found that the reproductive cycle of S. purpuratus and S. franciscanus from areas with contrasting temperature regimes did not diverge. Experimental trials conducted by Garrido and Barber (2001) with S. droebachiensis from Maine (USA) revealed that well-fed sea urchins attained similar gonad index values within 12 weeks at both 3 and 12 C, indicating that gonad growth in this species may be independent of temperature. In S. franciscanus, holding temperatures did not have any effect on the gametogenic development of captive specimens, which was similar to that of specimens from the field in California (USA) (McBride et al., 1997). Nevertheless, latitudinal gradients in gonad maturation have been noted in many species and are often perceived as evidence of the effect of temperature. For instance, populations of Diadema setosum near the equator seem to breed year long, whereas those living in subtropical areas where seasonal temperature patterns occur, have restricted summer spawning periods (Hori et al., 1987; Pearse, 1968a; Tuason and Gomez, 1979). Yonge (1940) proposed that species of tropical marine invertebrates could be categorized according to lower and/or upper sea temperatures that might limit their reproductive activity. He included D. setosum of the Indo-Pacific among the species that reproduce whenever sea temperatures are above ca. 25 C, and this inclusion has been supported by later work (Pearse, 1974; Tuason and Gomez, 1979). Iliffe and Pearse (1982) found that gonads of D. antillarum from Bermuda increased in size in spring in 1979 and 1980 as temperature rose above 20 C; gonad size then fluctuated erratically until the final drop in late fall or early winter after sea temperatures fell below 20 C. Although the latter study indicates that reproduction of D. antillarum may be restricted to periods when sea temperatures rise above ca. 20 C in Bermuda, the relatively low gonad indices found when sea temperatures exceeded ca. 25 C in August and September suggests that higher temperatures may also inhibit gonadal growth. In Curac¸ao and the Virgin Islands, D. antillarum is apparently ripe all year long, with a peak gonad index in winter and early spring (Randall et al., 1964). Lessios (1981) also reported that D. antillarum did not display any evident seasonality in Panama, where mean sea temperatures range between 26 and 28 C (Hendler, 1979). Reproduction of this species appears more restricted in Barbados, where spawning coincides mainly with minimum seawater temperatures (ca. 26 C) in winter and spring (Lewis, 1966). Gonadal growth and spawnings occurred mainly in late fall and winter on the Florida Keys (Bauer, 1976), when seawater temperature was below ca. 25 C. According to Pearse (1968a), D. setosum and Echinometra mathaei from the Indo-Pacific respond to sea temperature since
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Annie Mercier and Jean-Franc¸ois Hamel
reproduction occurred when temperatures were above 25 C for D. setosum and 18–20 C for E. mathaei. Yatsuya and Nakahara (2004) found that the reproductive cycles of Anthocidaris crassispina from Wakasa Bay ( Japan) were almost synchronous between two different habitats they studied, and suggested that the reproductive cycles may be controlled by seawater temperature. Seawater temperature was also suggested to play an important role in gonad maturation of Pseudocentrotus depressus, Hemicentrotus pulcherrimus and A. crassispina whereas photic conditions (continuous light, continuous darkness, out-of-phase photoperiod) was not (Ito et al., 1989; Sakairi et al., 1989; Yamamoto et al., 1988). Furthermore, there are several reports of experimentally induced gametogenesis out-of-season in echinoids that experience marked seasonal changes in sea temperature (Khotimchenko, 1982; Sakairi et al., 1989; Townsend, 1940; Yamamoto et al., 1988). Conflicting evidence exists for triggering and inhibiting gametogenesis using both colder and warmer temperatures. Viktorovskaya and Matveev (2000) found that when the seawater temperature fell to 0 C in December, the development of gametes in populations of Strongylocentrotus intermedius on the Primor’e Coast (Russia) slowed down. In spring, when the temperature increased to 1.5–4 C, gametes at different stages of development were observed. Finally, in June, the rate of gametogenic development increased as the seawater temperature reached 10 C. Vaschenko et al. (2001) showed that lower temperatures in summer months could slightly retard gametogenesis in S. intermedius. A recent study in the south-western North Sea revealed a high level of gametogenic synchronization among individuals of Echinocardium cordatum and a nearly perfect recurrence of the same reproductive cycle over 3 consecutive years (Nunes and Jangoux, 2004). This investigation suggests that a marked drop in seawater temperature followed by a regular temperature increase would initiate gametogenesis in this species. Gametogenesis in Pseudocentrotus depressus was induced several months early by holding animals in the laboratory at 20 C, a temperature coinciding with the onset of gametogenesis in the field after a decrease from summer highs of ca. 30 C (Yamamoto et al., 1988). According to Masaki and Kawahara (1995), a decrease in temperature can advance gonad maturation of P. depressus by a month. Other investigations have determined that gonad maturation in P. depressus is promoted when individuals are kept at a constant seawater temperature of 19–20 C, but not at 13 C (Noguchi et al., 1995; Yamamoto et al., 1988). Noguchi et al. (1995) further reported that gonad maturation in the adult sea urchins was enhanced by a rise in temperature to 25 C from February to June, and then a constant seawater temperature of 20 C after July. As in Strongylocentrotus purpuratus (see below), gametogenesis in P. depressus thus appears to be inhibited by higher temperatures. In contrast, gametogenesis in Anthocidaris crassispina occurred
Control of Reproduction in Echinoderms
27
in mid-summer and could be inhibited by holding specimens continuously at low temperatures of 15 C, and triggered several months earlier by maintaining them at 20 or 25 C (Sakairi et al., 1989). In Hemicentrotus pulcherrimus, gametogenesis normally occurs in fall and early winter when the sea temperature is below 20 C; gamete growth was suppressed when the animals were held at 20 C (Yamamoto et al., 1988) or 15 C (Sakairi et al., 1989). Gonad maturation could only be initiated by a change from high (ca. 25 C) to low (ca. 15 C) seawater temperature and was inhibited at constant seawater temperatures (Ito et al., 1989; Sakairi et al., 1989). According to Ito et al. (1989), adult H. pulcherrimus that had experienced a period of rising seawater temperature to 26 C could mature and spawn ca. 45 days after the temperature was again lowered to 15 C. Seasonal changes in gonad index and gonad developmental stage indicated that spawning in H. pulcherrimus in Oshoro Bay (Hokkaido, Japan) peaked in April (Agatsuma and Nakata, 2004), later than in southern Honshu (November–April) and roughly at the same time than at Matsumae (April–June) (Agatsuma, 2007). Agatsuma (2007) concluded that seawater temperature played a major role in gonad maturation of H. pulcherrimus, whereas light did not. Gonad maturation was initiated by a decrease in seawater temperature to ca. 15 C (Agatsuma and Nakata, 2004) as observed in the southern regions (Agatsuma, 2007). Gametogenesis of the sea urchin Strongylocentrotus purpuratus was inhibited in the laboratory at temperatures above 17 C, and no gravid specimens were found when the summer sea temperature exceeded 17 C in southern California, USA (Cochran and Engelmann, 1975). Sea urchins held at normal winter temperature in the laboratory delayed spawning by nearly 2 months compared with populations in the field. Moreover, Pearse (1981) kept animals at three experimental temperatures (7, 14, 21 C), and found that gametogenesis was completely inhibited at 21 C. Nonetheless, when Pearse (1981) reviewed synchronization of gametogenesis, he found that while gametogenesis and spawning of S. purpuratus were inhibited at temperatures above 17 C, temperature changes had not been shown to play any role in synchronizing reproductive activities. Another example of suppressed gametogenesis at high temperatures was observed in individuals of Eucidaris tribuloides lacking mature spermatozoa when held at 30 C for 2 months (Lares and McClintock, 1991). (b) Photoperiod Evidence for photoperiodic control of gametogenesis in echinoids was first presented half a century ago. Giese (1959a) mentioned the possibility in an early review and a few years later Boolootian (1963) reported that the testes of Strongylocentrotus purpuratus developed mature gametes only when the sea urchins were held under long day lengths and subsequently exposed to short day lengths. While subsequent
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Annie Mercier and Jean-Franc¸ois Hamel
short-term experiments with adults of S. purpuratus did not reveal any influence of photoperiod (Cochran and Engelmann, 1975; Holland, 1964), Leahy et al. (1978, 1981) found that gametogenesis in this species was nearly continuous when the animals were maintained in the dark at relatively low temperatures and provided with excess food. Although experiments to separate the role of light, food, and temperature were not carried out, trials and observations under variable food and temperature conditions suggested that these factors had little influence on the timing of gametogenesis in this species (Pearse, 1981). In some species gametogenesis appears to be controlled by short day lengths, e.g., Strongylocentrotus purpuratus (Bay-Schmith and Pearse, 1987; Pearse et al., 1986b), Eucidaris tribuloides (McClintock and Watts, 1990), Strongylocentrotus droebachiensis (Walker and Lesser, 1998), Paracentrotus lividus (Shpigel et al., 2004), whereas others are considered long-day species, for example, Psammechinus miliaris (Kelly, 2001). Pearse et al. (1986b) eventually confirmed the photoperiodic control of gametogenesis in Strongylocentrotus purpuratus during an 18-month study. Using field collected juveniles from Baja California (Mexico), they measured both oocyte size frequency and incorporation of 3H-labeled thymidine by the testes, showing that animals held 6 months out-of-phase with ambient photoperiod shifted their gametogenic cycle accordingly, in contrast to field and captive animals held under ambient photoperiods (Pearse et al., 1986b). Other experiments showed that individuals of S. purpuratus that were submitted to two successive 6-month periods of fall–winter photoperiods (<12 h of light daily) displayed continuous gametogenesis, whereas those held in two successive spring–summer photoperiod regimes (>12 h of light daily) failed to undergo substantial gametogenesis for over a year (Pearse et al., 1986b). Bay-Schmith and Pearse (1987) compared the gametogenic response of Strongylocentrotus purpuratus (California, USA) under different photoperiod regimes of fixed and seasonally changing day length. Quantification of gametogenic activity in enzymatically disaggregated ovaries and in histological sections of testes revealed that sea urchins were sensitive to both fixed and variable day lengths. After 1 year at fixed short day (8L:16D) or fixed neutral day (12L:12D), the gonads were ripe and undergoing gametogenesis, as were gonads of animals reared with varying photoperiod and sampled during the short-day phase of the cycle (Bay-Schmith and Pearse, 1987). Under fixed long day (16L:8D), the gonads did not contain significant numbers of gametes and had the constitution of gonads found in animals reared at varying photoperiod and sampled during the long-day phase of the cycle (Bay-Schmith and Pearse, 1987). Such findings suggest that gametogenesis in this species is sensitive to the absolute number of hours of light or dark. Photoperiods of 12 h or shorter promote growth of oocytes to full size and their maturation into ova in females, and the production of
Control of Reproduction in Echinoderms
29
spermatocytes and spermatozoa in males. In contrast, a regime of 15–16 h of light inhibits vitellogenesis and spermatogenesis. In S. purpuratus, gametogenesis is therefore likely under control of a critical day length of less than ca. 12 h (Bay-Schmith and Pearse, 1987). In the Gulf of Maine, the initiation of gametogenesis in Strongylocentrotus droebachiensis appears to be triggered by the onset of shortening day length in the fall (Walker and Lesser, 1998). The authors suggested that the changing photoperiod in autumn might lead to activation of oogonial or spermatogonial mitosis directly through a mitogen-induced mechanism or, alternatively, might result in mobilization of nutrients from nutritive phagocytes which would then stimulate gonial cell mitosis (Walker and Lesser, 1998). In the field, gonial cell mitosis occurs as seawater temperature drops from 17 to 13 C in autumn; in the experimental study of Walker and Lesser (1998), it occurred as temperature rose from 11 to 14 C. Low temperatures are probably required to complete vitellogenesis in this species. Bo¨ttger et al. (2006) have studied the effects of invariant summer versus progressing ambient (fall/winter) photoperiod regimes on the gonads of Strongylocentrotus droebachiensis from north-eastern USA. They observed that males and females maintained on commercial feed under invariant photoperiod did not initiate annual gametogenesis (Fig. 2.3), although some production of new spermatozoa was noted (Walker et al., 2005). Male and female gonads reached large sizes due to proliferation of nutritive phagocytes. In the ovaries, a few residual primary oocytes remaining from the previous year also grew (Walker et al., 2005). Dumont et al. (2006) showed that once gametogenesis was initiated in Strongylocentrotus droebachiensis spawning could not be halted by photoperiod regulation (Fig. 2.4). In other species, individuals collected from the wild and held under experimental conditions retained their internal reproductive calendars for long periods of time (Leahy et al., 1981). Dumont et al. (2006), however, suggested that the rate at which echinoids progress through the various developmental stages of gamete synthesis can be affected by the photoperiod regime. By the end of the 12-week experiment, sea urchins in all fed photoperiod treatments had completely spawned out, but the proportion of individuals in the recovering and growing stages were markedly different, the 16-h daylight treatment group having by far the greatest percentage of individuals in the growing stage (Dumont et al., 2006). A more direct influence of light was observed in Strongylocentrotus nudus from eastern Russia by Evdokimov et al. (2001) who found that light of wavelength 720 nm activated gonad development, while at 520 nm it had a suppressive effect by decreasing the oogonial and spermatogonial content without disturbing the cellular structure. In Stylocidaris affinis from the Gulf of Naples (Italy), the discrete reproductive cycle and the lack of seasonal fluctuations in temperature, salinity and other factors support photoperiod as the major factor affecting the
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Figure 2.3 Strongylocentrotus droebachiensis (Echinoidea). Representative ovary (A) and testis (B) of individuals maintained for 5 months at constant photoperiod showing predominance of nutritive phagocytes and few gametes. A few residual primary oocytes (RO) are present (but no new ones) near the ovarian wall and limited numbers of new spermatozoa (arrows) are evident between the expanded nutritive phagocytes, as are spermatogonial mitoses among the spermatogenic cells (SC). Representative ovary (C) and testis (D) of individuals maintained for 5 months at ambient photoperiod showing growing residual (RO) and new (NO) primary oocytes in nutritive phagocyte incubation chambers. The testicular lumen is filled with new spermatozoa and the nutritive phagocytes (dark granules containing cells) are reduced in size with only a slender strand of cytoplasm connecting them to the testicular wall. Circle denotes spermatogonial mitosis (SC); C, coelom. Scale bars ¼ 50 mm. Reprinted with permission from Bo¨ttger et al. (2006).
31
Control of Reproduction in Echinoderms
0 week 100
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Figure 2.4 Strongylocentrotus droebachiensis (Echinoidea). Mean frequency (%) of fed sea urchins at various gametogenic stages at each sampling date for the five photoperiod treatments: 0D, 0 h darkness per day; 8D, 8 h darkness per day; 16D, 16 h darkness per day, 24D, 24 h darkness per day, Ambient, ambient photoperiod with natural light. Numbers in parenthesis indicate the sample size. Reprinted with permission from Dumont et al. (2006).
reproductive cycle (Holland, 1967). The marked annual fluctuations in photoperiod probably influence reproduction in the sea urchins from Bocca Piccola, where the water is clear and receives sufficient light at 70 m to support growth of macro-algae. However, Holland (1967) estimated that the long periods of oocyte growth and spermatocyte accumulation did not closely follow photoperiod, nor did the short periods of spawning, initiation of oocyte growth, and initiation of spermatocyte accumulation. Even when photoperiod does not exert a direct influence on sea urchin reproduction, it may serve as a periodic reference point to synchronize an endogenous reproductive rhythm (Holland, 1967). Photoperiod could also have an important indirect effect on reproduction by influencing the quantity and quality of the algal food available to the sea urchins (Holland, 1967). McClintock and Watts (1990) studied Eucidaris tribuloides from Florida (USA) under two variable and two fixed photoperiod regimes at a constant
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Annie Mercier and Jean-Franc¸ois Hamel
temperature for a year to demonstrate the role of photoperiod in the regulation of gametogenesis. Individuals maintained 6 months out-ofphase with the ambient photoperiod did not become reproductively mature until March, indicating that gametogenesis was delayed until the day length decreased during the artificial winter photoperiod. Sea urchins held under fixed long days (15L:9D) delayed gametogenesis for the entire year; and only ca. 20% of them developed mature gonads. Sea urchins held under fixed short days (9L:15D) produced mature gametes throughout the year, and mature gonads were found in ca. 60% of these individuals. These observations suggest that short days or long nights enhance and entrain gametogenic development in E. tribuloides (McClintock and Watts, 1990). On the other hand, gametogenesis in Japanese echinoid species is apparently not under photoperiodic control (Sakairi et al., 1989; Yamamoto et al., 1988). Groups of laboratory-reared Pseudocentrotus depressus all developed ripe gonads at about the same time when held under ambient, out-of-phase, constant dark, and constant light conditions. Similarly, laboratory-reared Hemicentrotus pulcherrimus developed ripe gonads in early winter, and laboratory-reared Anthocidaris crassispina developed mature gonads in midsummer, whether they were held in constant dark, constant light, or ambient conditions. These authors suggest that the timing of gametogenesis is regulated by an endogenous temporal program and critical changes in sea temperature (Sakairi et al., 1989; Yamamoto et al., 1988). For details, see sub-section Temperature above.
(c) Uncertain influence of temperature versus photoperiod In some species, the respective roles played by temperature and photoperiod are somewhat unclear, either because of the incomplete or inaccurate environmental data available, or because experimental results are ambiguous. The influence of temperature and light on the reproductive cycle of Echinometra mathaei is not well understood. Based on the prediction of Pearse and Phillips (1968) that a minimum temperature (18 C) is required for the onset of gametogenesis, spawning in Kenya would be expected to occur year round (Muthiga, 2005) as it does in Rottnest Island, Western Australia (Pearse and Phillips, 1968), where seawater temperatures range from 18 to 22 C (Hodgkin et al., 1959). However, along the Kenyan coast, which is characterized by temperatures of 24–31 C, E. mathaei exhibits a restricted reproductive cycle (Muthiga, 2005), as in areas with a wider range of temperatures, such as Seto and Okinawa, Japan (Arakaki and Uehara, 1991; Onoda, 1936), Wadi el Dom, Gulf of Suez (Pearse, 1969b), and the eastern coast of South Africa (Drummond, 1995). Paradoxically, populations of E. mathaei from the northern Red Sea, closer to the equator, spawn throughout the year (Pearse, 1969b). Thus, seawater temperature is
Control of Reproduction in Echinoderms
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apparently not the main factor controlling gametogenic development of this species along the coast of Kenya (Muthiga, 2005). In Centrostephanus rodgersii from New South Wales (Australia), an increase in the rate of gametogenesis in May and the onset of breeding in June–July occurred at all locations studied over 9 of latitude (Byrne et al., 1998). This reproductive synchrony suggests that reproductive processes are controlled by exogenous factors operating at all locations, the most probable one being photoperiod according to the authors. They state that gametogenesis is probably initiated in April as days become shorter than nights and argue that while gamete production and spawning occur as sea temperature is decreasing, this factor would not provide a uniform cue at all the locations studied (Byrne et al., 1998). Furthermore, given the contrasting winter temperatures to which northern and southern populations are exposed, C. rodgersii likely does not require a temperature threshold to initiate reproductive processes, though temperature may still act on gamete storage and length of the spawning period (Byrne et al., 1998). Experimental trials conducted in Scotland have shown that the reproductive cycle can be altered by the manipulation of photoperiod or temperature regimes in Psammechinus miliaris (Kelly, 2001). The author wished to investigate the effect on gametogenesis of removing a specific environmental cue (either increasing spring days or increasing seawater temperatures). In the absence of increasing spring day lengths, the proportion of males and females producing mature gametes decreased significantly, indicating that reproduction in this species is influenced by photoperiod (Kelly, 2001). However, short days did not prevent the onset of gametogenesis, and no demonstrable difference in the developmental stages was found until late spring (Kelly, 2001). Cold water (in winter) was apparently important for the completion of oogenesis and less critical for spermatogenesis. Significantly fewer females in the temperature-controlled treatment produced mature oocytes, whereas there was no significant difference in the numbers of mature males found among the temperature treatments (Kelly, 2001). The investigator further determined that the temperature cue required by P. miliaris was between 6.2 and 9.8 C. The European echinoid Paracentrotus lividus has been studied in several regions, as well as under laboratory conditions, generating abundant yet occasionally conflicting results. On the west coast of Ireland, the species exhibits maximal periods of gonadal growth coinciding with decreasing sea temperatures and a day length of <12 h, suggesting that temperature and photoperiod may both influence gonad development (Byrne, 1990). In Southern Brittany (France), the cues responsible for the onset of gonadal growth and gametogenesis were also difficult to determine (Spirlet et al., 1998). Reproductive cycles resumed in late summer and gonad index values subsequently increased as both temperature and day length decreased (Spirlet et al., 1998). Due to prolonged exposure to sun at low tide,
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populations in tide pools were intermittently subjected to significantly higher temperatures than subtidal populations, suggesting that temperature was not a major regulating factor. Photoperiod was a more probable regulator of the reproductive cycle, although some individuals were mature a month earlier in one year than in the following year (Spirlet et al., 1998). The fixed photoperiod cycle of 14L:10D and the chosen temperature (ca. 18 C) seemed to work well for the captive maintenance of Paracentrotus lividus collected on the west coast of Portugal (Luis et al., 2005). Broodstock maturation was achieved throughout the year without unwanted spontaneous spawnings (Luis et al., 2005). Grosjean et al. (1998) were also able to maintain mature P. lividus throughout the year at 18–20 C, but in total darkness. More recently, Shpigel et al. (2004) presented evidence that temperatures of 18–22 C enhanced gonad growth in P. lividus from the Red Sea but that gametogenesis was controlled by photoperiod; long days reduced gametogenic rate while short days increased it. On the other hand, Spirlet et al. (2000) found temperature to be the main determinant of gonad development in P. lividus reared in the laboratory from broodstock collected in Brittany (France). The data of Luis et al. (2005) on the best combination of temperature and photoperiod to achieve continuous gonad growth and gametogenesis with P. lividus are ambiguous. It seems that any photoperiod is suitable for captive P. lividus broodstock within the temperature range 18–22 C, as long as the diet is appropriate (Luis et al., 2005).
2.2. Lunar cycle Evidence of lunar periodicity is much more abundant for spawning (see Section 2.5 in Chapter 3) than for gametogenesis, even though lunar spawning rhythms almost certainly reflect synchronized lunar gametogenic rhythms. 2.2.1. Crinoidea Holland (1981a) conceived a speculative model of spawning periodicity in Oxycomanthus japonicus according to which the final differentiation of gametes that occurs in the last week before spawning is triggered either by the full or new moon. This would explain the occurrence of gamete shedding at the last or first quarter of the moon, respectively. 2.2.2. Ophiuroidea Although his study was not rigorous, J. E. Smith (1940) believed that spawning of Ophiothrix fragilis in the UK might be influenced by lunar phases. It has also been suggested that Ophiopholis aculeata and Ophiura robusta in the White Sea spawn in synchrony with specific lunar phases (Mileikovsky, 1960, 1968 in Hendler, 1991).
35
Control of Reproduction in Echinoderms
100 90
Aggregation (%)
80
Pairs Trios Mass aggregation Spawning
70 60 50 40 30 20 10 0 February
April
March
May
Months (1998)
Figure 2.5 Holothuria scabra (Holothuroidea). Aggregative behaviour (lines) and spawning (triangles) of adults in outdoor tanks between February and May 1998. Open circles represent full moons and dark circles new moons. Reprinted with permission from Mercier et al. (2000a).
2.2.3. Holothuroidea Mercier et al. (2000a) noted that the lunar phase played a role in the prespawning pairing behaviour and gametogenic synchrony of Holothuria scabra populations in the Solomon Islands (Fig. 2.5). 2.2.4. Echinoidea Iliffe and Pearse (1982) observed a lunar reproductive rhythm in Diadema antillarum from Bermuda which appeared to resemble that found in populations on the Florida Keys (USA), where Bauer (1976) observed smaller gonads nearer the time of the full moon than at the adjacent new moons. Centrostephanus coronatus also followed synchronous gametogenic rhythms with a lunar pattern in southern California (Kennedy and Pearse, 1975; Pearse, 1972).
2.3. Food availability and nutrient storage Food availability and assimilation are required if an organism is to produce large masses of viable gametes. This is especially true in those invertebrates that utilize a major proportion of all stored metabolic energy for gamete production; food reserves must be assimilated and stored some time before the actual breeding or gametogenic season begins (Smith, 1971). While nutrition can influence reproduction in various ways, laboratory and field studies have yet to demonstrate that changes of food levels can affect the timing of reproduction in echinoderms (Eckelbarger and Watling, 1995). There is no
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inherent reason to expect echinoderms to cue their reproductive cycles to seasonal food pulses. Two possible control mechanisms of food supply on gametogenesis have been proposed by Hilbish and Zimmerman (1988), who demonstrated delayed gametogenic cycles in mussels with higher rates of nitrogen excretion and poorer nitrogen budgets; either the rate of energy assimilation regulates the rate of gamete development, or some critical level of energy acquisition and storage must have been reached before gametogenesis is initiated. Most of the evidence provided on the influence of food availability on the reproduction of echinoderms is gathered from correlations between gonad maturity and either seasonal or inter-annual magnitude of planktonic production. Alternately, comparisons between gonad maturation and nutrient storage/depletion can be used to interpret the translocation and importance of dietary input in reproductive processes. The ability of echinoderms to accumulate food reserves in various body tissues presumably helps lengthen the period during which nutrients for gamete production can be obtained (Lawrence and Lane, 1982). The competition between reproductive and somatic production in food-limited conditions can vary according to the environment and the population (Ebert, 1968; Harrold and Pearse, 1980; Kenner, 1992; Thompson, 1983). Sites of synthesis of vitellogenic nutrients are largely unknown for most echinoderms (Shirai and Walker, 1988). In crinoids, nutrient reserves are found in accessory cells within the genital haemal sinus of the gonad and in adjacent cells of the body wall of pinnules (Holland and Kubota, 1975). Ophiuroids do not possess specialised organs where long-term accumulation and storage of nutrients can occur. In holothuroids, nutrients are probably derived from accumulated reserves in the gonads and body wall (David and MacDonald, 2002). In asteroids, most nutrients used in gametogenesis are stored in large digestive organs called pyloric caeca, whereas in echinoids the majority of nutrients used in gametogenesis are stored within versatile, nutritive phagocytes (Shirai and Walker, 1988). In all cases where specialised sites exist for nutrient storage, significant quantities of nutrients are undoubtedly also delivered directly to the gonads as individuals feed (Shirai and Walker, 1988). Apart from unsubstantiated claims by early investigators (Madsen, 1961; Moseley, 1880), Hansen (1975) was among the first to suggest that seasonal variation in primary production in the euphotic zone may induce reproductive periodicity in organisms living at abyssal depths. Recent studies of the downward flux of surface-derived organic matter from primary production supports the possible occurrence of a seasonal pulse into the deep sea correlated with the spring phytoplankton bloom (Billett et al., 1983; Deuser and Ross, 1980; Deuser et al., 1981; Honjo, 1982), leading to the hypothesis that sinking organic matter could entrain seasonal reproduction in echinoderms (Tyler and Gage, 1980a; Tyler et al., 1982b). It is now known that the
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periodic deposition of organic matter to the deep-sea benthos is a widespread phenomenon in all regions where seasonal surface production is observed (e.g., Baldwin et al., 1998; Beaulieu and Smith, 1998; Billett et al., 1983; Grassle and Morse-Porteous, 1987; Rice and Lambshead, 1994; Smith et al., 1996; Thiel et al., 1989; Tyler, 1988). Variability of food supply on a seasonal or annual basis, especially critical compounds such as carotenoids, may have a considerable effect on reproduction, particularly in deposit-feeding invertebrates (Hudson et al., 2003). Indeed, evidence of seasonal reproduction coupled with seasonal input of phytodetritus has been provided for several deep-sea echinoderms (Tyler, 1988). Recently, the links between phytodetritus as a food source and the way variability in supply may influence the reproductive processes of benthic invertebrates have been documented for many deep-sea species, including asteroids (Benitez-Villalobos et al., 2007; Tyler and Pain, 1982; Tyler et al., 1993), echinoids (Campos-Creasey et al., 1994; Gage et al., 1986) and holothuroids (Wigham et al., 2003a). Young (1991) reported that some asteroids and echinoids begin their reproductive cycles roughly as food pulses reach the deep ocean floor and that several species have been photographed while feeding on the layer of detrital plankton. The circumstantial evidence is therefore compelling. While no definitive experimentation of this seasonalflux theory has been attempted, the idea is gaining support among the scientific community concerned with the biology of deep-sea organisms (Young, 1991). 2.3.1. Crinoidea Nichols (1991) suggested that the observed variation in reproductive activity in Antedon bifida might be caused by environmental factors, such as sudden increases in the levels of plankton on which the animal feeds. It is well established that the numbers of nutritive phagocytes can fluctuate over an annual cycle (Holland and Kubota, 1975; Raven, 1961; Wourms, 1987). In Oxycomanthus japonicus, histological evidence of nutrient accumulation and depletion in male and female gonadal accessory cells and the body wall suggests a massive transfer of stored nutrients to the germinal cells (Holland and Kubota, 1975). Presumably, a large amount of the material stored in the spherules supports the development of germinal cells during the advanced stages of gametogenesis (Holland, 1991). A similar accumulation of nutrients occurs in Comatella nigra and Comanthus parvicirra (Carpenter, 1884). In contrast, Mladenov (1986) indicated that accessory cells were absent from the ovaries of the ‘‘continuous’’ breeder Florometra serratissima. However, the high energy content of the viscera has also been suggested to be an energy source during gamete synthesis in Promachocrinus kerguelensis (McClintock and Pearse, 1987). Nichols (1994) indicated that these cells were present at least in some Antedon bifida throughout the year,
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but were more often absent during summer and autumn (i.e., after spawning) and were usually present during the build-up of mature oocytes. Roux and Pawson (1999) observed that the absence of genital pinnules in the deep-sea crinoid Hyocrinus foelli in the Pacific Ocean could be related to cyclic reproduction in a marginal environment depending on a seasonal food supply. 2.3.2. Ophiuroidea In reviewing the available literature, Hendler (1991) found evidence that the availability of food may be an ultimate or proximate factor affecting the reproductive cycle of ophiuroids, although he pointed out that in most instances food appeared to be a selective advantage or ultimate factor, rather than a real cue. To our knowledge, no further information has been forthcoming to explain the control of ophiuroid maturation and the triggering of spawning. The biochemical pathways through which nutrients are used by developing gametes, the nature of the stored substances (if any) and the storage sites remain virtually unknown. Patent (1969) stated that the resting period of the reproductive cycle of Gorgonocephalus eucnemis stemmed from the exhaustion of the nutrient stores available for gonadal growth. In the Bristol Channel (UK), Tyler (1976) found contrasting results for gonadal growth during the spring phytoplanktonic bloom in the planktivorous Ophiura albida and the earlier gonadal ripening of Ophiura ophiura, which is a generalist and therefore less dependent on seasonal food resources. The massive spring increase of gonad production in O. albida occurred during the period of maximum food consumption (Tyler, 1977), suggesting that food availability is a limiting factor in gonad production. Bowmer (1982) indicated that the beginning of the annual maturation in Amphiura filiformis coincided with the spring plankton bloom in Galway Bay (Ireland). Increased food has also been associated with increased gonad mass in A. filiformis and A. chiajei from Sweden (Sko¨ld and Gunnarsson, 1996) and Ophiocoma echinata from Florida (USA) (Pomory, 1997; Pomory and Lawrence, 1999). In addition, Rumrill (1984) indicated that changes in diet influence gonadal growth and regression in broadcast-spawning echinoderms. He proposed that drifting kelp and other associated detritus may provide an abundant source of food for the cryptic Ophiopteris papillosa (California, USA). Thus, the predictable cycle of increasing food availability initiates gametogenesis in this species in the late fall. Moreover, a more rapid oocyte growth was observed in cohorts of Ophiothrix fragilis (Dover Strait, France) that initiated gametogenesis in spring and summer than in cohorts that were maturing over the less productive fall and winter months (Davoult et al., 1990). Bourgoin and Guillou (1990) concluded that a minimum of food was necessary for survival of Acrocnida brachiata. Below this threshold, gonad growth did not occur. Just above it, gonad growth could occur but somatic
Control of Reproduction in Echinoderms
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growth was limited. Above a second threshold, both gonad and somatic growth were possible. According to Grange et al. (2004), the clear inter-annual variability in the reproductive effort of Ophionotus victoriae could be linked with the extent and magnitude of the preceding organic sedimentation event around the Antarctic Peninsula. All individuals of O. victoriae observed had developing gonads and the gonad index increased throughout the austral winter and spring, peaking during October and November and decreasing during December. However, considerable inter-annual variations were noted in the patterns. Although a direct relationship between reproductive effort and chlorophyll production could not be established, a connection was noted between sedimentation events at Rothera (Antarctica) and ophiuroid reproductive characteristics (Grange et al., 2004). The authors suggested that the brittle stars were predisposed to a high fecundity following a season of high organic flux, and vice versa. The scale and duration of annual sedimentation events, possibly modulated by patterns of ice cover and thickness, is likely to play a role in the following year’s reproductive success (Grange et al., 2004). Many deep-sea species (i.e., Ophiura ljungmani, Ophiocten gracilis, Ophiocten hastatum) show comparable seasonal patterns of gamete maturation based on histological evidence; gametogenesis is initiated in late winter or early spring, oocyte growth accelerating after the arrival of the flux of phytodetritus to the deep-sea floor (Gage et al., 2004; Sumida et al., 2000; Tyler and Gage, 1980b). Tyler and Gage (1980a) reported that although the deep sea is a more or less physically aseasonal environment the discrete, seasonal reproductive periodicity exhibited by Ophiura ljungmani may be a result of periodic nutrient increases owing to rapid transfer of particles from the surface zone to the deep, as implied by Schoener (1968). Tyler (1977) believed that food availability was an important factor in the control of the gametogenic cycle in ophiuroids. Support for these early hypotheses has been strengthening ever since. Gage and Tyler (1982) did not find any annual periodicity in the oocyte size frequency distribution of the deep-sea brittle star Ophiomusium lymani. The authors reconciled this with the inferred pattern of annual recruitment by postulating a seasonal cycle in the survival of post-larvae. This may be a response to annual fluctuation in downward flux of food particles from the surface, reflecting the seasonal cycle of primary production. Incidentally, a study of gonad development in Ophiacantha bidentata from 2200 m in the Rockall Trough (NE Atlantic) revealed a reproductive cycle in some females but distinct inter-individual asynchrony, suggesting that populations of this protandric hermaphrodite reproduce year round (Tyler and Gage, 1982). The gametogenic pattern observed in Ophiura hastatum from 4800 m in the Porcupine Abyssal Plain (NE Atlantic) is almost identical to that of O. ljungmani from 2900 m in the southern Rockall Trough (Tyler and
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Gage, 1980b), and very similar to that in O. gracilis from 900 m on the adjacent Hebridean continental margin (Sumida et al., 2000). Gametogenesis is initiated in late winter/early spring with oocyte growth accelerating after the arrival of the flux of phytodetritus to the deep-sea floor. Spawning appears to take place in January/February of each year, a timing coincident with other species known to show seasonal gametogenic cycles in the deep NE Atlantic (Tyler and Gage, 1984a; Tyler et al., 1982b). 2.3.3. Holothuroidea The body wall, intestinal tract and gonad of holothuroids are identified as potential areas for nutrient storage during the feeding season (Feral and Doumenc, 1982; Jayasree et al., 1994; Prim et al., 1976; Smith, 1981). Smiley et al. (1991) considered it unlikely that nutrients derived entirely from ongoing feeding activity could support vitellogenesis in holothuroids. The abundant microvilli on the surface of the ovarian peritoneal epithelial cells presumably take up yolk precursor glycoproteins from the coelomic fluid and later transfer them into the genital haemal sinus (Smiley et al., 1991). At the time, there was a general consensus that the genital haemal sinus must play a key role in conveying nutrients to growing oocytes (Smiley et al., 1991; Walker, 1982a). The haemal space presumably functions as a transport pathway for the coelomic fluid and the coelomocytes carrying gases and nutrients to developing gametes (Krishnan and Dale, 1975; Reunov et al., 1994; Smiley and Cloney, 1985). Histochemical observations have revealed seasonal reproductive and nutritional cycles in the tropical species Holothuria scabra (Krishnan, 1968). Autosynthesis of protein occurred in the ovaries, whereas the testes seemed to obtain protein from the gut. Lipids from the intestine were apparently used during oogenesis and lipids from the testicular epithelium during spermatogenesis (Krishnan, 1968). Carbohydrates were mainly found in the connective tissues of the gut and body wall (Krishnan, 1968), from where they could be distributed by means of the perivisceral fluid, as suggested by studies on the digestive tracts of other species like Leptosynapta inhaerens (D’Agostino and Farmanfarmaian, 1960), Leptosynapta inhaerens and Holothuria tubulosa (Farmanfarmaian, 1963). Conversely, nutrients stored in the gonads and gametes of H. scabra are catabolized during food deprivation (Morgan, 1999). The sea cucumber Cucumaria frondosa, which exhibits discrete seasonal reproductive and feeding activities in eastern Canada, is a good candidate for biochemical and correlative studies (Hamel and Mercier, 1998; Singh et al., 1999). Hamel and Mercier (1996b) found that there was no difference in gonad development and maturity index between starved and fed individuals during a 20-month experiment. Similarly, gonad development in C. frondosa in the Bay of Fundy persisted during the fall–winter non-feeding period (Singh et al., 2001). Thus, while food availability is likely to influence gonad
Control of Reproduction in Echinoderms
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development, no direct correlation between feeding and gametogenic activity has been noted in C. frondosa, supporting the hypothesis that holothuroids may continue gametogenic activity throughout the year irrespective of their seasonal feeding rhythm. Biochemical studies tend to confirm this ability. For instance, David and MacDonald (2002) described differences in the composition of tissues in C. frondosa that were attributed to the annual reproductive cycle, and suggested that the accumulation of reserves in the body wall during the feeding period served to support bodily functions and reproduction during non-feeding months. Nevertheless, higher levels of gonad protein and glycogen were measured when animals were actively feeding, suggesting that energy can be stored in gonads directly from feeding (David and MacDonald, 2002). The fact that glycogen decreased in both gonad and body wall after cessation of feeding implied that both tissues support the reproductive cycle over the fasting period. No clear pattern could be detected in lipids, which were abundant in the gonad and body wall, regardless of the season (David and MacDonald, 2002). Concurrently, with the onset of gametogenic development in C. frondosa (Hamel and Mercier, 1996a), protein and glycogen content of the gonads were higher during the post-spawning period, when energy reserves were accumulating (David and MacDonald, 2002). Histological data suggest that a similar cycle occurs in other temperate species. In Eupentacta chronhjelmi from Aoshima Island ( Japan), the gonad wall was thickest in September for females and October for males, when the gonad index was at its peak (Catalan and Yamamoto, 1994). Depletion of reserves in the gonad wall was observed during the rapid final stages of vitellogenesis in females and completion of spermatogenesis in males; gametes were spawned in October–December (Catalan and Yamamoto, 1994). The gonadal tubule wall of Psolus fabricii from eastern Canada also thickens during the period of gametogenic inactivity from autumn to midwinter (Hamel et al., 1993). Gametogenesis is likewise preceded by a thickening of the tubule wall in a variety of echinoderms, presumably due to an accumulation of reserves for gametogenesis (Gonor, 1973b; Pearse, 1969b). Overall increases in gonadal size may result from storage of materials in the tubule wall, for example, Aslia lefevrei (Costelloe, 1985) although increased gonadal mass is not always concurrent with gonad wall thickening, for example, P. fabricii (Hamel et al., 1993). Recent observations by Singh et al. (2001) support the contention that the haemal system functions as a delivery path and/or storage area for nutrients. In male Cucumaria frondosa, the haemal space is largest in May– July immediately after spawning and is a good indicator of spawning (Singh et al., 2001). The role of nutritive phagocytes in the resorption and recycling of residual gametes has been documented in holothuroids (Costelloe, 1985; Smiley and Cloney, 1985; Tanaka, 1958) and other echinoderms (Fenaux,
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1972b; Holland and Giese, 1965; Liebman, 1950). It is assumed that nutritive phagocytes transform reserves to dissolved compounds which are later used for gamete production (Holland and Giese, 1965). According to gonad indices and histological studies, fecundity is greater in winter than in summer months in the sea cucumber Amperima rosea from the Porcupine Abyssal Plain (NE Atlantic), although no clear evidence of seasonal or episodic reproductive events was found (Wigham et al., 2003a). Males were always mature, possessing spermatozoa, whereas most oocytes were of an intermediate size, either at the late pre-vitellogenic or early vitellogenic stage of development (Wigham et al., 2003a). Wigham et al. (2003a) therefore proposed that development of vitellogenesis leading to episodic spawning might be dependent on environmental factors, the most likely stimulus being food supply. The differences in gut pigment profiles suggest that several species of deposit-feeding holothuroids can partition the same phytodetrital food source, possibly providing a mechanism for maintaining the high diversity of deposit feeders at abyssal depths (Wigham et al., 2003b). Many deep-sea deposit feeders, including A. rosea, preferentially select the fresh components of phytodetritus (Billett, 1991), perhaps favouring the ingestion of organically rich and useful compounds, in this case carotenoid pigments that are important for vitellogenesis. The ovarian tissue of Amperima rosea and four other deep-sea holothuroids (Pseudostichopus villosus, Psychropotes longicauda, Paroriza prouhoi, and Oneirophanta mutabilis) sampled prior to the spring phytoplankton bloom had similar carotenoid profiles, with a dominance of zeaxanthin, echinenone and b-carotene, which are important compounds for reproductive success in echinoderms (Wigham et al., 2003b). However, the ovaries of A. rosea contained much higher concentrations of these pigments, implying that this species may be able to quickly exploit any change in the composition of phytodetritus and convert that advantage into a successful reproductive event (Wigham et al., 2003b). A. rosea has small oocytes (<200 mm) and high fecundity, and it exhibits an apparent arrest in vitellogenesis until resources become available (Wigham et al., 2003a). Hence, production of large numbers of viable gametes may depend on the availability of essential carotenoids after a change in the composition of the phytodetrital flux (Wigham et al., 2003b). Conversely, P. longicauda has the largest recorded oocytes of any echinoderm (ca. 4400 mm) and presumably undergoes direct larval development (Tyler and Billett, 1987), probably requiring large amounts of reproductively important carotenoids to permit vitellogenesis. Levels of b-carotene measured in its ovarian tissue were lower than in A. rosea and O. mutabilis, which could explain the lower fecundity of P. longicauda (Wigham et al., 2003b). In a comparable study, Hudson et al. (2004) suggested that the different patterns of temporal variation in fatty acid composition observed in several species of deep-sea holothuroids (A. rosea, Bathyplotes natans, Deima validum, P. longicauda, O. mutabilis, P. prouhoi,
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Benthogone rosea, Laetmogone violacea and Paroriza pallens) were possibly linked to different reproductive strategies exhibited by these species. A recent study of the Antarctic deep-sea holothuroid Protelpidia murrayi revealed that the onset of vitellogenesis in this species may be linked to the arrival of phytodetritus on the sea bed (Galley et al., 2008). A slightly different pattern was observed in another elasipod species, Peniagone vignoni, which appears to produce mature gametes year round with a more intense peak during higher detritic food pulses in summer. On the other hand, no correlation between reproduction and the seasonal deposition of organic matter has been noted in abyssal holothuroids of the family Deimatidae (Tyler and Billett, 1987), despite seasonal changes in the quantity of organic matter reaching the seabed in the NE Atlantic (Billett et al., 1983; Lampitt, 1985; Rice et al., 1986; Riemann, 1989). Hence, while deimatids occur primarily in regions where the input of organic matter to the deep-sea floor is either known or expected to vary seasonally, the correlation with reproduction remains tenuous (Tyler and Billett, 1987). 2.3.4. Asteroidea The pyloric caecum is a nutrient processing and storage organ unique to the Asteroidea (Farrand and Williams, 1988; Lawrence, 1985, 1987; Lawrence and Lane, 1982). Evidence suggests that it acts as a nutrient storage center for glycogen, fats, and proteins (Greenfield et al., 1958; Jangoux and van Impe, 1977; Nimitz, 1971). An inverse relationship between gonad and pyloric caecum indices is commonly observed in asteroids (Barker and Xu, 1991b; Boolootian, 1966; Byrne, 1992; Chia, 1969; Chia and Walker, 1991; Ferguson, 1964; Franz, 1986; Georgiades et al., 2006; Giese, 1966; Lawrence, 1973; Lawrence and Lane, 1982; Menge, 1975; Nimitz, 1971; Oudejans and Van Der Sluis, 1979; Rubilar et al., 2005; Ventura et al., 1997), suggesting nutrient transfer from pyloric caeca (where reserves would accumulate) to gonads during gametogenesis (Giese, 1966; Lawrence and Lane, 1982). (a) Indirect evidence from shifts in nutrient storage Farmanfarmaian et al. (1958) postulated that the pyloric caeca of Pisaster ochraceus from the western USA store nutrients during months of active feeding and later mobilize them and transfer them to the gonads. Chia and Walker (1991) reviewed several papers (Barker, 1979; Crump, 1971; Davis, 1985; Ferguson, 1974; Jangoux and van Impe, 1977; Lawrence, 1973; Lowe, 1978; Mauzey, 1966; Menge, 1970; Nichols and Barker, 1984a,b; Pearse, 1965; Town, 1980; Tyler et al., 1982b) and pointed out that many of them support the results of Farmanfarmaian et al. (1958), demonstrating seasonal changes in the size of the gonads, inversely related to the size of the pyloric caeca. Mauzey (1966) found a functional relationship between seasonal changes in feeding frequency and pyloric caecum and gonad indices in Pisaster
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ochraceus collected on the west coast of the USA. Active feeding preceded growth of the pyloric caeca, which in turn preceded gonadal growth. Cyclic changes in the size and histological appearance of the gonad and pyloric caeca were observed in this species (Mauzey, 1966). The gonads were smallest in the fall and grew during the winter to a maximum in the late spring, when spawning occurred. The changes in pyloric caecum size were approximately inverse to those in the gonads. Similar relationships among these variables have been found in Leptasterias hexactis from the same region (Menge, 1970). Nimitz (1971) showed that the pyloric caeca of Pisaster ochraceus increased in size from June to December in California (USA) and decreased in size during the spring at the time when gonads were growing. This inverse relationship suggests the withdrawal of material from the caeca for use by the gonads. In contrast, the pyloric caeca of Patiria miniata seemed to remain fairly constant in size during the breeding season (Nimitz, 1971). In both species, Nimitz (1976) indicated that prolonged starvation resulted in the failure of the gonads to achieve their normal size increment. Smith (1971) demonstrated experimentally that normal feeding during the summer months was necessary to accumulate materials utilized in subsequent gametogenesis in the brooding Leptasterias pusilla from the west coast of the USA. He also showed that there was a decrease in the size of the pyloric caeca coincident with rapid oocyte growth. However, Boivin et al. (1986) did not observe this inverse relationship in the sea star Leptasterias polaris in eastern Canada, though this may have been due to the way they sampled the population. In Luidia clathrata along the coast of Florida (USA), Dehn (1980a) reported that the peak of pyloric caecum development corresponded to the onset of gametogenesis and the peak of gonad development to the minimum in digestive gland size. Oudejans et al. (1979) indicated that the pyloric caecum index of Asterias rubens was high during the pseudo-resting stage of the ovaries and decreased gradually during ovarian growth. Moreover, Barker and Nichols (1983) observed that the well-defined gonad cycle of A. rubens from southern England showed an inverse correlation with the pyloric caecum index. Specimens from the sites they studied showed considerable variation in gonad size. Grice and Lethbridge (1988) showed that reproductive events in male and female sea stars Patiriella gunnii in south-western Australia were closely synchronized and pyloric caecum and gonad indices inversely related. A reduction in the pyloric caecum index at this time may have reflected the redirection of stored products into gamete formation. Similarly, an annual decrease in the weight of the pyloric caeca relative to gonadal growth has been shown in P. gunnii and P. calcar in south-eastern Australia (Byrne, 1992), which might indicate a transfer of stored nutrients to the gonads to support seasonal gametogenesis. The inverse and partially inverse
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relationships between the organ indices of P. gunnii and P. calcar, respectively, suggest that gonadal growth of P. gunnii may be more dependent on caecal reserves than that of P. calcar (Byrne, 1992). During gametogenesis, Patiriella pseudoexigua seems to utilize the energy from the body wall, drawing additional energy reserves from the pyloric caeca as the spawning season approaches (Chen and Chen, 1992). Chen and Chen (1992) suggested that the prolonged period of oogenesis in P. pseudoexigua may be due to a requirement to accumulate large amounts of energy to fuel the complex process of oogenesis. Barker and Xu (1991b) found that the gonad and pyloric caecum indices in both female and male Sclerasterias mollis in New Zealand had an inverse relationship, an accumulation of nutrients in the pyloric caeca occurring during summer and early autumn. They suggested that both the timing of the reproductive cycle and the duration of the stages varies slightly from year to year probably in response to environmental factors such as the availability of food. Rubilar et al. (2005) observed a clear annual cycle in the pyloric caeca in the sea star Allostichaster capensis in Chubut (Argentina) and a reciprocal relationship with gonad indices, supporting the conclusion that pyloric caeca have a storage function. Gonad indices displayed an annual cycle, with peak development in August (winter) and spawning in September (spring). Wasson and Klinger (1994) also observed that the pyloric caeca indices of Asterias forbesi decreased from March until spawning ceased in July, implying an energy transfer from the pyloric caeca to the gonad. In a study of Coscinasterias muricata at Governor’s Reef (Australia), a peak in pyloric caecum index coincided with the March equinox, while the gonad index was low, whereas a nearly opposite pattern occurred at the September equinox (Georgiades et al., 2006). The pyloric caecum index and gonad index were almost equal around the solstices. A similar inverse relationship had previously been noted for the same species, C. calamaria (¼muricata), in New Zealand (Crump and Barker, 1985). Although an inverse relationship between gonad and pyloric caecum indices is commonly observed, not all sea stars with seasonal reproduction display this trend (Carvalho and Ventura, 2002) and evidence from the literature is somewhat contradictory. This may be explained by the fact that the pyloric caecum index is also indicative of the nutritional state of individuals, and food availability may thus influence the relationship between the sizes of the gonads and pyloric caeca (Lawrence and Ellwood, 1991; Miller and Lawrence, 1999). When food is scarce, gonadal and somatic growth will both be low to zero; if food is moderately abundant, somatic and gonadal growth will be temporally displaced and if food is abundant, an inverse relationship between indices will be observed. However, it has been presumed that if food is abundant year-round, the gonads may not be as dependent on the long-term nutrient storage
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capabilities of the pyloric caeca (Harrold and Pearse, 1980; Xu and Barker, 1990b). For instance, in northern Patagonia (Argentina), males of Cosmasterias lurida showed a weak reciprocal relationship between gonad and pyloric caecum indices, whereas there was no correlation between lipids and proteins of pyloric caeca and gonads but a positive correlation for carbohydrates, suggesting that both organs simultaneously accumulated carbohydrates and that there was no nutrient transfer in males (Pastorde-Ward et al., 2007). Females of C. lurida did not display a reciprocal relationship between indices, and biochemical analysis confirmed the assumption that no transfer of nutrients was occurring (Pastor-de-Ward et al., 2007). Similarly, Franz (1986) did not observe an inverse relationship between gonad and pyloric caecum in Asterias forbesi in Long Island (NY, USA). The author indicated that the presence or absence of a reciprocal relationship between pyloric caeca and gonads would largely depend on the relative timing of energy-demanding processes in relation to energy intake. Therefore, if energy provided by food was sufficient to sustain gametogenesis, the storage role of the pyloric caeca would be minimised (Franz, 1986). However, the absence of an inverse relationship between gonad and pyloric caecum indices may also reflect the utilization of organic material from the body wall during gametogenesis (Nichols and Barker, 1984b,c). Cyclic changes in the lipid content of asteroids have often been correlated with the reproductive cycle (Boolootian, 1966; Ferguson, 1975, 1976). Oudejans et al. (1979) showed that neutral lipids were accumulated in the pyloric caeca of Asterias rubens before being transferred to the ovaries during reproduction. Falk-Petersen and Sargent (1982) also demonstrated cyclical changes in lipid contents in Ctenodiscus crispatus, Asterias lincki and Pteraster militaris in northern Norway. They proposed major roles for certain lipids in the development of the large lecithotrophic eggs of asteroids. It has also been suggested that well-developed haemal sinuses can store nutrients for subsequent transfer to the germ cells (Chia, 1968; Walker, 1980). Ferguson (1984) and Beijnink and Voogt (1984) suggested that circulation within the fluid-filled ‘‘perihaemal’’ coelomic channels might be primarily responsible for nutrient translocation, the haemal tissues functioning principally as storage reservoirs. Follicle cells may also play an important role in nutrient transfer. In Sclerasterias mollis, as in other asteroids, successful growth and differentiation of oocytes depends on the existence and maintenance of ovarian follicles (Walker, 1982a). The genital haemal sinus of S. mollis, however, enlarges soon after spawning occurs, instead of at the beginning of vitellogenesis or the end of the spermatogenic phase (Barker and Xu, 1991b). This suggests that initial accumulation of nutrients in the genital haemal sinus of S. mollis may be directly from ingested food but that as the cycle continues, reserves may be mobilized from storage in the pyloric caeca and body wall to the gonads. On the other hand, efficient utilization of recycled substances
Control of Reproduction in Echinoderms
47
from the intense phagocytic activities may enhance the development of gametes in both females and males (Barker and Xu, 1991b).
(b) Direct relationship with feeding Some studies have predicted that gametogenic activity and particularly vitellogenesis in asteroids depend directly on feeding. Comparative studies of Odontaster validus (Pearse, 1965) and Patiriella regularis (Crump, 1971) indicate that gametogenic output may be related to the abundance of food. In particular, Crump (1971) examined two populations of P. regularis in New Zealand and found that the timing of the reproductive events was similar in all cases, although there were marked differences between populations in amplitude of gonad and pyloric caecum indices. Crump (1971) concluded that low indices resulted from a shortage of suitable food. Pearse (1965) studied Odontaster validus in two areas in Antarctica (McMurdo Station and Cape Evans). He noted a clear difference in summer phytoproduction between the two locations resulting in O. validus being bigger, more numerous and exhibiting a darker body wall colour in the more productive area of Cape Evans. Despite this difference in food abundance and the higher fecundity of O. validus at Cape Evans, the two populations exhibited synchronous reproductive periodicities. Pearse (1965) argued that given the distinct regimes at the two locations, light and food apparently did not play any role in the synchronization of gametogenesis, at least in quantitative terms. However, he suggested that apart from slight seasonal variations in temperature and salinity, qualitative changes in phytoproduction may be important (Pearse, 1965). Worley et al. (1977) found that the time of maximum activity in both male and female reproductive cycles was positively correlated with the period of active feeding in the sea star Leptasterias tenera in Block Island Sound, on the east coast of the USA. Shick et al. (1981) found that reproduction in Ctenodiscus crispatus was aperiodic in Maine, with several superimposed periods of increased intensity. They interpreted the observed pattern as a manifestation of a continuously available food source and to an adaptation to a seasonally predictable rain of phytodetritus, as the increased intensity of reproduction corresponded precisely with spring and fall blooms of phytoplankton, which may provide sudden clear bursts of richer, less refractory and more accessible food at the sediment–water interface. In contrast, the experimental results of Bouland and Jangoux (1988) with Asterias rubens from the Netherlands support previous assertions, indicating that starvation does not affect the growth and biochemical composition of developing gonads in asteroids ( Jangoux and van Impe, 1977; Lawrence, 1973). The investigators found that the course of gonad development was similar in both field animals and experimentally starved individuals,
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suggesting that reproduction in A. rubens has a greater priority than somatic maintenance during gametogenesis. (c) Pulses of organic food to the deep sea In a study of Dytaster grandis from the Porcupine Abyssal Plain (NE Atlantic), Tyler et al. (1990) observed that the availability of labile organic material appeared to fuel vitellogenesis during summer and fall. Later, Tyler et al. (1993) examined the diets of two sympatric species of sea stars, Bathybiaster vexillifer and Plutonaster bifrons, from ca. 2200 m in the Rockall Trough (NE Atlantic) to determine whether diet could influence their respective reproductive patterns. In B. vexillifer, which exhibits non-seasonal breeding, the diet showed a high prey diversity index, whereas the diet of the seasonally breeding P. bifrons had a significantly lower prey diversity. Furthermore, the organic carbon content of the sediment residue in the stomach of P. bifrons displayed a seasonal cycle, while no seasonality was detected in B. vexillifer (Tyler et al., 1993). The Porcupine Sea Bight and the Porcupine Abyssal Plane (NE Atlantic) are subjected to significant seasonal changes in surface productivity, leading to a strong pulse of phytodetritus to the seabed between April and September (Rice et al., 1994). Benitez-Villalobos et al. (2007) suggested that adults of Henricia abyssicola utilize the energy source provided by this phytodetritus, which is reflected in the developing oocytes, the May peak being followed by a marked drop in gonad index, probably indicating an increase in spawning between June and July. In contrast, seasonality was not observed in the reproductive biology of three deep-sea asteroids (Hyphalaster inermis, Styracaster chuni, and Styracaster horridus) from the Porcupine Abyssal Plain, the Madeira Abyssal Plain, and the northwest African slope (RamirezLlodra et al., 2002). Oogenesis was similar in all three species at the three locations, with the continuous presence of a small complement of large oocytes. The males had a permanent supply of ripe spermatozoa in the lumen of the testes. There were no seasonal variations in gonad and pyloric caecum indices or fecundity in any of the species (Ramirez-Llodra et al., 2002). The authors suggested that a chance encounter between a male and a female would stimulate spawning in the male, enhancing fertilization success in a low density population (Ramirez-Llodra et al., 2002). Such a strategy has been suggested for other abyssal asteroids (Pain et al., 1982b; Tyler et al., 1984). 2.3.5. Echinoidea There is no general agreement that diet or nutritional factors play a role in truly regulating the initiation of gametogenesis in echinoids. However, it is widely accepted that food quality and quantity strongly influence gonad size and gamete production (Lawrence, 1987, 2007; Lawrence and Lane, 1982;
Control of Reproduction in Echinoderms
49
Pearse and Cameron, 1991), since well-fed individuals produce larger gonads and more gametes than underfed individuals (Andrews, 1986; Dix, 1970; Gonor, 1973b; Johnson and Mann, 1982; Keats et al., 1984; Kobayashi and Tokioka, 1976; Moore, 1935; Pearse, 1981; Pearse et al., 1970; Thompson, 1984). The absence of gametes has been reported in extreme cases of food limitation [e.g., Echinocardium cordatum (Buchanan, 1966) and Allocentrotus fragilis (Sumich and McCauley, 1973)], whereas prolonged spawning seasons can occur when food sources are not limited (Dix, 1970; Pearse, 1981). The apparent trade-offs in allocation of nutrients between somatic and gonadal growth in echinoids are also well documented (Ebert, 1982; Fuji, 1967; Gonor, 1972, 1973b; Lewis, 1958; Pearse et al., 1986b). Some authors believe that feeding conditions merely influence the quality of gametes produced for spawning (Gonor, 1973c; Lawrence, 1975; Masuda and Dan, 1977; Re´gis, 1979) and that insufficient food accounts for the poor development of gonads (Nichols et al., 1985), while others believe that the nature of food may also influence the time of reproduction (Bernard, 1977; Kawamura and Taki, 1965). The body of evidence pertaining to the repercussions of variation in food supply on the reproductive cycle of echinoids is too large to deal with comprehensively in this section. We have outlined a suite of examples that demonstrate the wide diversity of data, correlations and interpretations available on this topic. Since food levels can be quite variable among years and locations, food abundance is unlikely to directly entrain reproductive cycles. Pearse (1969a) suggested that fluctuations in food may be important in regulating reproductive periodicities of the echinoids Prionocidaris baculosa and Lovenia elongata in the Gulf of Suez, although he pointed out that photoperiod and/or temperature may be indirect driving forces through their direct impacts on food levels and/or feeding and metabolic rates. Furthermore, lack of food may result in a marked reduction in gamete numbers but does not generally influence the length and pace of gametogenesis (Spirlet et al., 1998). Kenner (1992) did not find lower gonad indices in Strongylocentrotus purpuratus from communities with scarce food resources. On the other hand, Thompson (1984) and Lozano et al. (1995) showed greater allocation of resources to reproduction, at the expense of somatic growth, in response to unfavourable conditions in Strongylocentrotus droebachiensis and Paracentrotus lividus, respectively, thereby enhancing their reproductive effort even though reproductive output was lower. Because echinoids lack pyloric caeca, the body wall may assume a greater importance as a storage organ, which has been demonstrated in several species, for example, Strongylocentrotus intermedius (Fuji, 1960), Allocentrotus fragilis (Giese, 1961), and Strongylocentrotus purpuratus (Farmanfarmaian and Phillips, 1962). Storage may also occur in the test and the gonad itself
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(Binyon, 1972). The role of the stomach and intestine as nutrient storage organs in Lytechinus variegatus (Bishop and Watts, 1992) is supported by the high inter-annual variability in somatic organ indices (Beddingfield and McClintock, 2000). Pearse (1969b) suggested that gametogenesis in echinoids could not be initiated until a ‘‘critical level’’ of nutrients was available within the storage tissues (nutritive phagocytes) to insure gamete growth. In contrast, Holland and Giese (1965) and Chatlynne (1969) proposed that as nutrient reserves are depleted during gametogenesis, nutritive phagocytes begin to destroy germ cells, thereby terminating gametogenesis. Nevertheless, populations experiencing different food conditions display essentially the same temporal patterns of reproduction (Keats et al., 1984; Pearse, 1981). Giese (1959a) demonstrated that the gonads of Strongylocentrotus purpuratus in Monterey Bay (USA) were usually largest during the fall, and that starved individuals failed to reproduce; both the quality and quantity of food affected gonad development and biomass. Ebert (1968) also found that gonadal growth in S. purpuratus was limited by food quantity and quality. Similarly, Holland (1964) showed that individuals fed continuously in light or dark conditions exhibited early gonad maturity, suggesting that the quantity of food available might be partially responsible for the rate of gonad development. Chatlynne (1969) indicated that the annual reproductive cycle in S. purpuratus from Oregon, USA, was roughly divided into two segments, the first when the nutritive phagocytes were filling with globules and the majority of gametes were in the growth phase, and the second period when the phagocytes were being depleted of their globules and gametes were mostly at stages earlier than the growth phase. According to the author, the fact that large growing oocytes were plentiful when phagocytes were full of globules suggested that oocyte growth depended on the globules, especially since polysaccharides and lipids appeared in the phagocytes before they did in the cytoplasm of the oocytes. Chatlynne (1969) supposed that variation in globulation was due to greater availability of food in the habitat during the time when the phagocytes were filling and its relative scarcity when they were becoming depleted. Gonor (1973c) suggested that differences in the amplitude of annual gonad indices in Strongylocentrotus purpuratus could be due to erratic food supply. Gerard (1976) then showed that the availability of food for S. purpuratus in the form of attached and drifting kelp increased in southern Monterey Bay (western USA) in the summer, and suggested that seasonal availability of food might act as a mechanism for synchronizing reproduction. However, Gonor (1973c) and Pearse (1981) both expressed doubt that seasonal differences in feeding could successfully maintain synchronous gametogenic cycles in the field. Data for Paracentrotus lividus are somewhat contradictory since higher gonad indices can be found in populations living in habitats with less food
Control of Reproduction in Echinoderms
51
(Re´gis, 1979) and larger gonads in subtidal, well-fed populations (Byrne, 1990). It is possible that maturation at the same age at sites with different growth rates can produce the effect of increased gonad indices at equal sizes (but different ages), suggesting that estimates of growth rates in different habitats should be obtained in addition to field data (Lozano et al., 1995). Inter-specific variability in response to stress or food limitation is another possibility. The argument has been made that echinoids are less sensitive to food limitation than other invertebrates (Andrew, 1989) and that gametogenesis may be the last process to be inhibited in starving individuals (Bennett and Giese, 1955). Furthermore, there are mechanisms to ensure a short-term recovery of gametogenic activity following pulses of available food (Bishop and Watts, 1992). Lozano et al. (1995) thus proposed that the transition from reproduction to somatic growth in unfavourable conditions should be mediated by factor(s) other than food availability. Frantzis and Gre´mare (1992) observed a highly significant correlation between ingested organic matter and cumulated gonadal growth in Paracentrotus lividus. The qualitative nutrient requirements for somatic and gonadal growth seem to be similar in this species (Frantzis and Gre´mare, 1992), a result that contradicts previous observations of significant differences in energy partitioning between somatic and gonadal tissues among echinoids fed on different macrophytes (Lawrence, 1975). Lawrence et al. (1992) demonstrated that good quality prepared diets fed to the sea urchin Paracentrotus lividus under laboratory conditions favoured the production of gonads during the season when gonadal production was not occurring in the field. They suggested that food was limiting in the field and that gonadal production could be induced out-of-season by an enriched diet, supporting the conclusion that both somatic and gonadal production occur when food availability is high (Gago et al., 2003; Lawrence et al., 1992). Other in vitro trials on this species showed that the gonad index was higher when small individuals were fed preferred food species (Fernandez and Caltagirone, 1995). In experiments conducted along the coast of Portugal, all feeding treatments throughout the year resulted in significantly higher gonad indices and larger induced spawnings in captive animals than in those concurrently sampled from the field (Luis et al., 2005). Some diets also yielded considerably higher gonad indices (Luis et al., 2005). Similarly, P. lividus feeding on erect algae exhibited better somatic growth and gonad size than populations feeding on encrusting algae (Gago et al., 2003). Furthermore, sea urchins benefiting from a greater supply of food spent more energy on reproduction (Gago et al., 2003), which is slightly inconsistent with the general conclusion of De Ridder and Lawrence (1982) that food availability has a greater effect on the size of the gonads than on the state of reproductive development in echinoids. Guidetti et al. (2003) suggested that variable reproductive conditions over a large scale were likely in response to inconsistent densities of animals
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and trophic conditions. Gametogenesis was delayed in Paracentrotus lividus living at high densities in southern Spain in habitats lacking palatable algae. In southern Portugal, where density was lower and food availability greater, sea urchins were richer in lipids, but they were in a recovery phase (Guidetti et al., 2003). Although laboratory experiments with Paracentrotus lividus have generally shown that both somatic and gonadal production occur when food availability is high and better gonad growth can be obtained with preferred diets, field data are contradictory (Boudouresque and Verlaque, 2007). Subtidal well-fed populations displayed larger gonads, in both open-ocean and lagoonal locations (Byrne, 1990; Fernandez, 1996; Fernandez and Boudouresque, 1997; San Martin, 1995). In spite of comparable feeding patterns, higher gonad indices have been recorded when population density is low (Guettaf and San Martin, 1995), whereas non-significant relationships have been documented between gonad and gut content indices (Re´gis and Arfi, 1978; Semroud and Kada, 1987). In Catalonia (NW Mediterranean), higher gonad index values were found in specimens from a shallow hydrodynamic habitat, with poorly developed benthic food sources and high sea urchin densities than in a deeper location with preferred food sources (Lozano et al., 1995). The results were interpreted as a greater investment in reproduction under less favourable nutritional conditions (Lozano et al., 1995), although the authors recognised the possible role of drift food of high nutritional value. A number of studies on Strongylocentrotus droebachiensis have shown that gonad growth and gamete production are positively related to both food quantity (Garrido and Barber, 2001; Hagen, 1998; Hooper et al., 1996; Keats et al., 1984; Meidel and Scheibling, 1998, 1999; Minor and Scheibling, 1997; Pearce et al., 2002a; Thompson, 1983, 1984; Vadas, 1977) and quality (Cuthbert et al., 1995; De Jong-Westman et al., 1995; Hooper et al., 1996; Keats et al., 1984; Larson et al., 1980; Lemire and Himmelman, 1996; Meidel and Scheibling, 1999; Pearce et al., 2002b, 2003, 2004; Russell, 1998; Scheibling and Anthony, 2001; Vadas, 1977; Vadas et al., 2000) and that an adequate food supply may ensure that there is enough energy to promote overall gonad growth, even during spawning periods (Dumont et al., 2006). In the latter experiment, starved sea urchins exhibited a decrease in gonad index over 12 weeks (Fig. 2.6), indicating that they did not have sufficient energy for gonad production (Dumont et al., 2006). Gonad development in Strongylocentrotus droebachiensis is more rapid, and gamete production greater, in specimens inhabiting food-rich habitats (Meidel and Scheibling, 1999; Wahle and Peckham, 1999). However, the major gametogenic stages developed roughly concurrently across barren to kelp bed habitats in Nova Scotia (Canada), although two or three gametogenic stages could be present in different individuals in a population at any given time during the reproductive season (Meidel and Scheibling, 1998). This type of
53
Control of Reproduction in Echinoderms
Post-hoc comparison
18
Photoperiod: 16 Da, 0 Dab, 8 Dab, 24 Dbc, Ambient c Time: 12a, 8b, 4c, 0d
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Gonad index (%)
14 12
Ambient (b)
10 8
0 D(c) no food
6 4 2 0 0
8
4
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Figure 2.6 Strongylocentrotus droebachiensis (Echinoidea). Mean gonad index (%) of fed sea urchins exposed to five different photoperiods at each sampling date (mean SE, n ¼ 10–15). Photoperiod treatments are: 0D, 0 h darkness per day; 8D, 8 h darkness per day; 16D, 16 h darkness per day; 24D, 24 h darkness per day; Ambient, ambient photoperiod with natural light. The treatment ‘‘0D no food’’ represents urchins starved and held under 24 h light. Different letters indicate significant differences among treatments within the photoperiod and time factors. Post hoc results (Fisher’s LSD test) are also shown for week 12 data only, following one-way ANOVA, with treatments sharing the same letter in parentheses not differing significantly (P > 0.05). Reprinted with permission from Dumont et al. (2006).
wide-ranging synchrony suggests that environmental factors such as temperature, photoperiod and current regime interact with local food quality and availability to control spawning periodicity (Scheibling and Hatcher, 2007). In studies that manipulated food allowance, individuals given a higher ration had a greater gonad index and reproductive output than those fed a lower ration (Meidel and Scheibling, 1999; Minor and Scheibling, 1997; Thompson, 1983). These results are consistent with laboratory and field studies, demonstrating that a diet of laminarian kelp, a preferred food of Strongylocentrotus droebachiensis, markedly enhances growth and reproduction (Briscoe and Sebens, 1988; Himmelman, 1978; Himmelman and Steele, 1971; Larson et al., 1980; Munk, 1992; Thompson, 1983; Vadas, 1977; Vadas et al., 2000). Preferred species of algae promote greater gonad production, possibly because of an increased feeding rate (Lemire and Himmelman, 1996) or higher protein content (De Jong-Westman et al., 1995; Meidel and Scheibling, 1999). Garrido and Barber (2001) found that food availability not only determined the size of gonads but also influenced the cellular composition of
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gonadal tissue in Strongylocentrotus droebachiensis. A relatively constant proportion of nutritive phagocytes was maintained in individuals fed ad libitum, whereas low ration was associated with a lower proportion of nutritive phagocytes and, as a result, increased the proportion of gametes (Garrido and Barber, 2001). Minor and Scheibling (1997) also reported that female sea urchins given high rations had a greater proportion of nutritive phagocytes than individuals given low rations. The experimental results of Guillou et al. (2000) revealed that high food availability modified the pattern of gonadal and somatic growth of Sphaerechinus granularis from the Glenan Archipelago (France). Furthermore, these changes were much more evident during the recovery stage than the maturity stage. During the latter period, gonad indices increased as in the field population, although test diameter and weight did not change. Starved specimens did not exhibit the gonad and test growth observed in the fed treatment, and no gonadal growth was noted during the recovery period. The organic matter level dropped significantly in all body components, especially in the test and gonads (Guillou et al., 2000). The authors concluded that somatic growth did not take place over the maturity period in S. granularis and that individuals in good nutritional condition allotted energy to gonad production and could store reserves in the body wall without growing. Under limiting nutritional conditions, gonadal growth may be inhibited, although total regression may not be complete and slight reproductive activity can remain (Guillou et al., 2000). Data gathered from other species are usually more fragmentary or purely speculative. Pearse and Giese (1966) found that nutrients were apparently accumulated in the nutritive phagocytes of the gonads of Sterechinus neumayeri at Ross Island (Antarctica) during the summer phytoproduction and probably utilized during the winter to maintain a relatively constant rate of gametogenesis. Fuji (1967) correlated feeding with reproductive activity in the sea urchin Strongylocentrotus intermedius. Gonad production by Tripneustes gratilla on sand bottoms in the Gulf of Aqaba was much lower than in seagrass beds ( Jafari and Mahasneh, 1984). Gonad indices of Lytechinus variegatus in the field were lower than in individuals fed formulated diets in the laboratory (Hammer et al., 2004; Watts et al., 2007). Brockington et al. (2007) reported that a significant portion of vitellogenesis in the sea urchin S. neumayeri from Adelaide Island (Antarctica) occurred in winter (April–September), when feeding was suspended. Nichols et al. (1985) indicated that habitat richness in terms of food availability determined gamete production in Echinus esculentus from the English Channel (UK); Buchanan (1966) had earlier demonstrated this relationship clearly in the spatangoid urchin Echinocardium cordatum. In a littoral habitat, where the food supply was abundant, E. cordatum grew relatively quickly and reproduced annually; while in an offshore habitat, where food was limited, the
Control of Reproduction in Echinoderms
55
growth rate was reduced, the sea urchins never reached reproductive maturity, and the gonads remained vestigial. The sea urchin Anthocidaris crassispina from Hong Kong receives a plentiful food supply in winter, which coincides with the period when nutrient reserves are accumulating in the gonads, leading to the assumption that food is the most important factor contributing to gametogenesis and successful recruitment (Chiu, 1988). Vernon et al. (1993) observed interannual variation in gonad size in Clypeaster ravenelii from the northern Gulf of Mexico that may have been due to an increase in food availability or consumption. Because C. ravenelii occurs in moderately deep water, it is possible that fall and winter sedimentation of primary production serves as a cue to entrain gametogenesis (Vernon et al., 1993). Inhabiting food-poor barren areas has a negative influence on reproduction in Centrostephanus rodgersii in New South Wales (Australia), probably due to low abundance of macro-algal food, which results in a smaller store of nutrients at the onset of gametogenesis (Byrne et al., 1998). In Evechinus chloroticus from New Zealand, gametogenesis can be linked to nutrient availability (Brewin et al., 2000), as previously observed by Dix (1970), Andrews (1986) and Barker et al. (1998). Furthermore, Brewin et al. (2000) proposed that variation in reproductive potential over distances less than 10 km (Fig. 2.7) is attributable to small-scale heterogeneity in algal food. Herna´ndez et al. (2006) found that temporal and spatial changes in gonad size of Diadema antillarum in the Canary Islands were the result, at least in part, of benthic food availability and intra-specific competition for it. (a) Proposed mechanisms Nutritive phagocytes in ovaries and spermaries of echinoids are monociliar accessory somatic cells that form an integral part of the germinal epithelium (Au et al., 1998; Cavey and Ma¨rkel, 1994; Eckelbarger et al., 1989; Longo and Anderson, 1969). The globules in the nutritive phagocytes of the ovaries may be precursor yolk protein for the oocytes (Chatlynne, 1972). Isolation from the pre-vitellogenic ovaries of a glycoprotein similar to the major yolk protein (MYP) in the eggs prompted Ozaki et al. (1986) to conclude that vitellogenesis involved translocation of material from the nutritive phagocytes to the oocytes. Walker (1982b) showed that proliferation, differentiation, and growth of spermatozoa in Evechinus chloroticus occurred uniformly in the gonads, concurrently with an apparent change in the role of the nutritive phagocytes from nutrient storage to nutrient transfer for gamete development. The nutritive phagocytes therefore appear to serve in the storage of nutrients in vacuoles, destruction of relict gametes (Pearse, 1965), and transfer of nutrients to the gametes during gametogenesis (Pearse, 1969b; Walker, 1982b). Observations by light microscopy have confirmed that as gametogenesis is initiated, nutritive phagocytes grow larger as they accumulate nutrients
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Perano head 30 25 20 15 10 5 0
Titi bay Gonad index (%)
30 25 20 15 10 5 0
Dieffenbach point 30 25 20 15 10 5 0 Sea temperature Daylength
16
1000
15
900
14
800
13 700
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Daylength (mins)
Sea temperature (⬚C)
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10 S
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N
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M M
J
S
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N
J
M M
J
S
1993
N
J
M M
J
S
1994
Figure 2.7 Evechinus chloroticus (Echinoidea). Changes in gonad index for pooled data from males and females (means SE, n ¼ 20) at three sites in New Zealand with corresponding variations in temperature and day length. Reprinted with permission from Brewin et al. (2000).
(Byrne, 1999; Lane and Lawrence, 1979; Walker et al., 1998, 2007), and that the stored material is mobilized from the nutritive phagocytes during gamete synthesis (Unuma et al., 1998; Walker et al., 1998), leading to a decrease in cell size until the minimum is reached (Reunov et al., 2004). Unuma et al. (2003) indicated that both male and female sea urchins Pseudocentrotus depressus accumulate the MYP in the nutritive phagocytes of
Control of Reproduction in Echinoderms
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immature gonads before gametogenesis. Measurement of this protein, combined with data from other studies, led the investigators to suggest that MYP serves as a protein reserve that accumulates before gametogenesis and is used for synthesizing new substances in both sperm and eggs (Unuma et al., 2003).
(b) Deep sea The gametogenic cycle of the deep-sea echinoid Echinus affinis was determined from samples collected from 2200 m in the northern Rockall Trough (NE Atlantic) and revealed an annual reproductive periodicity (Tyler and Gage, 1984a). The onset of gametogenesis occurred in November and December, while mature oocytes of the preceding generation were still present in the gonad. Once mature oocytes had been spawned, vitellogenesis of the new generation of oocytes was initiated and spawning took place 14 months later (Tyler and Gage, 1984a). The authors suggested that the larval period coincides with the sinking of organic matter derived from the surface primary production and that: (1) this process provides a suitable food source for the echinopluteii; and (2) the organic matter reaching the sea bed in late spring and summer constitutes a labile source of energy for vitellogenesis in adults. The gametogenic cycles of the slope-dwelling congeners E. alexandri and E. acutus norvegicus resembled those of E. affinis (Tyler and Gage, 1984a). Campos-Creasey et al. (1994) showed increases in stomach contents of the sea urchin Echinus affinis that coincided with phytodetritus deposition at 2200 m depth. Together with photographic observations of feeding, the data suggest coupling between the seasonal deposition of phytodetritus and the diet, growth and seasonal reproduction of E. affinis (Campos-Creasey et al., 1994). Laboratory studies on bathyal echinoids have shown an increase in gonad size in response to food enhancement under experimental conditions but no noticeable changes in the timing of reproduction (Eckelbarger and Watling, 1995). Young et al. (1992) demonstrated that successful gametogenesis and spawning in the bathyal sea urchin Stylocidaris lineata from the Bahamian slope appeared to depend on acceptable quantity of food available. Although the organic flux hypothesis suggests the adaptive value of periodicity in gamete production and recruitment, the factors that determine initiation of gametogenesis and spawning are more difficult to define (Tyler and Gage, 1984a). The initiation of gametogenesis may be controlled by an unknown endogenous rhythm and spawning may be related to sediment re-suspension or the rapid transmission of a spawn-inducing substance throughout the population during periods of increased eddy kinetic energy (Tyler and Gage, 1984a).
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2.4. Inter-population and inter-individual communication It has been demonstrated in a growing number of echinoderms that temperature, photoperiod and food supply play a major role in the various stages of gamete synthesis and in the synchronization of the entire process of gametogenesis and gonad growth. However, it is not easy to explain the onset and coordination of development among individuals or of gametogenesis in entire populations, whether exposed to similar or distinct local environmental conditions. This is especially important for freely spawning species that may waste a large portion of their gametes if this synchronization is not well orchestrated. Wasson and Watts (2007) investigated the production and function of hormones and steroidal pheromones from echinoderms in the northern Gulf of Mexico, which produce a variety of steroid products that are, in some cases, homologous to those found in vertebrates, including testosterone, dihydrosterone, androstane derivatives, and estrone. Several echinoderm species produce large quantities of water-soluble steroid conjugates, primarily glucuronides, which may have pheromone activity. These steroids and steroid-related compounds present in echinoderm tissues may function as chemical signals which regulate physiological processes within individuals and influence both intra and inter-specific chemical communication. Although reports of chemical communication related to gametogenesis among echinoderms are still scarce and often speculative, studies on this topic have recently provided interesting evidence for holothuroids, asteroids and echinoids. 2.4.1. Holothuroidea An experimental study carried out on Cucumaria frondosa by Hamel and Mercier (1996b, 1999) revealed that environmental factors, coupled with various endogenous reactions, could not adequately explain the synchronous initiation and progress of gamete synthesis in male and female sea cucumbers. This work explored the role of chemical mediators during gametogenesis and showed that mucus, one of its constituents or a chemical emitted with it plays a determinant role in the fine-tuning of gametogenesis within and among entire populations of holothuroids (Hamel and Mercier, 1996b, 1999). The data showed that sea cucumbers secrete a biologically active chemical which promotes synchrony of gamete synthesis among individuals. Laboratory experiments revealed that the gametogenesis was significantly less synchronous among individuals that were maintained separately under natural environmental conditions than it was among similarly treated individuals kept in groups (Hamel and Mercier, 1996b) (Fig. 2.8). Furthermore, the presence of more mature individuals of the same sex induced gametogenesis in less developed individuals, even those that had not previously been exposed to an increase in day length, which
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marks the onset of gametogenesis in this species (Hamel and Mercier, 1996b). Additional studies indicated that the active substance was present in the mucus secreted by the body wall, enabling it to travel as far as 20–30 m away from the secreting animal (Hamel and Mercier, 1999) (Fig. 2.9). These findings suggest that the lunar cycle, photoperiod, food supply and temperature cannot individually account for the onset and synchronization of reproduction, but rather that environmental cues act synergistically and can be transmitted within and between populations through chemical communication among congeners (Hamel and Mercier, 1996b). Such inter-individual communication could explain the synchrony observed in the maturation of deep-water and shallow-water populations of sea cucumbers, despite the fact that the former presumably cannot directly perceive the initial environmental cue (Fig. 2.10).
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Another interesting study was conducted by Arakaki et al. (1999) with the sea cucumber Polycheira rufescens from the intertidal zone in Japan. Field caging experiments revealed that some individuals can undergo sequential sex changes from male to female via hermaphrodite stages and back to male again within a single reproductive season. The sex ratio of the population which was initially male-dominated shifted toward equality as the reproductive season progressed (Arakaki et al., 1999). The proportion of immature or spent individuals increased towards the end of the breeding season. A slightly stronger tendency to aggregate was observed in males than in females, and females seemed to attract males, according to the relatively short female to male distance that was observed. The spatial distribution of P. rufescens during the reproductive period may therefore be partly determined by the individual needs of sea cucumbers at different sexual stages (Arakaki et al., 1999). Although experimental studies on chemical communication during gametogenesis are rare, the occurrence of aggregations associated with the reproductive cycle provides circumstantial evidence of inter-individual exchange (see Section 2.8.1 in Chapter 3 for a more complete discussion of aggregations). Spatial distribution observed during tank experiments suggested that adults of Holothuria scabra aggregate prior to spawning, in response to the lunar cycle (Fig. 2.5). The formation of pairs, trios or larger groups increased during the new moon and was most common just before the full moon (Mercier et al., 2000a). Male and female spawnings were observed in the tanks, typically around the full moon. Spawning occurred both during the peak in aggregation and later, when the individuals were more evenly distributed. No aggregation was noted in individuals <110 mm in length, which were presumably juveniles or immature (Mercier et al., 2000a). Dense aggregations of the elasipods Elpidia glacialis, Scotoplanes globosa and Achlyonice violaecuspidata were observed in the Weddell Sea (Antarctica) by Gutt and Piepenburg (1991) during extensive benthic surveys in 1983–1985. The investigators proposed that bioluminescence could act as a signal to facilitate the formation and persistence of these aggregations. Socalled herds or clumps in the distribution of elasipod holothuroids are fairly well documented by photographic observations of various species, for example, Barham et al. (1967), Heezen and Hollister (1971), Menzies et al. (1973), Grassle et al. (1975), Pawson (1976, 1982), Ohta (1983). Billett and Hansen (1982) reported mean densities of 4–50 ind. m2 for Kolga hyaline in the deep ocean west of Ireland and proposed that the heterogeneity in the distribution pattern was due to temporal aggregations. Although spermatozoa as lines. The gametogenic stages are: 1, post-spawning; 2, recovery; 3, growth; 4, advanced growth; and 5, maturity. Control experiments were performed using individuals without stimulation. Vertical lines represent 95% confidence intervals. Reprinted with permission from Hamel and Mercier (1999).
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Photic zone
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Figure 2.10 Cucumaria frondosa (Holothuroidea). Seasonal changes, from April 1992 to November 1993, of the gonad index in males and females collected either in the photic (10 m) or aphotic zone (110 m). Vertical lines represent 95% confidence intervals. Reprinted with permission from Hamel and Mercier (1996a).
explanations given for aggregations of grazing elasipod holothuroids include food supply, the persistent herding was apparently best explained by communication between individuals (Billett and Hansen, 1982). 2.4.2. Asteroidea Both direct and indirect evidence of chemical exchanges during gamete synthesis has been obtained in this class. For instance, shallow-water sea stars in the genus Archaster commonly aggregate during the breeding season (Boschma, 1924; Mortensen, 1931; Run et al., 1988), and spawning pheromones are known or suspected to be produced by other species of asteroids (Beach et al., 1975; Hamel and Mercier, 1995b; Miller, 1989). Studies of chemical signalling in asteroids have largely focused on breeding episodes (see Section 2.8.2 in Chapter 3 for details). Briefly, Ormond et al. (1973) showed that an active component released by the gonad of the sea star Acanthaster planci induced reproductive behaviour in nearby mature adults, Run et al. (1988)
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suggested that a sex-specific contact chemoreception could partially explain sex recognition in the sea star Archaster typicus, and Miller (1989) discussed the periodic presence of a long-lived, bioactive, sex-specific substance in natural seawater during the reproductive season of sea stars. There is much less evidence of inter-individual interactions during gametogenesis. Hamel and Mercier (1995b) found that chemical communication via contact in the sea star Leptasterias polaris seemed to play a role in gametogenic synchronization, mostly during the late stages of gamete maturation before spawning. Such clustering behaviour initiated well before spawning, whereby the chemical interaction may influence the final development of gametes in preparation for spawning, has not often been reported. Run et al. (1988) documented the mating behaviour of the sea star Archaster typicus throughout its reproductive cycle and noted an increased tendency for male motility coincident with the annual spring increase in the gonad index. A large increase in the number of male-onfemale pair assemblages followed this change in behaviour, which occurred approximately 2 months before the peak spawning period. This suggests that males of A. typicus recognise the sex of other individuals prior to spawning and that some form of communication occurs during gametogenesis. No evidence of pre-spawning sex recognition or extended pair formation was observed in the pseudo-copulating Antarctic asteroid Neosmilaster georgianus (Slattery and Bosch, 1993). 2.4.3. Echinoidea Early reports by Orton (1914) and Lewis (1958) mentioned the occurrence of pre-spawning clustering in echinoids. Spatial aggregations throughout the year have been hypothesized to facilitate reproduction in some species (Dix, 1969; Orton, 1914). Furthermore, Orton (1914) noted that most intertidal pairs of Echinus miliaris were heterosexual, although such aggregations or pairing have not been reported since. 2.4.4. Deep-sea Tyler (1988) proposed that various physical and chemical factors control gametogenic seasonality in the deep sea, but the proximate mechanisms by which deep-water organisms synchronize spawning to ensure successful fertilization remain largely unknown. Several abyssal and bathyal echinoderms form dense aggregations (Billett and Hansen, 1982; Grassle et al., 1975; Rice et al., 1982) or small discrete groups (Fujioti et al., 1987; Pawson, 1976). Although some investigators have suggested that such aggregations form to facilitate breeding (Pawson, 1976), others have interpreted them as feeding aggregations (Grassle et al., 1975). Because it is generally assumed that deep-sea invertebrates do not cue reproduction on celestial factors such as sunlight or moonlight, inter-individual communication may be important (Young et al., 1992). Observations
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Figure 2.11 Breeding aggregations of deep-sea echinoderms in the field and in the laboratory. (A) Aggregations of the echinoid Stylocidaris lineata photographed in situ at ca. 700 m in the Bahamas. (B) Aggregation of the echinoid Cidaris blakei from a similar depth at another site in the Bahamas. Photos were taken using a Johnson-Sea-Link submersible in May 2008 (courtesy of Craig M. Young, University of Oregon).
from a manned submersible at bathyal depths in the northern Bahamas revealed discrete, single-species aggregations of 2–6 individuals of the echinoid Stylocidaris lineata (Young et al., 1992) (Fig. 2.11). Histological determination of reproductive condition in isolated and aggregated individuals showed that, in February 1990, all individuals contained developing gametes, regardless of their spatial distribution. In May 1988, during the breeding season, most isolated individuals contained spent gonads, whereas aggregating individuals mostly contained ripe gonads with mature or nearly mature gametes (Young et al., 1992). No aggregations were observed in the autumn months, at a time when gonads were either spent or immature, strongly suggesting that bathyal cidaroids aggregate for reproductive purposes (Young et al., 1992). Homosexual and heterosexual pairs occurred as predicted by the sex ratio. Young et al. (1992) thus postulated that aggregation may facilitate spawning synchrony, increase the probability of gamete encounters, or cause gametes to be retained at high concentrations near the adults long enough for fertilization to occur. Other bathyal echinoid species, such as Aspidodiadema jacobyi, Cidaris blakei and Salenia goesiana are commonly observed to form breeding aggregations (Young, 2003). While the spatangoids Archaeopneustes histrix and Palaeopneustes cristatus, the cassiduloid Conolampas sigsbei, and the arbacioid Coelopleurus floridanus also occur in groups at bathyal depths in the Bahamas, these aggregations are present throughout the year and probably do not form for the explicit purpose of reproduction (Young et al., 1992). A recent laboratory study revealed that aggregations of the bathyal asteroid Henricia lisa occurred exclusively during the biannual spawning period
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(Mercier and Hamel, 2008). Many other species of deep-sea asteroids were observed to periodically form pairs in similar captive settings; however, their reproductive status was not assessed. It is clear that further investigations will be required to solve the mystery of deep-sea aggregations (additional information on this topic can be found in Section 2.8.1 in Chapter 3).
3. Endogenous Mediation The timing of reproductive processes in marine invertebrates is controlled by the nervous and endocrine and/or neuro-endocrine systems. Other factors such as seasonally fluctuating environmental variables and chemical signals likely act as proximate cues (see Section 2) to synchronize reproduction by inducing biochemical changes within the gonads. The annual gametogenic cycle of certain echinoderms is the result of intricate mechanisms involving specific hormones and target tissues. In their review of the chemical control of asexual and sexual reproduction in echinoderms, Shirai and Walker (1988) discussed the perception and interpretation of environmental information by an organism. How external cues are perceived by the echinoderm body and then delivered to and interpreted by relevant, internal effectors is not well understood. Controlled laboratory investigations of these mechanisms have not often been conducted, partly because adequately equipped, flow-through seawater facilities are not always available (Shirai and Walker, 1988). The nervous system and structures such as ocelli at the arm tips of asteroids may be involved in perception and may produce neuro-chemicals. Alternatively, the entire surface of the echinoderm body may respond to environmental stimuli (Shirai and Walker, 1988). Variations in hormone levels during gametogenesis have been studied in echinoderms (Barbaglio et al., 2007). There is experimental evidence that hormones, particularly steroids, can play a role in echinoderm reproduction as well as in other physiological processes (Hines et al., 1992; Schoenmakers and Dieleman, 1981; Voogt et al., 1991; Wasson et al., 2000b; Watts et al., 1994; Xu and Barker, 1990b). Progesterone, androstenedione, testosterone, estradiol-17b and estrone have been studied primarily in asteroids (Barbaglio et al., 2006; Georgiades et al., 2006; Lavado et al., 2006a; Voogt et al., 1985) although they have also been detected in echinoids and a few other echinoderms (Schoenmakers and Dieleman, 1981; Voogt and Dieleman, 1984; Wasson et al., 2000b; Xu and Barker, 1990b). In the sea stars Sclerasterias mollis and Asterias rubens (¼vulgaris), levels of progesterone, estrone and testosterone fluctuate with the reproductive cycle and exhibit a sex-specific relationship (Hines et al., 1992; Voogt and Dieleman, 1984; Xu and Barker, 1990b). Ophiuroids, holothuroids and crinoids apparently synthesize sex steroids through metabolic pathways analogous to those found in vertebrates. For instance, a tissue-specific and sometimes sex-specific pattern has been
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noted in the activity of D5–D4-isomerase,17b-hydroxysteroid dehydrogenase, 5a-reductase, 3b- and 3a-hydroxysteroid dehydrogenase, 11b-hydroxylase and 11b-hydroxysteroid dehydrogenase (Hines et al., 1992, 1994; Janer et al., 2005; Schoenmakers and Voogt, 1981; Voogt et al., 1990; Watts et al., 1994). While sex steroids and steroid-metabolizing enzymes do occur in echinoderms, the relationship between steroids and reproduction is not fully understood (Barbaglio et al., 2007).
3.1. Crinoidea Evidence of endogenous regulation of gamete synthesis in crinoids remains largely anecdotal. For example, the fact that all oocytes begin to differentiate simultaneously in Oxycomanthus japonicus has led to the suggestion that environmental stimuli are acting on all oocytes at once through nervous or endocrine mechanisms (Holland, 1991; Holland et al., 1975). No further support has been published and most studies at this level have centered on the storage and transport of nutrients prior to and during gametogenesis (see Section 2.3 on this topic). Nevertheless, specific cytosolic androgen and estrogen binding sites were recently discovered in Antedon mediterranea (Lutz et al., 2004) and endocrine disruptors shown to have an impact on regenerative ability and steroid levels in crinoids (Barbaglio et al., 2006; Candia Carnevali, 2005; Lavado et al., 2006a).
3.2. Ophiuroidea Little information exists on internal physiological rhythmicity relating to reproduction in the Ophiuroidea. It is known that cyclic AMP initiates oocyte maturation in Amphipholis kochii (Yamashita, 1986, 1988).
3.3. Holothuroidea Several compounds exhibit cycles closely linked to gamete synthesis in holothuroids. The glycoside content in the ovaries of Apostichopus (=Stichopus) japonicus increases 40-fold during the pre-spawning period (Aminin and Anisimov, 1987). Similarly, concentrations of saponins in Holothuria tubulosa vary according to the reproductive phase (Louiz et al., 2003). The accumulation of triterpene glycosides in ovaries of sea cucumbers during this period may therefore reflect their participation in gametogenesis (Kalinin et al., 2007). Indeed, saponin-rich mucus secreted by the body wall of Cucumaria frondosa mediates gametogenesis synchrony (Hamel and Mercier, 1999). Another potential function of the triterpene glycosides in sea cucumbers is the inhibition of oocyte maturation through increased microviscocity of the oocyte membrane resulting from the inhibition of Ca2þ transport (Aminin and Anisimov, 1992). Kalinin et al. (2007) proposed that saponins may thus
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play two regulatory roles during reproduction: (1) to inhibit oocyte maturation and (2) to act as a mediator of gametogenesis. Bandaranayake and Des Rocher (1999) indicated that most marine organisms contain a complex mixture of mycosporine-like amino acids (MAAs), and that some MAAs accumulate as a result of seasonal changes in reproductive state or diet (Stochaj et al., 1994). Observations on Holothuria atra suggest that while some MAAs have a photo-protective role, others are involved with the reproductive process, and that the viscera serve as temporary storage until the MAAs are translocated to the reproductive organs (Bandaranayake and Des Rocher, 1999). Mycosporine-gly, one of the most abundant MAAs found in marine organisms, is the most abundant MAA in the tissues and ovaries of H. atra (Bandaranayake and Des Rocher, 1999).
3.4. Asteroidea In asteroids, final oocyte maturation occurs shortly after a hormonal peptide, or gonad-stimulating substance (GSS), is released from the nervous system into the coelomic cavity (Kanatani, 1964, 1969, 1979; Kanatani and Ohguri, 1966). When stimulated by GSS, the ovarian tissues produce a meiosisinducing substance (MIS) which has been identified as 1-methyladenine (1MA) (Kanatani, 1969). However, 1-MA is probably not involved in the regulation of gamete synthesis or gonadal growth but rather restricted to the processes of ovulation and spawning (see Section 5.4 in Chapter 3 for details). Variations in gonad size in asteroids have been associated with fluctuations in steroid levels (Greenfield, 1959; Schoenmakers and Voogt, 1981; Voogt, 1982). Estrogens and progesterones have been found in the gonads and pyloric caeca of several species: Pisaster ochraceus (Botticelli et al., 1960), Asterias amurensis (Kanatani et al., 1971), Astropecten irregularis pentacanthus (Colombo and Belvedere, 1976), Asterias rubens (Dieleman and Schoenmakers, 1979; Schoenmakers, 1981; Voogt and Dieleman, 1984; Voogt et al., 1984) and Sclerasterias mollis (Xu and Barker, 1990b). Estrogens and progesterone might have several functions in both reproduction and nutrition during the annual reproductive cycle of asteroids (Schoenmakers, 1981; Voogt et al., 1984; Watts and Lawrence, 1985, 1987). However, it is not clear whether or not the synthesis of intermediate steroid hormones is under the control of environmental factors such as temperature or photoperiod (Pearse and Eernisse, 1982), and if so, how. One of the most extensively studied species with respect to the role of steroids in reproduction is Asterias rubens (¼vulgaris). Schoenmakers and Dieleman (1981) determined that seasonal patterns of progesterone and estrone in females of A. rubens were related to stages of oogenesis and proposed an antagonistic relationship in the regulation of vitellogenesis. Voogt and Dieleman (1984) later reported varying levels of estrone and
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progesterone during the annual gametogenic cycle of males of A. rubens, suggesting that these steroids were also involved in spermatogenesis. Other investigators have shown that progesterone metabolism (Voogt et al., 1986) and 3b-HSD activity (Schoenmakers, 1981) vary in the ovaries and pyloric caeca during the reproductive cycle of A. rubens. Injections of estradiol-17b into the coelom caused a tenfold increase in the estrone level in the ovaries and larger oocytes were also found in the females that were treated with the estradiol-17b (Schoenmakers, 1981; Schoenmakers et al., 1981). Hines et al. (1992) determined that the testes and ovaries of the sea star Asterias rubens (¼vulgaris) exhibited annual growth cycles during which testicular or ovarian mass increased up to a hundredfold as production and storage of gametes progressed. In males, sex steroid levels were highest at the onset of spermatogenesis. Specifically, transient increases in the levels of estradiol coincided with spermatogonial mitotic proliferation, whereas increases in the levels of testosterone and progesterone coincided with spermatogenic column formation and spermiogenesis, respectively. In the ovaries, the highest levels of estradiol and testosterone were recorded at the onset of oogenesis while progesterone levels did not change significantly throughout the annual cycle (Hines et al., 1992). Pyloric caeca displayed similar seasonal variations in levels of sex steroids as the gonads in both sexes. The authors thus hypothesized that transient increases in the levels of sex steroids during gametogenesis could serve as endogenous modulators of reproduction (Hines et al., 1992). In another study of Asterias rubens (¼vulgaris), Watts et al. (1990) found that the specific activity of ornithine decarboxylase (ODC) followed testis development, remaining low during the coldest period of the winter when testis growth was minimal and increasing in early spring with maximum testis growth. Furthermore, they observed that high ODC activity translated into an increased level of polyamines associated with cell division. Sible et al. (1991) reported that cells in the inactive spermatogenic epithelium of A. rubens (¼vulgaris) were competent to undergo mitotic proliferation when supplied with polyamines, suggesting that seasonal regulation of ODC transcription was an essential component of the reproductive cycle. An increase in oocyte diameter and in lipid amount in vivo, as well as an increase in RNA levels in vitro, were detected following exposure of ovarian fragments to estradiol in both Asterias rubens and Asterina pectinifera (Schoenmakers et al., 1981; Takahashi and Kanatani, 1981; Van Der Plas and Oudejans, 1982). Takahashi (1982) observed a significant increase in ovarian protein in Asterina pectinifera following the administration of estrone but not estradiol-17b or testosterone. Furthermore, progesterone appeared to depress the growth of the ovaries and to reduce ovarian protein levels. Most previous investigations on the direct effect of injection of steroids on gametogenesis in sea stars have been carried out with individuals in the latter stages of gametogenesis (Schoenmakers et al., 1981; Takahashi, 1982).
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Seasonal changes in the levels of estradiol-17b, estrone and progesterone in the ovaries and the pyloric caeca of the sea star Sclerasterias mollis from New Zealand are closely related to the stages of the reproductive cycle and biochemical composition of these organs, suggesting endogenous control of reproductive processes (Barker and Xu, 1991a; Xu and Barker, 1990b). Daily injections of estradiol-17b or estrone for 16 days at the early stage of the gametogenic cycle caused an increase in the estrone and progesterone levels in the ovaries (Barker and Xu, 1993). There was a considerable increase in oocyte diameter and protein level in the ovaries of the treated animals. This and earlier studies on S. mollis suggest that estrogens and progesterone are involved in a regulatory system to control reproduction and nutrient cycles (Barker and Xu, 1993). The function of asterosaponins was described by Ikegami et al. (1972), who showed that these substances inhibited spawning in Asterias amurensis. Maturation of oocytes was repressed by asterosaponins, and ovarian follicle cells proved to be the site of action of the saponins (Ikegami, 1976), leading to the suggestion that regulation of oocyte maturation and spawning may be an important function of asterosaponins (Voogt and Huiskamp, 1979). The latter investigators observed that in A. rubens saponin levels were low from May to late September, increased steadily through the beginning of January, remained unchanged until May, and finally dropped abruptly upon spawning. Yasumoto et al. (1966) also reported seasonal variations in the level of asterosaponins in A. amurensis following the gametogenic cycle, with high values in summer and low values in winter. According to Ikegami et al. (1972), high levels of asterosaponins in summer would act to prevent spawning, whereas lower levels in winter would allow spawning to take place in February–March. However, this pattern is not always observed, indicating that inhibition of spawning may not be the primary function of asterosaponins in all asteroid species. For instance, Burns et al. (1977) observed maximal levels of asterone in A. rubens (¼vulgaris) in May–June, just before spawning, and Mackie et al. (1977) similarly reported high levels of asterosaponins in the gonads during the breeding season of Marthasterias glacialis. Wasson and Klinger (1994) reported a decrease in total DNA content and an increase in DNA concentration in the pyloric caeca prior to spawning in Asterias forbesi, suggesting a depletion of cytoplasmic reserves and catabolism of whole cells to mobilize nutrients for reproduction. After spawning, DNA concentration decreased but DNA content increased, indicating that nutrients were being stored by increasing the number and the average size of the cells of the pyloric caeca. Shirai and Walker (1988) discussed the role of neural and other chemical mechanisms in controlling gametogenesis: interrelationships between source cells, their chemical products and target cells and tissues in
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echinoderms are most apparent in the well-studied period of gametogenesis before the first meiotic cytokinesis.
3.5. Echinoidea A recent review has shown that there are several levels of endocrine control of echinoid reproduction, with sex steroids, proteins, catecholaminergic and cholinergic factors all playing roles in regulating aspects of gonad function (Walker et al., 2007; Wasson and Watts, 2007). The harmonious progression of gametogenic and nutrient translocation activities among and within the gonads supports the existence of a physiologically controlled coordination mechanism (Wasson and Watts, 2007). Chemical messengers, of neuronal or other origin, may be transmitting the information to the gonads. It has been argued that the haemal system, which interconnects with each gonad via the aboral ring complex, may provide the most efficient and specific means of control (Wasson and Watts, 2007). In spite of recent advances in this field, the respective roles of exogenous and endogenous control mechanisms, and possible links between them, remain unclear. Similar winter–spring spawning periods in populations of Strongylocentrotus purpuratus from Baja California to Washington on the west coast of North America, in areas where temperature, food, and photoperiod regimes differ markedly, prompted Boolootian (1966) to propose that endogenous factors likely mediate reproduction in this species. Olive and Garwood (1983) suggested that the reproduction of other species inhabiting apparently aseasonal environments are also under endogenous control, by means of an internal oscillator. However, Giese and Pearse (1974) argued that a synchronized seasonal pattern could hardly be totally independent of an exogenous regulator, and it was demonstrated that gametogenic activity in S. purpuratus is regulated by photoperiod, without any evidence of an internal oscillator (Pearse et al., 1986b). Data on steroid levels and metabolism are scarce and limited to a few echinoid species. Botticelli et al. (1961) were the first to demonstrate the occurrence of progesterone-like substances in the sea urchin Strongylocentrotus franciscanus. Much lower steroid levels were recorded in Lytechinus variegatus (testosterone: 60–320 pg g1; estradiol: 5–160 pg g1) than in asteroids [testosterone: 140–5500 pg g1 gonad; estradiol: 4–460 pg g1 gonad (Hines et al., 1992)]. According to Wasson et al. (2000b), this may be due to different mechanisms regulating gamete nutrition in the two echinoderm groups (Pearse and Cameron, 1991; Walker, 1982a; Wasson et al., 2000b). Using radiotracers, Colombo and Belvedere (1976) showed that the gonads of Paracentrotus lividus could convert androstenedione (the mammalian precursor to testosterone and estrogens) into testosterone, which attests to the activity of 17b-hydroxysteroid dehydrogenase in gonadal tissues. Varaksina and Varaksin (1991) later confirmed that developing oocytes
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and spermatids contain 17b-hydroxysteroid dehydrogenase activity, thus supporting the role of this enzyme in gonad function. In vitro radiotracer experiments have shown that ovaries and testes of Lytechinus variegatus produce testosterone and 5a-reduced androgens (Watts et al., 1994). Furthermore, activity of 11b-hydroxylase and 11b-hydroxysteroid dehydrogenase related to production of 11-oxygenated androgens was detected in the testes (Watts et al., 1994). 11b-Keto testosterone and 11a-keto testosterone have also been identified in other echinoderm species (Watts et al., 1993). Measurements of androgen metabolism during the annual reproductive cycle of L. variegatus suggests a relation between the activity of steroid-converting enzymes and reproduction (Wasson et al., 2000b). Maximal accumulation of 5a-adiols was found in April at the onset of a decrease in the gonad index (i.e., spawning season) in both sexes. Furthermore, the ovaries consistently synthesized higher levels of 5a-adiols than testosterone. From this sex-specific pattern of 5a-adiols accumulation, Wasson et al. (2000b) suggested that these compounds influence reproduction in L. variegatus. Sex-specific differences in androstenedione metabolism have also been demonstrated in this species (Wasson et al., 1998). Testosterone in the gonad of Paracentrotus lividus is mainly converted to dihydrotestosterone by 5a-reductase, whereas in the gut it is transformed to 4-androstene-3b,17b-diol by 3b-hydroxysteroid dehydrogenase ( Janer et al., 2005). Dietary administration of progesterone, testosterone and estradiol apparently have an impact on the gonad index and gametogenesis in Pseudocentrotus depressus (Unuma et al., 1999; Wasson et al., 2000a) and Lytechinus variegatus (Wasson et al., 2000a). In juveniles of P. depressus fed for 30 days on a diet containing progesterone, androstenedione, testosterone, estrone, or estradiol-17b, males in the androstenedione and the estrone-treated groups had significantly higher gonad indices than those in the control group (Unuma et al., 1999). Histological analysis confirmed that spermatogenesis in the estrone-treated group was enhanced, strongly inferring that androstenedione, estrone, and possibly their derivatives are involved in the reproductive activity of males (Unuma et al., 1999). Wasson et al. (2000b) suggested that a receptor mediates the effect for these hormones, although evidence for the existence of steroid receptors in echinoderms is still circumstantial. Nevertheless, radio-receptor assays have recently shown the presence of binding sites for testosterone and estradiol in Paracentrotus lividus (Lutz et al., 2004). Available data on the influence of endocrine disrupters on gametogenesis, fertilization and development in echinoids (Lavado et al., 2006b; Moschino and Marin, 2002; Novelli et al., 2002; Pesando et al., 2004; Roepke et al., 2005, 2006; Wasson and Watts, 1998) further suggests a possible role for sex steroids in reproductive physiology. Growth and maturation of oocytes can be suppressed by noradrenalin and dopamine in Strongylocentrotus nudus, illustrating the inhibitive effect of
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these substances on temperature-triggered oogenesis (Khotimchenko, 1982, 1983). The level of these catecholamines vary according to the reproductive state, remaining low when gametogenic activity is low and immediately before spawning, which coincides with peaks in catecholamine concentrations (Khotimchenko and Deridovich, 1991). Khotimchenko (1982, 1983) concluded that the suppression of oocyte growth resulted from the inhibition of RNA and protein synthesis and that the catecholamines influenced oogenesis via the coelomic fluid. In contrast, gamete release may be regulated by cholinergic mechanisms since acetylcholine was secreted in the regions of neuromuscular contacts of the gonads and induced a reduction in the muscle elements of the acini (Khotimchenko, 1982). Murata et al. (2003) indicated that rising levels of pulcherrimine (a sulfurcontaining amino acid) from September to December followed maturation of ovaries in Hemicentrotus pulcherrimus (south-western coast of Japan), suggesting that it accumulates in the oocyte or ovum during oogenesis. The pulcherrimine content did not decrease rapidly after spawning, presumably due to the presence of phagocytised residual ova (Murata et al., 2003). Varaksina and Varaksin (2002) investigated protein synthesis in the ovary of Strongylocentrotus intermedius at different stages of the reproductive cycle following a treatment with estradiol dipropionate. 3H-leucine was incorporated into the oocytes during early and active gametogenesis, but estradiol dipropionate did not cause any changes in protein synthesis before spawning. After the treatment, puromycin and actinomycin (inhibitors of protein synthesis) reduced 3H-leucine incorporation into the oocytes and protein synthesis in the ovary (Varaksina and Varaksin, 2002).
C H A P T E R
T H R E E
Spawning Contents 74 76 77 77 85 87 87 87 89 93 102 109 118 120 121 139 139 143 147 148 156 156 158 158 158 159 159 162 167
1. General Note 1.1. Crinoidea 1.2. Ophiuroidea 1.3. Holothuroidea 1.4. Asteroidea 1.5. Echinoidea 2. Correlation with Exogenous Factors 2.1. Photoperiod and light intensity 2.2. Time of day 2.3. Temperature 2.4. Phytoplankton, phytodetritus and other food sources 2.5. Lunar cycle 2.6. Tides and currents 2.7. Salinity 2.8. Inter-population and inter-individual communication 3. Evidence from Spatial and Inter-Annual Variation 3.1. Ophiuroidea 3.2. Holothuroidea 3.3. Asteroidea 3.4. Echinoidea 4. Evidence from Artificial Induction 4.1. Holothuroidea 4.2. Echinoidea 5. Endogenous Mediation 5.1. Crinoidea 5.2. Ophiuroidea 5.3. Holothuroidea 5.4. Asteroidea 5.5. Echinoidea
Advances in Marine Biology, Volume 55 ISSN 0065-2881, DOI: 10.1016/S0065-2881(09)55003-1
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2009 Elsevier Ltd. All rights reserved.
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Annie Mercier and Jean-Franc¸ois Hamel
1. General Note Oocytes and spermatozoa must be present and mature at exactly the same time for successful reproduction to occur, especially in light of the typically short swimming time of spermatozoa, which must occur at relatively high concentrations in order for fertilization to take place (reviewed by Levitan, 1995). In marine environments, fertilization success may be assured by a number of mechanisms, including breeding behaviours that bring congeners together (e.g., Hamel and Mercier, 1995b; Run et al., 1988), environmental cues that favour simultaneous release of gametes (reviewed by Giese and Kanatani, 1987; Giese et al., 1991), and, in some cases, by chemical communication (e.g., Miller, 1989). Nevertheless, evidence for epidemic spawning is ambiguous for most species (Young, 1999), and only a few experimental studies (e.g., Mercier et al., 2007; Starr et al., 1990) have shown its importance in subtidal environments. For species with external fertilization, aggregative behaviours and an increase in the importance of chemical communication have been predicted (Hamel and Mercier, 1995b; Young, 1999). Modifications of gametes may also occur (Eckelbarger, 1994; Eckelbarger et al., 1989). In spite of the potentially large number of recruits produced by broadcast-spawners, fertilization success may be low unless individuals: (1) aggregate (Levitan, 1991; Levitan et al., 1992; Pennington, 1985), (2) synchronize gamete release (Levitan, 1988; Pearse et al., 1988; Pennington, 1985), and (3) are located in low to moderate flow conditions (Denny and Shibata, 1989; Hamel and Mercier, 1996d; Levitan et al., 1992; Pennington, 1985; Sewell and Levitan, 1992). This implies a need to elaborate an appropriate of response to their environment and to congeners. In a review of spawning in marine invertebrates, Himmelman (1999) proposed that proximate spawning cues should readily be distinguishable from background environmental variation and should enhance reproductive fitness through increased fertilization success, outbreeding, or survival of larvae and juveniles. Perception of an environmental cue and its translation into release of gametes or larvae may present variable degrees of complexity, depending on the control pathways in the species under consideration. For instance, a cue may elicit gamete release directly by causing contraction of the body wall or gonad muscles. However, spawning in most species involves multiple neuro-endocrine pathways that introduce a delay between the perception of the cue and the response to it. An extreme example is the entrainment of internal rhythms by environmental cycles, which eventually culminate in spawning (Himmelman, 1999). Barnes (1975) stated that the timing of spawning in invertebrates is independent of prior rhythmic reproductive physiology and that some
Control of Reproduction in Echinoderms
75
type of independent stimulus is required to induce gamete release. However, Giese and Pearse (1974) suggested that it might sometimes be impossible to separate the stimuli for gamete production from the actual spawning cue, since the culmination of production may itself stimulate spawning. Indeed, the identification of spawning cues is a major challenge in that it requires three types of evidence: (1) that an environmental change coincides with spawning in the field or precedes it at a fixed interval, (2) that the same change provokes animals to spawn when other conditions are maintained constant, and (3) that other factors can be eliminated as possible spawning cues. The latter point is important because numerous environmental and oceanographic factors vary in parallel. A number of methods (gonad indices, histology and microscopic examination of the gonads, oocyte size frequency distributions, and field and laboratory observations) have been used with various degrees of accuracy to determine the spawning periods of echinoderms, and different interpretations of factors that control reproduction have been proposed with more or less certainty. Analyzing the various and possibly contradicting conclusions from the different methods used is thus crucial in establishing trends and models. The three main types of data that provide evidence of spawning are: (1) deduction from the reproductive cycle (i.e., disappearance of mature gametes in serial histological sections of the gonads); (2) spawning observed in the field; (3) spawning observed in the laboratory. The first can most easily provide repeated evidence of gamete shedding when sampling protocols are properly designed, but it usually suffers from significant flaws and limitations (see Section 1 in Chapter 4), so that correlations made with mediating factors remain largely speculative. Furthermore, proximate cues that trigger gamete release on a fine scale can hardly be deduced from monthly or biweekly gonad samples. Observation of gamete release in situ is obviously the most desirable evidence of spawning because, at least under ideal conditions, it enables the simultaneous determination of social behaviour, level of synchrony and prevailing environmental conditions. However, the drawback is that such observations are typically fortuitous and/or of short duration and therefore hard to prolong or repeat in order to pinpoint the spawning cues. In most instances, only a few isolated individuals are observed to spawn, making it even more difficult to ascertain the significance of the spawning event and the mediating forces at play. Nevertheless, the rare detailed accounts of mass spawning in the field provide some of the best data available for the factors that underlie spawning periodicities. Compiling data on gamete release in the laboratory can also be a powerful tool and is perhaps the perfect compromise when the holding conditions are right (i.e., animals maintained in unfiltered running seawater under ambient conditions of light and temperature). Spontaneous breeding under appropriate captive conditions can be extremely reliable when
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Annie Mercier and Jean-Franc¸ois Hamel
spawning events are repeated and/or corroborated by observations in the field (via serial samples or direct sightings). However, because they are time and space consuming, such studies are rarely undertaken, although aquaculture settings are beginning to offer excellent opportunities. Phytoplankton (Starr et al., 1990, 1992, 1993), seawater temperature (Minchin, 1992; Selvakumaraswamy and Byrne, 2000), day length (Selvakumaraswamy and Byrne, 2000), lunar cycles (Mercier et al., 2000a, 2007), and water-borne gametes (Beach et al., 1975; Starr et al., 1990; Unger and Lott, 1994) have all been proposed to cue spawning. The role of these stimuli is presumably to orchestrate a mass spawning which should enhance fertilization success if conspecifics are in close proximity (Levitan, 1995). It is commonly assumed that variations in environmental factors that can affect sublittoral species are not as prevalent in the deep sea. For instance, photoperiodic spawning cues are often deemed to be absent in the deep ocean (Young, 2003). Although this can be debated in light of recent evidence (Baillon, Hamel and Mercier, unpublished data), deep-sea echinoderms may have developed particular reproductive synchronizers and their study is providing valuable insights for the understanding of spawning cues. Some species live in persistent herds (Young, 1994), whereas others are scattered and may exhibit very low population densities. Among the latter, many species of echinoids, holothuroids and ophiuroids form pairs and other small-scale aggregations during the breeding period (Mercier and Hamel, 2008; Tyler et al., 1992; Young, 1994, 1999; Young et al., 1992). Such aggregations have been documented more frequently in deep-sea species than in shallow-water ones (Young, 2003).
1.1. Crinoidea The factors that influence spawning in crinoids are still poorly known (Holland, 1991). Continuous reproduction is common in tropical crinoids, where cyclical exogenous stimuli are not well-defined (Nichols, 1994), although synchronized annual cycles have been reported (Mladenov and Brady, 1987). Boolootian (1966) summarized what was known of the reproductive physiology up to the mid-1960s, reporting the existence of more or less extended annual breeding periods in some 20 species of crinoids, based on the accounts of Clark (1921), Dan and Kubota (1960), and Mortensen (1920a, 1937, 1938). From these data it is apparent that different species, even in the same localities, breed at different times. Holland (1991) mentioned that when a crinoid species has a wide distribution, spawning seasons may vary significantly from one population to another; however, to date, no species has been studied intensively enough to test this possibility.
Control of Reproduction in Echinoderms
77
The very few documented spawning events are of short duration: ca. 5 min for Oxycomanthus japonicus (Kubota, 1981), 2 min for Oxycomanthus (¼Comanthus) bennetti (Meyer et al., 1984), and 25 s for Lamprometra klunzingeri (Fishelson, 1968). Spawning of all the females in a population of O. japonicus was reportedly completed within 1 h (Dan and Dan, 1941; Kubota, 1981), whereas the males spawned repeatedly over a few days, including at the exact time of female spawning (Kubota, 1981).
1.2. Ophiuroidea Periodicities in spawning events are very difficult to identify in ophiuroids. Most of the long-term evidence is indirectly derived from gametogenic cycles and direct observations of spawning has either been fortuitous or has occurred under artificial and often stressful laboratory conditions (Hendler, 1991). Patent (1969) reported that the duration of known spawning seasons for ophiuroids populations ranged from 1 month (e.g., Ophiothrix texturata; Mortensen and Lieberkind, 1928; Olsen, 1942) to 6 months in Amphiura filiformis (Mortensen and Lieberkind, 1928; Olsen, 1942) and Ophiothrix fragilis ( J. E. Smith, 1940). Ophioten sericeum reportedly spawns for 4–5 months (Thorson, 1934) and the viviparous Amphipholis squamata appears to breed throughout the year in New Zealand (Fell, 1946). Spawning in the laboratory has usually been induced by the stress of collection or subsequent light and heat shocks (Balser, 1998; Hendler, 1991; Selvakumaraswamy and Byrne, 2000). The only accounts of spawning in the natural habitat that we could find were those of Hendler and Meyer (1982) for Ophiarthum pictum on shallow reefs of the Palau Islands, Van Veghel (1994) for Ophioderma rubicundum at Curacao, Hagman and Vize (2003) for O. rubicundum and O. squamosissimum in the Gulf of Mexico (USA), and by Himmelman et al. (2008) for Ophiopholis aculeata and Ophiura robusta in the Gulf of St. Lawrence (eastern Canada). However, it is possible that general accounts of massive spawning events on tropical reefs could include ophiuroids species.
1.3. Holothuroidea Studies of spawning periodicities in holothuroids are among the most complete. Many of them have deduced spawning from long-term sampling, either from the occurrence of larvae in the field or by following the gametogenic cycle or gonad index. In such investigations, correlations with environmental factors are difficult to make due to irregular and often widely spaced samplings, and measurement of only limited environmental variables. Nevertheless, numerous experimental studies and accounts of
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spontaneous spawning in the field (Table 3.1) have contributed to the build-up of the knowledge base. Data from thorough monitoring of gamete shedding are limited. Direct observations of spontaneous spawning in the laboratory have been reported for Labidoplax buskii (Nyholm, 1951), Aslia lefevrei (Costelloe, 1985), Holothuria scabra (Hamel et al., 2001), Isostichopus fuscus (Mercier et al., 2007), and several north-eastern Pacific species (McEuen, 1988). Observations of spawning in the field have been published on IndoPacific aspidochirotids (for an early review, see Giese and Kanatani, 1987). Babcock et al. (1992) reported in situ observation of spawning for several species, that is, Actinopyga lecanora, A. miliaris, Bohadschia argus, Euapta godeffroyi, Holothuria atra, H. coluber, H. edulis, H. fuscopunctata, H. hilla, H. leucospilota, H. nobilis, Pearsonothuria (¼Bohadschia) graeffei, Stichopus chloronotus, S. variegatus and Thelenota ananas on the Great Barrier Reef (Australia) between 1978 and 1992. There are also examples from temperate regions. For instance, gamete release by Parastichopus (¼Stichopus) californicus was observed in British Columbia (Canada) on two distinct occasions (Levitan, 2002b; Pearse et al., 1988), simultaneous spawning of Cucumaria miniata and C. piperata has been recorded in situ in British Columbia (Sewell and Levitan, 1992), spawning of Cucumaria frondosa has been monitored in situ in Quebec, eastern Canada (Hamel and Mercier, 1995a), spawning of Pseudocnus lubricus (¼Cucumaria lubrica) has been documented from field observations in Puget Sound, USA (Engstrom, 1982), and the spontaneous spawning of 12 holothuroid species has been observed around the San Juan Archipelago, USA (McEuen, 1988). While a few shallow-water species reportedly display an aperiodic mode of reproduction in certain locations (Smiley et al., 1991), deep-sea holothuroids typically do not exhibit any seasonal reproduction (Walker et al., 1987). Absence of seasonality is also the norm in the brooding Antarctic species Psolus dubiosus (Gutt, 1991). However, the number of tropical/equatorial species of holothuroids for which spawning has been observed throughout the year has increased considerably in recent years. According to the review by Smiley et al. (1991), some 20 broadcast spawners within the order Aspidochirotida release gametes during the warm season, with the exception of Holothuria (¼Microthele) nobilis (Conand, 1981, 1993b). Two or more annual spawning events occur in several of these species, such as Holothuria scabra (Conand, 1993b; Hamel et al., 2001; Krishnaswamy and Krishnan, 1967; Mercier et al., 2000a), H. atra (Harriott, 1985), H. leucospilota (Hamel and Mercier, 2007), Leptosynapta tenuis (Green, 1978), Isostichopus fuscus (Mercier et al., 2007), and Stichopus chloronotus (Franklin, 1980). Most dendrochirotids broadcast their gametes between late winter and spring in temperate and cold latitudes (Boolootian, 1966; Costelloe, 1985; Hamel and Mercier, 1996c; Smiley et al., 1991). There is clear evidence from direct spawning observations that only a portion of H. scabra populations from the
Table 3.1 In situ observations of spawning in holothuroids Species
Location
Time
Details
No. of individuals
Source
Aspidochirotida Actinopyga agassizi A. echinites A. echinites
Jamaica Papua New Guinea New Caledonia
Dusk 10:00–16:00 17:00
– Scattered individuals 1/20
Hammond (1982) Shelley (1981) Desurmont (1996)
A. miliaris
New Caledonia
16:00
3/15
Conand (1989)
Bohadschia argus
Night
–
B. argus B. marmorata
Great Barrier Reef (Australia) New Caledonia Papua New Guinea
– New moon 4 days before new moon (15 February 1996) at high tide High tide and last moon quarter; also observed mid-tide and first moon quarter; day time October–January a few days after full moon Mid-tide and new moon New moon in December
Babcock et al. (1992) Conand (1993b) Shelley (1981)
B. marmorata
Palau
14:00–20:00
B. marmorata
New Caledonia
17:00
B. marmorata
La Re´union
17:00
B. similis
New Caledonia
17:00
B. similis
New Caledonia
Day time
Night 16:00
New moon and full moon in Jul–August 4 days before new moon (15 February 1996) at high tide 5 days after new moon (24 April 2004) at low tide 3 days before new moon (20 December 2003) at high tide Mid-tide and first moon quarter
– All individuals at study site Several 50% of individuals
Hendler and Meyer (1982) Desurmont (1996)
2
Rard (2004)
1
Desurmont (2004b)
–
Conand (1993b) (continued)
Table 3.1 80
(continued)
Species
Location
Time
Details
No. of individuals
Source
B. vitiensis
La Re´union
18:00
2
Durville (1998)
B. vitiensis
French Polynesia
15:00
1
Jardin (1998)
B. vitiensis
New Caledonia
15:45–17:45
New Caledonia
16:30–16:45
50% of all visible individuals 2
Desurmont (2005)
B. vitiensis B. vitiensis
La Re´union
15:30–18:15
1 initially, spreading to 20 after an hour
Gaudron (2006)
Holothuria coluber
Lizard Island (Australia) New Caledonia Lizard Island (Australia)
09:00–17:00
Full moon (15 February 1995) at low tide 4 days after full moon (27 January 1997) 3 days before full moon (24 November 2004) 4 days after new moon (11 June 2005) at low tide 6 days after full moon (19 February 2006) at ebb tide 3 days after full moon (11–12 January 1993) Last moon quarter 1 day before third moon quarter (16 December 1993) After episode of heavy rain (23 September 2000) – April New moon in November– December 2 days after first moon quarter 3 days before full moon (24 November 2004) – 2–4 days after new moon (27 June to 3 July 2003)
50% of individuals
Uthicke (1994)
2/2 2
Conand (1989) Uthicke (1994)
Several of both sexes
Putchakarn (2001)
– 1 male Scattered individuals
Hammond (1982) Sloan et al. (1979) Shelley (1981)
–
Conand (1993b)
1
Desurmont (2005)
– Several
Hammond (1982) Valls (2004)
H. flavomaculata H. fuscopunctata H. impatiens
16:00 16:30
H. mexicana H. nobilis H. scabra
East coast of Thailand Jamaica Aldabra Papua New Guinea
Afternoon Dusk – 16:00
H. scabra versicolor
New Caledonia
–
H. scabra versicolor
New Caledonia
15:45–17:45
H. thomasi H. tubulosa
Jamaica Eastern Spain
Dusk 15:00
Desurmont (2006)
H. tubulosa
Aegean Sea
16:00–17:00
H. tubulosa
Azores
18:30–19:30
H. whitmaei
Coral Bay (Western Australia) Jamaica Woodlands Bay (BC, Canada)
–
Isostichopus badionotus Parastichopus (¼Stichopus) californicus
Dusk –
P. californicus
Vancouver Island (BC, Canada)
P. californicus
Vancouver Island (BC, Canada)
–
Pearsonothuria (¼Bohadschia) graeffei P. graeffei
Great Barrier Reef (Australia)
Late afternoon
Lizard Island (Australia)
16:30
Over several years: 3–4 days before full moon, 5–6 days after new moon, 2 days before full moon, 5 days after full moon July and August in several years. Often just before full moon August 2002, January 2003 and April 2003 – June and July with increased daily bright sunshine and phytoplankton bloom Long sunny period, phytoplankton bloom, synchronized with three echinoid species (Strongylocentrotus) High tide, 1 day after full moon. Synchronized with Pearsonothuria graeffei –
Few isolated spreading to others
Moosleitner (2006)
Several
Bertoncini et al. (2008)
1–12 males – –
Wolkenhauer and Shiell (2008) Hammond (1982) Cameron and Fankboner (1986)
–
Levitan (2002a)
–
Pearse et al. (1988)
–
Conand (1989)
3 days before first moon quarter (29 December 1992)
1
Uthicke (1994)
81
(continued)
82
Table 3.1 (continued) Species
Location
Time
Details
No. of individuals
Source
P. graeffei
Lizard Island (Australia)
16:15
4
Uthicke (1994)
P. graeffei
17:00–18:00
Several
Purwati (2003)
Late afternoon
26 May 2003
Several
Hill et al. (2008)
Late afternoon 15:10 Night
8 (15%)
Hill et al. (2008) Hill et al. (2008) Babcock et al. (1992) Uthicke (1994)
1
Uthicke (1994)
14 (20%)
Uthicke (1994)
8
Uthicke (1994)
1
Desurmont (2004a)
S. chloronotus
La Re´union
Several
S. hermanni
New Caledonia
09:00 and 17:00–1830 17:30
1
Barre`re and Bottin (2007) Desurmont (2003)
S. hermanni
New Caledonia
1700–1830
7 June 2005, new moon 5 November 2007 November and January, 2–3 days after full moon 2 days after full moon (12 November 1992) 3 days after full moon (13 November 1992) 2 days after full moon (12 December 1992) 3 days after full moon (11 January 1993) 2 days after full moon (11 December 2003) at low tide 3 days after full moon (7 December 2006) 4 days before full moon (12 February 2003) at high tide 7–9 January 2008 (new moon ¼ 8 January) close to high tide
A few 2 –
S. chloronotus
Anambas Islands, South China Sea Northern Mozambique Maldives Seychelles Great Barrier Reef (Australia) Lizard Island (Australia) Lizard island (Australia) Lizard Island (Australia) Lizard Island (Australia New Caledonia
2 days after third moon quarter (16 February 1993) 13–14 March 2002
1–3
Desurmont (2008)
P. graeffei P. graeffei P. graeffei Stichopus chloronotus S. chloronotus S. chloronotus S. chloronotus S. chloronotus
18:00–18:30 18:30 18:30 18:40 18:30
S. variegatus
Great Barrier Reef (Australia) Lizard Island (Australia) Lizard Island (Australia) Great Barrier Reef (Australia)
Afternoon and night 17:30
San Juan Archipelago (WA, USA)
Daylight
C. frondosa
St. Lawrence Estuary (eastern Canada)
C. miniata
Barkley Sound (BC, Canada)
05:00 (sunrise) (males first) and until 08:00 h the next day for females Daylight
C. miniata
San Juan Archipelago (WA, USA)
–
C. piperata
San Juan Archipelago (WA, USA)
Daylight
C. piperata
Barkley Sound (BC, Canada)
Daylight
S. variegatus S. variegatus S. variegatus
Dendrochirotida Cucumaria fallax
17:40 End of afternoon
83
1–3 days after full moon
–
1 day after new moon (25 November 1992) 2 days after new moon (26 November 1992) 4 days after new moon
–
Babcock et al. (1992) Uthicke (1994)
Several
Uthicke (1994)
–
Conand (1989) also Conand (1993b)
March–May with abundance of phytoplankton Low tide, low current, phytoplankton bloom, increased temperature in mid-June
Several males and females
McEuen (1988)
ca. 100% of individuals
Hamel and Mercier (1995a)
High synchrony between individuals and sexes, correlation with phytoplankton bloom and slack tide March–May with phytoplankton blooms, sunny days February–May with abundance of phytoplankton Correlated with phytoplankton bloom and slack tide
Large numbers of both sexes
Sewell and Levitan (1992)
Several
McEuen (1988)
Several males and females
McEuen (1988)
Two males
Sewell and Levitan (1992) (continued)
Table 3.1
(continued)
Species
Location
Time
Details
No. of individuals
Source
C. populifera
San Juan Islands (WA, USA) Puget Sound (USA)
–
February after 2 days of sun
Several males
McEuen (1988)
Males 11:30– 14:00; females 16:30–18:00 11:00–15:00
Low or slack tide
Several
Engstrom (1982)
Several males and few females
McEuen (1986); McEuen (1988)
–
December–January after several days of sun and phytoplankton bloom April, males spawn first
–
Early morning
March–June
Several males and females
Young and Chia (1982) McEuen (1988)
Night
October–December close to full moon November
–
Leptosynapta clarki
Great Barrier Reef (Australia) West Coast (USA)
Opheodesoma spectabilis
Hawaii (USA)
Evening
Pseudocnus lubricus (¼Cucumaria lubrica) P. lubricus Psolus chitonoides P. chitonoides Apodida Euapta godeffroyi
San Juan Archipelago (WA, USA) San Juan Islands (WA, USA) San Juan Archipelago (WA, USA)
–
Changes in light intensity in September
2–4 grouped individuals Several, grouped individuals
Babcock et al. (1992) Everingham (1961) Berrill (1966)
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Solomon Islands and I. fuscus from the coast of Ecuador spawns monthly (Hamel et al., 2001; Mercier et al., 2000a, 2004, 2007). Both locations are close to the equator. A variety of environmental factors influences holothuroid spawning (see Table A6 for a complete list), including seawater temperature (Conand, 1981; Tanaka, 1958), photoperiod (Cameron and Fankboner, 1986; Conand, 1982), water velocity (Engstrom, 1980), salinity (Krishnaswamy and Krishnan, 1967), a combination of seawater temperature and photoperiod (Costelloe, 1985), the lunar cycle (Mercier et al., 2007) and phytoplankton blooms (Hamel et al., 1993). The in situ study of spawning in Cucumaria frondosa (Hamel and Mercier, 1995a) has revealed that various regulatory factors may be acting on different time scales. There was a good correlation of spawning with phytoplankton abundance on an annual scale, but gamete release actually took place at sunrise during low tide when temperature and light were increasing markedly (Fig. 3.1). Laboratory experiments were not successful in stimulating spawning of ripe specimens by means of phytoplankton from the study site. However, spawning was triggered by a progressive increment in temperature and a rapid increase in light intensity, mimicking conditions at sunrise in the field (Hamel and Mercier, 1995a). Combining these data from field and laboratory settings suggests a synergistic effect of numerous factors, such as availability of phytoplankton, tidal/current conditions, temperature, time of day and inter-individual communication (via sperm or pheromones).
1.4. Asteroidea Spawning periodicities in the class Asteroidea have been studied extensively. Field observations of gamete release have been reported for Asterias amurensis in Japan (Ino et al., 1955), A. forbesi (Loosanoff, 1964) and Leptasterias littoralis (O’Brien, 1976) in the USA, Patiriella regularis in New Zealand (Byrne and Barker, 1991) and Acanthaster planci in Australia. Accounts of spontaneous spawning in many species of asteroids in nature have been provided by Pearse et al. (1988) and Minchin (1987, 1992). The former reported having seen one Dermasterias imbricata, one Orthasterias koehleri, one Pisaster brevispinus and six Stylasterias forreri and other echinoderms releasing gametes simultaneously in Barkley Sound (BC, Canada). The latter observed the simultaneous spawning of the sea stars Marthasterias glacialis and Asterias rubens off Ireland, and spawning of A. rubens (¼vulgaris) was recently observed by Raymond et al. (2007) and described in detail by Himmelman et al. (2008) in the Gulf of St. Lawrence (eastern Canada). Natural spawning in the laboratory has been observed in Asterias forbesi (Costello and Henley, 1971), Leptasterias sp. (Pearse and Beauchamp, 1986), L. hexactis (Chia, 1968), L. polaris (Boivin et al., 1986; Hamel and Mercier, 1995b), L. pusilla (Smith, 1971), Ophidiaster granifer (Yamaguchi and Lucas,
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Wind velocity (km/h)
Chlorophylla (mg/m3)
Temperature (⬚C)
Spawning period 7 6 5 4 3 2 1 4 3.5 3 2.5 2 40
Coast line (north)
20 0 20 40
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Tidal elevation (m)
Current velocity (cm/sec)
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5 4 3 2 1 7.5 5 2.5 0 2.5 5 7.5
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100 75 50
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25 0
10 12 14 16 18 20 22 24 2
16 June
4
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Time (h)
Figure 3.1 Cucumaria frondosa (Holothuroidea). Changes in water temperature, chlorophyll a concentration, wind velocity, water transparency, current direction and velocity, and tide level recorded in situ every hour during the mass spawning of males and females in eastern Canada. The number of spawning individuals is expressed as a percentage of the total number of individuals observed during a given dive. Reprinted with permission from Hamel and Mercier (1995a).
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1984), Patiriella parvivipara (Keough and Dartnall, 1978), Pisaster ochraceus (Pearse and Eernisse, 1982; Pearse et al., 1986a), Protoreaster nodosus (Scheibling and Metaxas, 2008), Pteraster militaris (McClary and Mladenov, 1988) and Smilasterias multipara (Komatsu et al., 2006). It was also reported in the Antarctic species Odontaster validus (Pearse and Bosch, 2002), O. meridionalis and Porania antarctica (Bosch and Pearse, 1990), as well as in the bathyal asteroid Henricia lisa (Mercier and Hamel, 2008).
1.5. Echinoidea Apart from histology-based estimations, most data available on spawning in echinoids are derived from artificial induction with potassium chloride (KCl) injections, which do not always allow the reliable determination of true periodicities and mediating factors. Although the results cannot necessarily be equated to natural spawning rhythms, KCl injections have been used to determine readiness to spawn in the field and in the laboratory (e.g., Dotan, 1990; Levitan, 1988; Muthiga, 2005). Among the most complete records of spontaneous gamete release are those of a mass synchronous spawning of Evechinus chloroticus in Doubtful Sound, New Zealand (Lamare and Stewart, 1998), three Strongylocentrotus species monitored by Levitan (2002b) off the coast of British Columbia (western Canada), and in situ observations of S. droebachiensis recently reported by Himmelman et al. (2008) in eastern Canada. Furthermore, the presence of sperm in the water (i.e., male spawning) was established by fertilization trials conducted in the field along the coast of Maine, USA (Gaudette et al., 2006). Very fragmentary information comes from the observation of a single female S. droebachiensis shedding gametes in western Canada (Pearse et al., 1988) and of one male Phyllacanthus imperialis spawning at Lizard Island (Australia) (Olson et al., 1993).
2. Correlation with Exogenous Factors 2.1. Photoperiod and light intensity Giese and Pearse (1974) noted that day length is often considered an ideal synchronizer for biological events because it is so invariant from year to year for the same latitude and the same period. The farther the position from the equator, the greater the seasonal difference in day length and the more probable that photoperiod could serve as a cue for season. Conversely, day length is unlikely to serve this purpose at the equator, where photoperiod varies little throughout the year (Giese and Pearse, 1974). Himmelman (1999) agreed that photoperiod is the most predictable seasonal signal and noted that experimental studies on a number of marine
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invertebrates have shown that this is the major factor determining when gonad development occurs (see Section 2 in Chapter 2). However, while photoperiod may control the annual component of the reproductive cycle of predictable spawners, other factors (e.g., lunar, tidal, temperature, phytoplankton and diel cycles) appear better suited to determine the precise timing of gamete release. In other words, photoperiod is an unlikely spawning cue in species that spawn annually in a particular season but at different times from year to year (Himmelman, 1999). Correlative and experimental studies show that diel dark–light cycles determine the precise timing of gamete or larval release for a number of species (see Section 2.2). 2.1.1. Ophiuroidea No study to date has investigated the possible role of day length or other light cue on brittle star reproduction, although variation in light and dark exposure has been used to induce spawning in Ophiopholis aculeata (Balser, 1998). Among the rare accounts, Morgan and Jangoux (2002) determined that long days >15 h are essential for spawning in Ophiothrix fragilis. 2.1.2. Holothuroidea Binyon (1972) has stated that many holothuroids probably spawn in response to an increase in the intensity of ambient light. Spawning in Parastichopus (¼Stichopus) californicus in the field was almost exclusively observed after periods of bright sunshine, and phytoplankton was abundant during some spawnings in British Columbia, Canada (Cameron and Fankboner, 1986). McDaniel (1982) reported a similar occurrence of large numbers of P. californicus spawning in the early spring, coincident with a period of bright sunshine and the presence of a phytoplankton bloom. Spawning in response to variations in light intensity has been reported in the sea cucumber Cucumaria frondosa from eastern Canada (Hamel and Mercier, 1995a). 2.1.3. Asteroidea The summer solstice was proposed as an environmental spawning cue in Coscinasterias muricata at Governor’s Reef (Australia) based on gonad indices and measures of oocyte size frequency, individuals appearing to spawn or be ready to spawn around this period both in 1999 and 2000 (Georgiades et al., 2006). However, the authors also noticed that the main spawning event coincided with the lowest seawater temperatures in September and were unable to distinguish between the effects of the two factors. 2.1.4. Echinoidea Byrne et al. (1998) suggested that spawning in the sea urchin Centrostephanus rodgersii coincided with short days and lunar conditions associated with the winter solstice in New South Wales (Australia). Spirlet et al. (1998) noted
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that spawning in a population of Paracentrotus lividus in Southern Brittany (France) is usually initiated when the day length reaches 15 h and periodically occurs when both day length and temperature are high. Spawning apparently ends as day length starts declining and temperatures reach a peak. Either factor or a combination of both could be a signal for the end of the breeding activity.
2.2. Time of day The day/night cycle, a component of the light regime, is one of the most obvious factors to affect spawning directly. However, this factor can only be investigated by monitoring gamete release, not through indirect sampling methods, and generates data that can be anecdotal if observations are fortuitous rather than planned. 2.2.1. Crinoidea Bury (1888) and Seeliger (1892) reported spawning around 07:00–08:00 h in Antedon rosacea. In captivity, Heterometra savignyi spawned around 15:00 h and Lamprometra klunzingeri around 19:00 h (Mortensen, 1937, 1938). Using underwater time-lapse video, Meyer et al. (1984) observed an individual of Oxycomanthus bennetti releasing gametes for ca. 2 min just after dark (i.e., 18:04–18:05 h) on the Great Barrier Reef in Australia. Two other species, L. klunzingeri (Fishelson, 1968) and Capillaster multiradiatus (Hendler and Meyer, 1982) also spawn near dusk at around the same time according to field observations. In one of the most thoroughly investigated species, Oxycomanthus japonicus, spawning in the field and in the laboratory was consistently observed between 14:30 and 16:00 h (Dan and Dan, 1941; Dan and Kubota, 1960; Kubota, 1981), while ovulation was noted a few hours earlier, at ca. 12:00 h (Holland and Dan, 1975; Kubota, 1981). 2.2.2. Ophiuroidea Because many ophiuroids spawn at night, both the time of day and light intensity have been proposed as spawning cues (Grave, 1916; Hendler, 1991; Hendler and Meyer, 1982; Patent, 1969; Selvakumaraswamy and Byrne, 2000). Most reported spawning events occurred shortly after sunset: Grave (1898) observed spawning of Ophiocoma echinata, Ophiura brevispina, and Ophiopholis aculeata between 20:00 and 22:00 h in Jamaica; Patent (1969) observed spawning of Gorgonocephalus caryi between 19:00 and 21:00 h in the San Juan Islands (USA); and Hagman and Vize (2003) reported that Ophioderma rubicundum and O. squamosissimum from the north-western Gulf of Mexico (USA) spawned exclusively at night, approximately 1–1.5 h after sunset. Species that have spawned nocturnally in the laboratory include: Amphioplus abditus, Gorgonocephalus caput-medusae, Gorgonocephalus eucnemis, Hemipholis elongate, Ophiocoma echinata, Ophiocoma
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pica, Ophiocoma pumila, Ophioderma cinereum, Ophiopholis aculeata, Ophiothrix orstedii and Ophiothrix propinqua (reviewed by Hendler, 1991). In contrast, massive spawning of Ophiactis resiliens and Ophiothrix spongicola in Australia occurred both during the day and at night (Selvakumaraswamy and Byrne, 2000), although some of these observations could have been influenced by capture, transport and laboratory conditions. Mass spawning events of Ophiopholis aculeata and Ophiura robusta were observed in the northern Gulf of St. Lawrence, eastern Canada, in the morning and in the afternoon (Himmelman et al., 2008; J.-F. Hamel, personal observation). Experiments on spawning induction also suggest a sensitivity to light intensity or time of day. Selvakumaraswamy and Byrne (2000) found that the brittle star Ophionereis schayeri could be induced to spawn in late evening and during the night. They also reported that Ophiarthrum pretum spawned after dark and interrupted gamete release when stimulated by artificial lights. 2.2.3. Holothuroidea Hyman (1955) postulated that most holothuroids spawned in late afternoon, evening, or at night. Extensive data compiled by McEuen (1988) showed that most low-light spawners are aspidochirotids (see Table 3.3 therein): 14 of the 26 species known to spawn in the laboratory or in the field late in the day or at night are aspidochirotids, 12 of them having tropical distributions. The only exceptions in data for aspidochirotids are: (1) isolated individuals of Holothuria scabra spawning in the field at 10:00 h (Shelley, 1981) and (2) a few Stichopus tremulus spawning in the morning after collection (Holland, 1981b). It has therefore been postulated that spawning of aspidochirotid populations in late afternoon, evening and night may be in response to lower light intensity (McEuen, 1988). Recent accounts of sea cucumber spawning in situ indicate that most aspidochirotid species spawn late in the afternoon (Table 3.1). James (1994a,b) noted that males H. scabra usually spawned around 10:00 h and females around 14:00 h. The slightly more diurnal spawning habit of H. scabra compared with other aspidochirotids is also reported by MPEDA (1989) with most oocytes released around 15:00 h, though Battaglene (1999a) reported that spontaneous spawners released their gametes between 15:00 and 18:00 h. Light as a proximate trigger of spawning has also been suggested for Thyone briareus (Conand, 1981). One of the oldest records mentions that gamete release in T. briareus always occurred late in the afternoon in conditions of dim light (Ohshima, 1925). However, this species was later observed to spawn under various natural and artificial light conditions, as well as in total darkness (Colwin, 1948), therefore questioning the role of light as a spawning cue. Babcock et al. (1992) reported that Actinopyga lecanora, Bohadschia argus, Euapta godeffroyi, Holothuria atra, H. coluber, H. edulis, H. fuscopunctata, H. hilla, H. nobilis, Pearsonothuria (¼Bohadschia) graeffei, Stichopus chloronotus,
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S. variegatus and Thelenota ananas on the Great Barrier Reef in Australia generally spawned in the late afternoon or in the evening, although mid-day episodes were noted for A. miliaris and H. leucospilota. A long-term study of Isostichopus fuscus along the coast of Ecuador revealed that gamete release, which was observed on 99 separate occasions, invariably took place around sunset (Mercier et al., 2007) (Fig. 3.2). Males always spawned first followed shortly by females suggesting that, unlike males, females do not necessarily react to the day–night cycle but may rely on communication between individuals (Mercier et al., 2007). Among dendrochirotids, light is a potential spawning cue for Leptopentacta elongata (Chia and Buchanan, 1969) and Psolus chitonoides (McEuen, 1988). Evidence that the latter responds to increases in light intensity includes the release of gametes when ripe individuals were exposed to higher light levels, morning spawnings recorded in laboratory tanks on sunny days, and a field sighting of free-spawning during late morning (McEuen, 1988). Conversely, spawning of Aslia lefevrei takes place only in low light or complete darkness, that is, in the evening, at night or in the early morning (Costelloe, 1985). Eupentacta chronhjelmi also spawns between midnight and early morning (04:00 h) under laboratory conditions in Japan at ambient seawater temperatures (12 C) (Catalan and Yamamoto, 1994),
Number of spawning individuals
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Sunset
Male Female
15
10
5
0 18:10:00
18:30:00
18:50:00
19:10:00
19:30:00
19:50:00
20:10:00
Time of day
Figure 3.2 Isostichopus fuscus (Holothuroidea). Spawning event recorded on 15 April 2002, showing the number of males and females releasing gametes over time. Reprinted with permission from Mercier et al. (2007).
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and Eupentacta quinquesernita spawns in low light, although earlier in the night than E. chronhjelmi, between 17:00 and 24:00 h (McEuen, 1988). In situ monitoring showed that spawning of the sea cucumber Cucumaria frondosa in the lower St. Lawrence Estuary (eastern Canada) began at sunrise and continued until the middle of the afternoon (Hamel and Mercier, 1995a). The highest number of spawning individuals was recorded at 15:00 h. Conditions mimicking sunrise (increasing temperature and light intensity) successfully triggered spawning in the laboratory (Hamel and Mercier, 1995a). 2.2.4. Asteroidea The sea star Marthasterias glacialis was observed to spawn during the afternoon and early evening between 13:30 and 21:30 h on sunny days during July and August in Lough Hyne and Mulroy Bay, Ireland (Minchin, 1987). Byrne and Barker (1991) reported in situ observation of males and females of Patiriella regularis spawning in Otago Harbour (New Zealand) in January 1990. These individuals were located 0.5–5 m from each other and spawning coincided with sunlit conditions and slack tides. On the Great Barrier Reef (Australia), massive spawning of Acanthaster planci started at 21:54 h and continued for ca. 2 h (Babcock and Mundy, 1992). The authors also reported the spawning of Linckia laevigata during the same night and noted several instances of A. planci spawning between early afternoon and late evening (Babcock and Mundy, 1992). Gladstone (1992) also observed in situ spawning of A. planci in the Whitsunday region of the Great Barrier Reef, individuals spawning in the afternoon during ebb tide, 2 days after the spring tide. Himmelman et al. (2008) observed several mass spawnings of Asterias rubens (¼vulgaris) while diving in eastern Canada, both in the morning and in the afternoon. Yamaguchi and Lucas (1984) indicated that spawning of Ophidiaster granifer from Guam occurred during the night under laboratory conditions. Several temperate species from eastern Canada, including Solaster endeca, Crossaster papposus, Asterias rubens (¼vulgaris), Pteraster militaris and Henricia sanguinolenta, spawned during the day under natural photoperiod in tanks supplied with ambient unfiltered flowing seawater (Hamel and Mercier, unpublished data). 2.2.5. Echinoidea Olson et al. (1993) observed one male Phyllacanthus imperialis spawning during the night at Lizard Island (Australia), with several other individuals lying on the top of coral heads or on rubble. Pearse et al. (1988) recorded gamete release in one individual of Strongylocentrotus droebachiensis in the afternoon off Vancouver Island (western Canada), whereas large numbers of the same species spawning between 09:00 and 10:00 h in the Gulf of St. Lawrence (eastern Canada) in 2003 (Himmelman et al., 2008).
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2.3. Temperature While it is generally agreed that temperature plays a role in the early development of marine invertebrate larvae and is therefore significant in the timing of the reproductive cycle, some authorities believe that it has no direct influence on spawning (Barnes, 1975; Giese, 1959a; Giese and Pearse, 1974). On the other hand, temperature is among the factors most often discussed as a potential spawning cue in the literature, especially since temperature changes in the laboratory can often induce mature animals to shed gametes (e.g., see review by Himmelman, 1999). It should, however, be noted that temperature shocks such as those used in vitro are unlikely to occur in vivo, except perhaps during rapid upwelling or downwelling events. Despite the emphasis placed on temperature as a spawning cue, the number of accounts providing convincing evidence of the role of temperature in gamete release remains low. One possible weakness is the lack of concurrent data on other environmental factors, for example, abrupt or unnatural temperature fluctuations can result in variations in water chemistry. Experimental studies have demonstrated that in numerous species gametogenesis can be stimulated by an increase in temperature (see Section 2.1 in Chapter 2), but few studies have shown that gamete release occurs when a particular temperature is attained (e.g., Hamel and Mercier, 1995b; Mercier and Hamel, 2008), although many have provided evidence that spawning coincides with significant temperature variation (reviewed by Himmelman, 1999; Himmelman et al., 2008). 2.3.1. Crinoidea Kubota (1981) proposed a dual role of the lunar cycle and surface seawater temperature in the regulation of the annual spawning in Oxycomanthus japonicus in Japan. Spawning occurs only when the temperature drops below 22 C, which explains the choice of first of last quarter moon when both occur during the breeding season between late September and early October. Dimelow (1958) noted that an abrupt change in seawater temperature could induce spawning in Antedon bifida in the laboratory. 2.3.2. Ophiuroidea The most common environmental factor associated with spawning in ophiuroids is temperature. However, Hendler (1991) indicated in his review that evidence for the role of temperature in reproduction was generally ambiguous. This statement is still valid today, demonstrating the lack of experimental studies. While it is clear that temperature may constrain certain reproductive processes, seasonal changes in other environmental factors such as photoperiod and food availability are certainly important (Barnes, 1975) especially since they are synergistic in many environments.
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Notwithstanding the lack of experimental evidence, temperature is considered to be the principal spawning cue, particularly for species that exhibit discrete seasonal cycles (Bowmer, 1982; Fenaux, 1970, 1972a; Hendler and Tyler, 1986; Stancyk, 1974; Tyler, 1977). Rumrill (1984) suggested that three species of brittle stars from the coast of California (USA) could synchronize their breeding seasons using temperature as a proximate cue, with different results for each species. It is often proposed that the release of gametes is timed to correspond with optimal temperature for larval development (Fenaux, 1968; Runnstro¨m, 1927). For instance, Byrne (1991) suggested that spawning and brooding in Ophionereis olivacea may be cued by exogenous factors such as seawater temperature and day length in such a way as to release the juveniles at an optimal period for their survival. The similarity of temperature during corresponding phases of the reproductive cycles of Ophioderma longicauda (Fenaux, 1972a) and O. brevispinum suggests temperature governs the processes of gonadal growth and spawning (Hendler and Tyler, 1986). The importance of temperature in the timing of the reproductive cycle is further supported by comparative observations on the reproduction of different populations of O. brevispinum made by Hendler and Tyler (1986). Periods of gonadal growth and spawning were short in a northern population (Hendler and Tyler, 1986) and much longer in a southern population (Stancyk, 1974), suggesting that warmer waters can extend growth and spawning phases. Furthermore, four tropical species of Ophioderma display longer growth and spawning phases than their temperate congeners (Hendler, 1979). After noting that spawning of ophiuroids from tropical shallow regions typically occurred during the warm months (spring–summer), Hyman (1955) suggested a relationship with increased seawater temperature. Spawning of Ophiura albida in different locations (e.g., North Sea, Denmark and Bristol Channel, UK) was later reported to occur only when the temperature exceeded 12.5 C (Rees, 1954; Thorson, 1946; Tyler, 1977). Similarly, Morgan and Jangoux (2002) found that Ophiothrix fragilis spawned only at temperatures 16 C. Gamete release in many other species coincides with periods of temperature maxima or seasonal increases in temperature: Ophiothrix longipeda (Stephenson, 1934), Ophiocantha bidentata (Kaufmann, 1974), Ophionotus hexactis (Morison, 1979), Amphiura filiformis (Bowmer, 1982). The spawning cue in Ophiothrix fragilis from France may be the maximum annual temperature, although this has not been demonstrated unequivocally (Davoult et al., 1990; Gounin and Richard, 1992). On the other hand, temperature decreases and minima have also been correlated with spawning in ophiuroids. Blake (1978) determined that Ophiopholis aculeata spawned during a period of falling temperature in Maine (USA) and Newfoundland (Canada). McClintock et al. (1993) observed that spawning in the basket star Asteroporpa annulata was correlated
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with decreasing seawater temperature in the northern Gulf of Mexico. Stewart and Mladenov (1995) found a correlation between a rapid drop in temperature and spawning in Astrobrachion constrictum in May–June in Fiordland (New Zealand). To our knowledge, the only experimental evidence to support the role of temperature variation as a spawning cue has been provided by Yamashita (1983, 1985), who found that spawning in Amphipholis kochii could be induced by lowering seawater temperature and increasing it back to ambient. Correlative studies have shown inconsistent responses to ambient seawater temperature, spawning occurring either during increasing and decreasing temperature or at different temperatures every year, suggesting that spawning may coincide with optimal temperature for larval development (Hendler, 1991). Adding to the confusion, some species spawn at comparable seawater temperatures throughout their distribution, while others do not. For instance, Ophiopholis aculeata spawns at 6.5–7 C in Alaska (Taylor, 1958) and at 5.5–6 C farther north in the White Sea (Mileikovsky, 1960). However, temperature during spawning of Amphiura chiajei, Ophiocoma echinata and Ophiura albida may differ by at least 8 C over a much shorter distance between populations (Hendler, 1991). Tyler (1976, 1977) found that O. albida spawned when ambient temperatures reached 12.5 C in each year of a 2-year study, while O. ophiura spawned at different temperatures each year. Hendler (1979) considered that so-called ultimate factors could not be solely responsible for the patterns of maturation which he observed in nine species of Panamanian ophiuroids. He did not establish a correlation between spawning and temperature because conspecifics from the Atlantic and Pacific coasts of Panama (i.e., subject to different regimes of temperature and salinity) spawned simultaneously. Nevertheless, Himmelman et al. (2008) compiled several in situ observations of mass spawning in Ophiopholis aculeata and Ophiura robusta from eastern Canada and noted that they coincided with major seawater temperature increases caused by downwelling of warm surface water into deeper strata. 2.3.3. Holothuroidea Very little solid data have been published on the role of temperature in the spawning of holothuroids, although there are numerous accounts of breeding periods coinciding with the highest or lowest sea surface temperatures, or with periods of increasing or decreasing seawater temperature. Some of the major assumptions reported in the literature are outlined below. Smiley et al. (1991) compiled the spawning periods of several species of holothuroids. They found that in temperate regions, 84% of free-spawning and 73% of brooding shallow-water species spawned for 2–3 months during the warm season, as did 83% of the shallow-water tropical species (Smiley et al., 1991).
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Nyholm (1951) made field observations of the hermaphrodite Labidoplax buskii in Gullmar Fjord (Sweden) over 3 years as well as some laboratory observations. He noted a peak spawning season in November–December when seawater temperatures were around 9–11 C, and reported that the optimum temperature for spawning and development in the laboratory was also 9 C. A mid-summer lag in the reproduction of Leptosynapta tenuis occurred during the period of highest temperature in North Carolina, eastern USA (Green, 1978). Spawning of Aslia lefevrei in Galway Bay (Ireland) is also influenced by temperature, as well as light intensity (Costelloe, 1985), which makes it difficult to determine whether certain temperature conditions or fluctuations are required for spawning to occur. Temperature at the study site did not change suddenly during the peak spawning period, but it did increase from values recorded earlier during winter (Costelloe, 1985). Conand (1981) stated that Holothuria (¼Microthele) fuscogilva and Thelenota ananas spawned during the warm season in New Caledonia. Conand (1982) also correlated the reproduction of Actinopyga echinites with the warm season. However, H. (¼Microthele) nobilis from New Caledonia (Conand, 1981) and H. kefersteini from Panama (Mortensen, 1921) all spawned during the cooler months. Spawning of Holothuria scabra is reportedly tied to temperature variations in New Caledonia (Conand, 1990, 1993b), the Philippines (Ong Che and Gomez, 1985), Indonesia (Tuwo, 1999), and Australia (Harriott, 1982). Moiyadeen (1994) reported that a combination of factors, including temperature change, salinity and food availability could trigger spawning of H. scabra in Sri Lanka. Observations of gamete shedding in various species have led investigators to make purely circumstantial correlations. For instance, Tanaka (1958) proposed that temperature was a key factor in the spawning of Apostichopus (=Stichopus) japonicus and other holothuroids based on his own observation that seawater temperature varied between 12 and 22 C during the spawning season and on similar accounts for other species, for example, Caudina chilensis (Inaba, 1930) and Thyone briareus (Colwin, 1948), which also spawned roughly when temperatures were between 15 and 20 C. Despalatovic et al. (2004) came to similar conclusions for Holothuria tubulosa in the Adriatic Sea, where spawning coincided with the rising seawater temperature, especially when it increased from 22 to 26 C. Thermal shock remains the most common method used to induce spawning in holothuroids (Dolmatov and Yushin, 1993; Hamel and Mercier, 2004; Hamel et al., 2001; James, 1994a; Pitt and Duy, 2004; Smiley et al., 1991; Sui, 2004; Wang and Yuan, 2004; Yanagisawa, 1998). Moreover, conditions replicating sunrise (increasing temperature and light intensity) can successfully trigger spawning of ripe Cucumaria frondosa in the laboratory (Hamel and Mercier, 1995a). However, the significance of this
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remains unclear since the mechanism(s) through which this stimulus promotes ovulation and spawning is still not known (McEuen, 1987; Ramofafia et al., 1995). 2.3.4. Asteroidea Spawning of Asterias forbesi from Long Island Sound (eastern USA) began when seawater temperature was approximately 15 C, which is normal for the middle of June (Loosanoff, 1964). Franz (1986) found that the same species in the same location spawned when the bottom temperature was between 16 and 18 C. Costello and Henley (1971) maintained gravid A. forbesi and A. rubens (¼vulgaris) in tanks of refrigerated seawater and then induced them to spawn by increasing the temperature to room temperature (ca. 20 C). Hancock (1958) noted that individuals of A. rubens (¼vulgaris) around Essex (UK) spawned synchronously when the seawater temperature reached ca. 15 C. In a study by Keough and Dartnall (1978) on the brooding species Patiriella parvivipara under laboratory conditions, individuals kept for 2 months at 15 C exhibited little activity, whereas those at 20–23 C were induced to reproduce and all animals produced young over 7 days. Animals kept at 12 C and subjected to a rise of similar magnitude produced no young. The results suggest that a temperature of 20–23 C, rather than merely a rise in temperature, acts to stimulate emergence of juvenile (Keough and Dartnall, 1978). The spawning of male Leptasterias littoralis in Maine (USA) preceded that of females and is probably induced by the decrease of seawater temperature (O’Brien, 1976). O’Brien (1976) collected several L. littoralis during the pre-spawning period when the sea temperature was around 9 C. Some of them were exposed to a slow decrease of 4 C and the others kept at 12 C. The first group spawned synchronously whereas the second did not, suggesting that temperature below 9 C induced spawning. Spawning in Leptasterias polaris from eastern Canada also appears to be correlated with decreasing temperature (Hamel and Mercier, 1995b). In this experimental study, breeding aggregations were observed among all sea stars that were exposed to seasonal changes in seawater temperature under natural flow-through conditions, both in darkness and under the natural photoperiod. Gamete release occurred when the temperature decreased to ca. 2 C. This lower temperature may have triggered or facilitated the release of hormones through a pathway otherwise inhibited and favoured the formation of breeding clumps, followed by spawning (Hamel and Mercier, 1995b). Minchin (1987) concluded that the rapid increase in seawater temperature was of importance in synchronizing spawning in Marthasterias glacialis from the coast of Ireland. Although M. glacialis occurs at various depths,
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it generally spawns only at depths less than 4 m, where the increase in temperature is greatest (Minchin, 1987). Seasonal breeding of Patiriella gunnii and P. calcar in south-eastern Australia may be cued by the annual temperature and day length cycles (Byrne, 1992). Temperature may serve as a proximate cue for the onset of spawning as gamete release started when sea temperatures increased and terminated well before the maximum temperature was reached, P. gunnii spawning out at 19–20 C (Byrne, 1992). Stewart and Mladenov (1995) reported a weak correlation between the spawning time and a drop in seawater temperature in Astrobrachion constrictum in Doubtful Sound, southern New Zealand. According to histological examination of the gonads and gonad indices, the main spawning events in Coscinasterias muricata at Governor’s Reef (Australia) coincided with the lowest seawater temperatures, in September (Georgiades et al., 2006). However, correlations were also made with photoperiod (see Section 2.1) and a weaker secondary spawning episode was detected in the austral spring. Recent in situ observations of Asterias rubens (¼vulgaris) in the Gulf of St. Lawrence (eastern Canada) have shown that spawning events coincide with seawater temperature increases resulting from the downwelling of warm surface water (Himmelman et al., 2008). According to a long-term laboratory monitoring study of the deep-sea asteroid Henricia lisa from ca. 600 m that spanned three breeding seasons, the onset of spawning consistently took place at 3–4 C (when ambient seawater temperature was either increasing or decreasing), leading to biannual reproduction (Mercier and Hamel, 2008). However, gonadal sections from populations at ca. 1300 m did not show evidence of the biannual pattern, possibly due to more uniform temperature conditions at this depth. 2.3.5. Echinoidea Stott (1931) observed that the European echinoid Echinus esculentus spawned when the temperature was rising from 7 to 9 C, but sea urchins from Greenland to Portugal spawned almost simultaneously or at least synchronously enough that the temperature range at the time of spawning was rather broad. Paracentrotus lividus undergoes one or two spawning episodes annually. According to Lopez et al. (1998) the timing of reproduction should be influenced by temperature in populations along the coast of Spain, as suggested by the correlation between the onset of the main recruitment peak and the increase in temperature during spring. A temperature between 13 and 16 C was proposed to be the proximate trigger by Boudouresque and Verlaque (2007), since spawning commenced as the temperature either rose or fell to a critical level (Byrne, 1990; Fenaux, 1968; Pedrotti, 1993). Alternately, the initial spawning event may be triggered by day length (ca. 15 h of daylight), and the end of the spawning period would be set by
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temperature (Spirlet et al., 1998). Spawning began in May in both years studied, at a temperature >13 C, and proceeded until temperature reached a maximum of ca. 18 C in August. Important differences, or the occurrence of one or two annual peaks, can be observed within a given region, as well as between localities and habitats. For instance, Byrne (1990) recorded inter-annual variations in spawning of P. lividus in Ireland, with the onset of gamete release differing by as much as 4 weeks between years. One hypothesis is that the zoogeographic differences in spawning may reflect the existence of different ‘‘physiological races’’ of P. lividus that spawn at different temperatures at the different latitudes (Byrne, 1990). The spawning season of Strongylocentrotus nudus (September and October) corresponded to a drop in seawater temperature from 25 to 20 C in Wakasa Bay, Japan (Tsuji et al., 1989), and from 20 to 15 C in Tohoku and Hokkaido (Agatsuma et al., 1988; Odagiri et al., 1984; Sugimoto et al., 1982). The reproductive period of Hemicentrotus pulcherrimus in Japan appears to vary among locations, depending on the temperature regime. In eastern Fukui, spawning took place from December to April, at a time when the temperature fell from 13 to 10 C and rose again to 13 C, maximum gamete release occurring in January–March when seawater temperature was ca. 10 C (Kawana, 1938). In northern Kyushu, sea urchins spawned from December to May as seawater temperature fell to <15 C and rose again to 20 C, a peak again being observed in January–March (Shimazaki et al., 1987). Off the south-western coast of Japan, the gonad index increased from August to a maximum in December–January as the gonads went from recovery to maturity and gamete release occurred from late January to late February, when the seawater temperature dropped from 13 to 10 C (Isemura, 1991). Off the Pacific coast, spawning took place from January to March (Kobayashi and Konaka, 1971), whereas in southern coastal waters of the Sea of Japan (Hokkaido), the onset of gonad maturation was in November and spawning occurred from March to June when the seawater temperature rose from 6 to 13 C. The delay in spawning was attributed to low seawater temperature in winter (Agatsuma, 1992, 2007; Agatsuma and Nakata, 2004) as reported for Strongylocentrotus purpuratus (Cochran and Engelmann, 1975). The sea urchin Anthocidaris crassispina spawned in July and August off the coast of Kyoto and Nagasaki in the south-western Sea of Japan and along the Pacific coast of Chiba in central Japan (Masuda and Dan, 1977; Tsuji et al., 1989; Yamazaki and Kiyomoto, 1993). In Wasaka Bay, Kyoto, the gonad index increased after December and reached a maximum in June–July before decreasing abruptly in July or August, when the seawater temperature rose from 23 to 29 C (Tsuji et al., 1989). In New Zealand, the reproductive potential of Evechinus chloroticus and the timing of spawning varied between years at the sites studied, possibly as a
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result of inter-annual variability in physical and biological conditions (Brewin et al., 2000). The major spawning event apparently coincided with the period of highest sea surface temperature. Variability was noted in the duration of spawning, which ranged from 1 to 4 months. The investigators suggested that a large synchronous spawning would indicate strong or rapid changes in the cue factor, whereas a partial spawning might represent a weaker or slower change in the cue (Brewin et al., 2000). In the Bay of Brest (France), Sphaerechinus granularis exhibited a brief spawning period between May and June (Guillou and Lumingas, 1998), in contrast to the 2- to 3-month-long breeding period of S. granularis in the Gle´nan Archipelago, South Brittany (Guillou and Michel, 1993). While the spawning period at the latter site generally ended in June, the date of onset varied according to seawater temperature during the period of gonadal growth. The average onset was estimated to be 5 April according to mean temperature conditions calculated on a 35-year basis (Guillou and Lumingas, 1998). A relationship between the deviation in the spawning period from the theoretical date and the sum of monthly temperature anomalies during the normal period of gonadal activity (Guillou and Michel, 1993) showed that the temperature deficit in the Bay of Brest in 1992 and 1993, together with the mean temperatures of the Bay of Concarneau, should have resulted in 1 month of delay in the onset of spawning, which was consistent with the observations and supported the influence of temperature on spawning (Guillou and Lumingas, 1998). Seward (2002) found a significant relationship between temperature and spawning in the sea urchin Strongylocentrotus droebachiensis along the coast of Maine (USA) in both areas she studied. However, the strength of the relationship between temperature and gonad indices varied between sexes, between sites, and between regions. Spawning occurred when the temperature increased from 3 to 6 C in both the Georges Islands and Jonesport (Seward, 2002) a range that is consistent with breeding periods reported in some populations of green sea urchins (Cocanour and Allen, 1967; Miller and Mann, 1973; Stephens, 1972), but not with others (Himmelman, 1976; Oganesyan, 1998; Taylor et al., 1957). If temperature were a proximate spawning cue, spawning should have started earlier in central Maine than eastern Maine, which was not observed in 2000 (Seward, 2002). The hypothesis that temperature is the proximate cue for spawning in green sea urchins has been challenged (Himmelman, 1978; Starr et al., 1990, 1993), and it is possible that high temperatures lethal to developing larvae can inhibit spawning (Pearse, 1981). Stephens (1972) showed that S. droebachiensis larvae developed normally at 0–4 C and asynchronously and abnormally at 10 C, while at 12 C cell division was arrested and mortality occurred. Nevertheless, linear regression models demonstrated coupling between spawning times and increases in temperature (Seward, 2002). Himmelman et al. (2008) recently observed large numbers of S. droebachiensis
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spawning in the Mingan Archipelago (eastern Canada) and suggested that the increase in seawater temperature from downwelling of warm surface water was the factor responsible. Nunes and Jangoux (2004) examined the role of temperature in inducing spawning of Echinocardium cordatum in Northern France. Yakovlev (1987) and Nakamura (2001) had previously argued that the spawning cue in E. cordatum was either an increase or a decrease of temperature to around 15 C. In contrast, Nunes and Jangoux (2004) indicated that the prevailing temperature during spawning (April–May) varied between 10 and 13 C, and that seawater temperature was 14–16 C when the breeding season came to an end. They proposed that temperature was a threshold cue (maximum value) ending the breeding season, higher temperatures inhibiting spawning. Yonge (1940) believed that the spawning periods of many of the marine invertebrate species of the Great Barrier Reef (Australia) and other tropical reefs were influenced by temperature fluctuations. He divided the breeding periods into four groups based on inferred temperature requirements: (1) those spawning during a brief summer period when temperatures reach ca. 30 C, (2) those with a slightly extended breeding period at temperature above ca. 24 C, (3) those spawning in spring and autumn at temperatures between ca. 25 and 27 C, and (4) those spawning year round, at temperatures above ca. 20 C. Diadema setosum appears to belong roughly to the third category, since seawater temperatures were above 25 C at every locality where it was reproducing (Pearse, 1968a). Winter sea surface temperatures generally fall below 25 C at latitudes above 10–20 in the Western Pacific (Muromtsev, 1963) and D. setosum probably does not spawn in winter at or above these latitude. At the Low Isles (Australia), the temperature during the spawning period of D. setosum ranged from 25 to 33 C. All the temperatures taken by Fox (1924b) at Suez (Egypt) for July, August and September, when reproductive activity occurred, were above 26 C. Similarly, the spawning peak for D. savignyi on the Kenyan coast coincided with the highest seawater temperatures (28–32 C) during the north-east monsoon period (Muthiga, 2003). A lower critical temperature around 18–20 C, corresponding roughly to Yonge’s (1940) fourth category, may apply in the reproduction of Echinometra mathaei (Pearse, 1968a). Individuals were ripe at these temperatures at both Rottnest Island (Western Australia) and Hilo (Hawaii, USA), which was year round, at least at the former locality. A few mature animals were found at Al-Ghardaqa (north-western Red Sea) in mid-winter, when the daily temperature fluctuated from 10.5 to 21.2 C (Pearse, 1968a). Mature animals did not occur near Suez (Egypt) between late November and April, however, when the temperature fluctuated from 18.5 to 21.7 C, averaging ca. 19 C. On the west central coast of Honshu Island ( Japan),
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E. mathaei probably does not spawn in winter when the sea temperatures are about 15 C (Pearse, 1968a).
2.4. Phytoplankton, phytodetritus and other food sources Conditions favourable for the development and survival of offspring such as the presence of planktonic food are often proposed to be the ultimate mediator of reproductive cycles. Seasonal peaks in phytoplankton abundance are especially pronounced in temperate and high latitudes, with major blooms generally occurring in the spring, and occasional secondary blooms developing in late summer or fall. Synchronization of the planktonic larval phase with maxima in phytoplankton abundance can be achieved by cuing gamete release on environmental factors (i.e., temperature, photoperiod) or on the algal bloom itself (Himmelman, 1999). However, examples of seasonal spawning by Antarctic species without planktonic larvae suggest that spawning coinciding with algal blooms can be induced by factors other than the presence of suitable food for planktotrophic larvae (Pearse et al., 1991). We have observed several species of echinoderms with lecithotrophic development (e.g., Solaster endeca, Crossaster papposus) spawning simultaneously with planktotrophic species in the spring around Newfoundland in eastern Canada (Hamel and Mercier, unpublished data), suggesting that further research is required into the possible function of phytoplankton as a spawning cue. 2.4.1. Crinoidea Fell (1966) speculated that in areas where plankton levels are variable, spawning in crinoids tends to be synchronized with the period of highest plankton abundance, even though crinoid larvae are lecithotrophic. 2.4.2. Ophiuroidea The spawning of planktotrophic ophiuroid species may be expected to follow primary productivity especially when the latter exhibits a predictable cycle (reviewed by Hendler, 1991). Examples of such correlations are common, for instance, different populations of both Ophiura albida and O. ophiura were reported to spawn following the period of maximum phytoplankton density in Norway (Skjaeveland, 1973), and spawning of Ophiothrix spiculata and Amphiodia occidentalis from southern Monterey Bay (USA) was suggested to occur with the onset of the late spring phytoplankton bloom (Rumrill, 1984). However, the presence of ophioplutei throughout the year (Rees, 1954 in Hendler, 1991) suggests that larvae of brittle stars are not necessarily limited by food availability. Furthermore, Ophiocoma species in Panama spawn at times other than the phytoplankton bloom, and species with either planktotrophic or lecithotrophic larvae may spawn during the same period (Hendler, 1979).
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In deep waters, which are ostensibly characterized by negligible seasonal variability, some species nevertheless display an annual cycle in reproduction. Cyclic variations in the downward flux of particles derived from surface primary and secondary production may influence the timing of reproduction in deep-water ophiuroids (Hendler, 1991). A number of studies support this hypothesis (e.g., Gage and Tyler, 1982; Hendler, 1991; Schoener, 1968), suggesting that gametogenesis and, ultimately, spawning could be timed to coincide with maximal food availability (Tyler and Gage, 1980b). For instance, Schoener (1968) suggested that the availability of food may control the reproductive periodicity of Ophiura ljungmani and Ophiomusium lymani. The limited data provided by Litvinova and Sokolova (1971) implied brief summer spawning periods in two abyssal Amphiophiura species of the Indian and Pacific Oceans. Finally, vitellogenesis in O. ljungmani coincides with pulses of sinking materials produced near the surface in the late summer (Tyler, 1980). 2.4.3. Holothuroidea Increased primary production has been identified as a possible spawning cue for a number of temperate species. Most sea cucumbers from high latitudes breed in the spring or summer, when plankton is abundant and can presumably provide food to sustain their larvae and/or juveniles (Smiley et al., 1991). Very few species, such as Cucumaria pseudocurata, a brooder from the west coast of North America, reproduce in early winter, when planktonic food is potentially scarce (Rutherford, 1973). Even if spawning is likely not cued on primary production, the larval food timing hypothesis may still hold, since this species requires several months for the tentacles to grow and the young are ready to feed only when plankton becomes more abundant in the spring (Rutherford, 1973). The distinctive breeding seasons of Cucumaria frondosa, which occur in July in the Arctic (Runnstro¨m and Runnstro¨m, 1919), in mid-June in eastern Quebec, Canada (Hamel and Mercier, 1995a), in February–May in Newfoundland, Canada (Coady, 1973), and in April–May along the coast of New England, USA ( Jordan, 1972) suggest that phytoplankton blooms, which occur earlier in lower latitudes than in higher ones, play an important role in the initiation of spawning. Mass spawning of C. frondosa in the field (eastern Canada) is indeed correlated with a period of phytoplankton abundance, although a more detailed study of environmental factors during gamete release revealed no direct correlation with levels of chlorophyll a that could identify it as a proximate spawning cue (Hamel and Mercier, 1995a). Details on the other factors monitored during this field study are provided in other sections of the text (see Sections 2.1–2.3). Phytoplankton is also believed to initiate spawning in other lecithotrophic species from the northern hemisphere such as Cucumaria miniata,
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C. piperata, C. fallax (McEuen, 1988), and Psolus fabricii (Hamel et al., 1993). In both 1988 and 1989, spawning in P. fabricii coincided with the predicted onset of the phytoplankton bloom (Hamel et al., 1993), whereas gamete release in C. miniata has been observed during well-developed phytoplankton blooms by Sewell and Levitan (1992) and by McEuen (1988). Spontaneous spawning of the planktotroph Parastichopus (¼Stichopus) californicus was observed by Levitan (2002b)in situ off Vancouver Island (western Canada) during a spring phytoplankton bloom (March). Similarly, Cameron and Fankboner (1986) indicated that localized periodic blooms could explain the pattern of spawning observed in P. californicus. Another example is the report by Tan and Zulfigar (2001) who observed that the spawning period of Stichopus chloronotus in the Straits of Malacca (Malaysia) coincided with high chlorophyll a levels in both 1996 and 1997. Correlative studies may sometimes be misleading because primary production is usually tied to a number of other factors such as temperature, photoperiod and freshwater runoff, which are not easy to discriminate. Induction of spawning by the addition of algae has often been attempted. Battaglene et al. (2002) were able to trigger spawning in roughly 10% of mature females Holothuria fuscogilva by adding a suspension of dried algae Schizochytrium sp. (AlgamacÒ ). A similar technique was also used on H. fuscogilva, with up to 36% spawning success in some months, supporting the contention that phytoplankton exudates may influence spawning (Ramofafia et al., 2000). In the deep-sea environment, pulses of falling detritus have frequently been suggested to be zeitgebers that can entrain seasonal cycles of gametogenesis and spawning, though the evidence is still ambiguous. Studies have suggested that there may be a seasonal input of phytodetritus into the deep sea following the spring phytoplankton bloom (Deuser and Ross, 1980; Deuser et al., 1981), leading to the hypothesis that sinking organic matter provides a food source for gamete development in the adult echinoderms undergoing seasonal reproduction as well as for larvae in the water column (Tyler and Gage, 1980a; Tyler et al., 1982b). (See Section 2.3 in Chapter 2 for details on the coupling between pulses of organic matter and the reproductive cycle). No evidence of phytodetritus acting as a spawning cue for deep-sea holothuroids has been published. 2.4.4. Asteroidea There is little evidence that seasonal food supplies can directly control spawning in asteroids. The possible influence of phytodetritus on gametogenic cycles has been discussed earlier (Section 2.3 in Chapter 2). Decreasing photoperiod and an increasing food supply for larvae have been proposed to trigger spawning in Cosmasterias lurida in Golfo Nuevo, Northern Patagonia, Argentina (Pastor-de-Ward et al., 2007). Tyler et al. (1990) observed that the downward flux of phytodetritus coincided with the feeding period
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of the larvae of Dytaster grandis from the Porcupine Abyssal Plain (NE Atlantic), although the spawning cue in this species remains unknown. 2.4.5. Echinoidea The most convincing evidence for the role of phytoplankton in the spawning of echinoids comes from studies of the cold-temperate species Strongylocentrotus droebachiensis and its congenerics. Himmelman (1975, 1976, 1981) initially reported that free-spawning marine invertebrates from eastern Canada, including S. droebachiensis, spawned at the onset of the spring phytoplankton bloom and that the presence of dense concentrations of suspended phytoplankton was the most probable proximal stimulus for gamete release. Since then, correlations between spawning in S. droebachiensis and the spring peak in algal abundance have been reported by several authors (Gaudette et al., 2006; Starr et al., 1993; Vadas and Beal, 1999). Starr et al. (1990) demonstrated experimentally that chlorophyll a can induce gamete release, and subsequent experiments revealed that exudates of various species of phytoplankton can trigger spawning in sea urchins (Starr et al., 1992). Concentrations of 5 107–10 107 cells l1 of the diatoms Skeletonema costatum and Phaeodactylum tricornutum induced ca. 50% of the individuals to spawn, and similar levels of Dunaliella tertiolecta and Thalassiosira nordenskioldii triggered some 31–33% of them to spawn. The response was linked to phytoplankton concentration. Starr et al. (1992) characterized the properties of the substance that induced spawning in S. droebachiensis. The partially purified active fraction contained yellowish pigments that absorbed ultraviolet light and reacted with ferric chloride and potassium ferricyanide, suggesting that they were phenolic compounds. The observed absorption peak around 260 nm is typical of yellow substances exuded by a variety of algae. Starr et al. (1992) stated that the presence of a spawning inducer in Fucus vesiculosus indicated that macro-algae may also contribute to natural spawning in S. droebachiensis. Furthermore, Starr et al. (1993) noted spawning events around 12–29 June in 1983 and 7–13 June in 1984 when chlorophyll a concentrations increased from low values to significant levels of 1.3–2 mg m3 for a period >3 days (Fig. 3.3). Although it is now apparent that Strongylocentrotus droebachiensis responds to phytoplankton by releasing gametes under laboratory conditions, the relationship established from field observations is not always as clear according to compilations by Starr et al. (1993) and Seward (2002) (Table 3.2). For example, Munk (1992) found that the onset of spawning in S. droebachiensis from Kodiak (Alaska, USA) coincided with the spring phytoplankton bloom (late March–April) in two of the 3 years investigated. In the third year, however, spawning started 6–8 weeks after the bloom. Likewise, a study by Seward (2002) demonstrated that most populations of S. droebachiensis in Maine (eastern USA) spawned when chlorophyll a concentrations were low (ca. 2 mg m3), only one group spawning at concentrations
Tidal amplitude (m)
5 4 3 2 1
Temperature (⬚C)
12
Urchin spawning
Urchin spawning
8 4
Seasonal trend
Minimum point of the seasonal trend
30 20 Daily mean
Chlorophyll a (mg • m−3)
8 6 4 2 0
Gonadal Index (%)
10
20 16 12 8 4
Daily mean
Minimum point of the seasonal trend
Strongylocentrotus droebachiensis
Gonadal index Gonadal index Mature oocytes
April
May
Mature oocytes
June 1983
July
April
May
June
July
100 80 60 40 20 0
Mature oocytes (%)
Salinity (ppt)
Seasonal trend
Daily mean
Daily mean
0
1984
Figure 3.3 Strongylocentrotus droebachiensis (Echinoidea). Temporal variations in the mean gonad index and the percentage of mature oocytes (n ¼ 30) in relation to tidal amplitude, daily mean temperature and salinity, and chlorophyll a concentration in the St. Lawrence Estuary (eastern Canada), during the spring and summer of 1983 and 1984. Vertical lines represent 95% confidence intervals. Reprinted with permission from Starr et al. (1993).
Table 3.2 Spawning periods of the green sea urchin Strongylocentrotus droebachiensis with respect to temperature and phytoplankton blooms. Adapted from Seward (2002) and Starr et al. (1993) Location
Spawning period
Seawater temperature
Phytoplankton bloom
Pointe-au-Pe`re (QC, Canada) St. Lawrence Estuary (QC, Canada) Gulf of St. Lawrence (eastern Canada) Gulf of St. Lawrence (eastern Canada) Portugal Cove (NL, Canada) St. Margaret’s Bay (NS, Canada)
June (Starr et al., 1993)
4–10 C (Starr et al., 1993)
June (Starr et al., 1993)
4–10 C (Starr et al., 1993)
Ends in May (Starr et al., 1993) Early July
<4 C (Bugden et al., 1982) ca. 6 C (Himmelman et al., 2008) <3 C (Himmelman, 1969) 2–4 C (Miller and Mann, 1973)
Starts in June, maximum in July (Starr et al., 1993) Starts in June, maximum in July (Starr et al., 1993) Late April to early May (Steven, 1974) Likely similar to above
Mahone Bay (NS, Canada) Lamoine (ME, USA) Salisbury Cove (ME, USA) Boothbay Harbor (ME, USA) Georges Islands (ME, USA)
March–April (Himmelman, 1978) March–April (Meidel and Scheibling, 1998; Miller and Mann, 1973) March–April (Meidel and Scheibling, 1998) April (Cocanour and Allen, 1967) April to mid-May (Harvey, 1956) Early April (Stephens, 1972) Mid–late April (Seward, 2002)
April (Himmelman, 1978) April (Platt and Irwin, 1970)
–
–
–
Starts in April, sometimes in May (Bigelow et al., 1940) Starts in April, sometimes in May (Bigelow et al., 1940) Starts mid- to late March (Bigelow et al., 1940) Starts mid-April or May (Seward, 2002)
– 8 C (Taylor et al., 1957) 4–8 C (Seward, 2002)
(continued)
Table 3.2
(continued)
Location
Spawning period
Seawater temperature
Phytoplankton bloom
Jonesport (ME, USA)
Mid–late April (Seward, 2002) Late April (Stephens, 1972)
4–6 C (Seward, 2002)
Starts late April or May (Seward, 2002) Starts in late March to third week of April (Bigelow et al., 1940) Mid-winter bloom (Fish, 1925) April (Himmelman, 1976)
Cape Cod (MA, USA) Woods Hole (MA, USA) First Narrows (BC, Canada) Botanical Beach (BC, Canada) Bergen (Norway)
March (Boolootian, 1966) April (Himmelman, 1976) April (Himmelman, 1976) Late March (Runnstro¨m, 1927)
– 1–2 C (Taylor et al., 1957) 6–8 C (Himmelman, 1976) 8–9 C (Himmelman, 1976) 4–5 C (Brown, 1984)
Troms (Norway)
February–March (Vasseur, 1952)
2 C (Brown, 1984)
Troms -sundet (Norway)
March (Falk-Petersen and Lonning, 1983)
–
White Sea
Mid-June to mid-July (Kaufmann, 1974)
3–5 C (Kaufmann, 1974)
Barents Sea
February–April (Oganesyan, 1998)
0–2 C (Oganesyan 1998)
Mid-April (Himmelman, 1976) Starts in mid-March, max. in March–April (Sakshaug and Mykiestad, 1973) Starts in mid-March, max. in March–April (Sakshaug and Mykiestad, 1973) Starts in mid-March, max. in March–April (Sakshaug and Mykiestad, 1973) Starts in mid-March, max. in March–April (Sakshaug and Mykiestad, 1973) Starts in March, max. in April (Propp, 1971; Kuznetsov, 1991; both from Seward, 2002)
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typical of a bloom in that location (ca. 8 mg m3). The author suggested that the conflicting evidence from laboratory experiments and field studies questioned the role of phytoplankton as the single proximate cue for spawning. Nevertheless, spontaneous spawning of S. droebachiensis, S. purpuratus and S. franciscanus was observed by Levitan (2002b) in the field off Vancouver Island (western Canada) during spring phytoplankton blooms (March–April). The timing and length of the spawning season in the red sea urchin Strongylocentrotus franciscanus appear to be explained by patterns of food availability (Bernard, 1977). This author noted that emission of gametes occurred in mid-July in groups of S. franciscanus held in unconnected tanks (Vancouver Island, Canada). However, spawning in the field frequently involved aggregations of urchins some tens of meters across, and adjacent individuals did not shed gametes, although the gonads were equally ripe (Bernard, 1977), again suggesting that the presence of phytoplankton cannot be the sole and universal spawning stimulus. Guettaf et al. (2000) noted that Paracentrotus lividus spawned throughout the year at all the sites they studied along the coast of Algeria, but for any given site a spawning event appeared to be closely linked to food availability (algae in particular) and indirectly to the prevailing hydrodynamic conditions. Diadema savignyi on the Kenyan coast (Muthiga, 2003) and Echinometra vanbrunti in the Caribbean (Lessios, 1981) spawn just before the monsoonal peak in phytoplankton production. Muthiga and Jaccarini (2005) concluded that a combination of factors related to monsoonal seasonality, including light intensity and phytoplankton, regulate the reproduction of Echinometra mathaei on the East African coast. As for holothuroids and asteroids, the influence of detritic food pulses on the reproduction of deep-sea echinoids has been proposed and discussed. However, it refers more directly to the cycle of gamete synthesis (Section 2.3 in Chapter 2) than to gamete release per se.
2.5. Lunar cycle It has long been known that some aspects of the cyclical behaviour of marine organisms, including gametogenesis, spawning, mating, and the release of larvae or juveniles, are correlated with the phases of the moon (Naylor, 1999; Omori, 1995). Beyond the fact that lunar phases provide a means of synchronization, the underlying principles of lunar reproductive cycles are still unclear (Naylor, 1999). The possibility that moonlight itself acts as a mediator of reproductive synchrony was initially questioned (Korringa, 1947; Pearse, 1972), prompting experimental studies to determine whether lunar control was indirectly mediated by the tides. A number of semi-lunar and lunar rhythms have indeed been shown to follow neap/
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spring cycles of tides, and thus provide evidence of indirect control (Naylor, 1999). However, there are also examples of the direct influence of moonlight (Mercier et al., 2007). Moreover, both free-running and directly cued lunar or semi-lunar cycles have been observed, further complicating the interpretation of such periodicities. Evidence of spawning occurring a few days before or after specific lunar phases has been obtained for several echinoderms (e.g., Babcock et al., 1992; Coppard and Campbell, 2005; Fox, 1924a; Iliffe and Pearse, 1982; Kennedy and Pearse, 1975; Kobayashi, 1994; Kubota, 1981; Lessios, 1981; Mercier et al., 2000a, 2007; Muthiga, 2003; Pearse, 1975, 1990). However, there are few accounts of a predictable, synchronous and widespread spawning pattern related to lunar phases. The crinoid Oxycomanthus japonicus releases gametes during specific lunar phases of every year (Kubota, 1981), and a similar pattern has recently been described in two apodid sea cucumbers (Kubota, 2000; Kubota and Tomari, 1998). Despite the prevalence of lunar rhythms, their ultimate and even proximate causes remain difficult to identify, because studies are either too short or focus mainly on indirect evidence of reproductive processes (e.g., histology, gonad index). Many diadematid sea urchins display monthly lunar periodicities in breeding, but the evidence has generally been obtained from gonad indices and/or histological analysis (Coppard and Campbell, 2005; Iliffe and Pearse, 1982; Kobayashi, 1969, 1992; Muthiga, 2003, 2005), from the presence of gametes in dissected animals (Fox, 1924b) or through KCl-induced spawning (Lessios, 1981; Levitan, 1988). Studies of induced spawning in the field have produced slightly different results than gametogenic studies; for example, Levitan (1988) observed that gamete shedding in Diadema antillarium can be triggered on almost any day of the month, although it is slightly more common around the new moon. Such data emphasize that lunar periodicity in gametogenesis may not necessarily equate to lunar periodicity in gamete release. Direct evidence of monthly spawning (i.e., based on records of gamete release) associated with lunar phases is rare. Repeated in situ observations on the Great Barrier Reef have provided convincing support for a few species of tropical sea cucumbers, including Bohadschia argus, Euapta godeffroyi, Stichopus chloronotus and Stichopus variegatus (Babcock et al., 1992). Continuous monitoring of Holothuria scabra in large outdoor tanks over 4 months (Mercier et al., 2000a) and of Isostichopus fuscus over 4 years (Mercier et al., 2007) have also helped define and characterize lunar rhythms. 2.5.1. Crinoidea Oxycomanthus japonicus spawns according to the lunar cycle, although it remains to be determined whether moonlight acts directly or through the entrainment of an endogenous clock (Dan and Dan, 1941). A relationship between spawning and the tidal phase was also observed, although
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individuals removed from such influence continued to spawn in synchrony with the lunar phase (Dan and Dan, 1941). Over the years, the annual spawning of O. japonicus has consistently been observed to occur between late September and mid-October, during the first or last quarter of the moon (Holland et al., 1975; Kubota, 1981). Holland (1981a) suggested that the linkage between the perception of full moonlight and spawning at the quarter moon in O. japonicus probably required: (1) an endogenous semilunar rhythm, whereby the full moon would elicit a response in the endocrine system of the crinoid (a mechanism that would still function should the moonlight be diffused or blocked by clouds); (2) a 1-week period of gonadal differentiation acting as an internal timer, which would result in spawning in the last quarter if triggered at full moon, and in spawning in the first quarter if triggered at new moon. Holland (1981a) also mentioned that the spawning observed around 15:00 h by Kubota (1981) could have been determined by an endogenous circadian rhythm of gonad differentiation entrained by the day–night cycle, which would imply that the exact hour of spawning is determined by the interaction of two endogenous rhythms, one biweekly and the other circadian. However, no subsequent research has been conducted to test the proposed hypotheses. Furthermore, the first of Holland’s (1981a) assumptions, that cloud cover would prevent the direct perception of the moonlight cue, is rather tenuous. Experiments conducted on Oxycomanthus japonicus on the predicted day of spawning revealed that germinal vesicle breakdown and ovulation occurred at ca. 12:00 h and that oocytes were consistently shed ca. 4 h later (Holland and Dan, 1975). The fact that arms severed at 14:00 h released gametes synchronously with the rest of the spawning females led the authors to suggests that once the cue is perceived, the chain reaction occurs within the gonads rather than through a centralised system (Dan and Kubota, 1960). Furthermore, Kubota (1981) noted that oocytes removed from the gonads at 10:00 h still ovulated and matured between 12:00 and 14:00 h. A correlation between gonad ripeness and spawning at the full moon in captivity has been noted in another species, Heteromorpha savignyi from the Red Sea (Mortensen, 1938). 2.5.2. Ophiuroidea Assessments of lunar periodicities in brittle stars are few and lack rigour; both positive and negative correlations are therefore largely speculative (Hendler, 1991). Large numbers of brittle stars Ophioderma rubicundum from the Gulf of Mexico (USA) spawned on the seventh and eighth evenings following the full moon in August 2000 (Hagman and Vize, 2003). Many individuals of another species, O. squamosissimum, also released gametes early in the evening on the eighth day after the full moon (Hagman and Vize, 2003).
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2.5.3. Holothuroidea The possible influence of lunar cycles on holothuroid reproduction has received little attention, although there are some credible recent studies, and in situ observations of spawning often refer to lunar phases (Table 3.1). Babcock et al. (1992) observed that holothuroid species from the Great Barrier Reef (Australia) such as Bohadschia argus, Euapta godeffroyi, Stichopus chloronotus and Stichopus variegatus spawned during a 1- to 3-day period during certain lunar phases. However, in most cases the occurrence of spawning was limited to a portion of the population. A clear picture was obtained of the reproduction and recruitment of Holothuria scabra in the Solomon Islands after combining data from laboratory experiments and field observations (Hamel et al., 2001; Mercier et al., 2000a,b). First, the adults had an increasing tendency to aggregate just before the full moon (Fig. 2.5). Recruitment data and direct observation of individuals in outdoor tanks indicated that spawning occurred during the following days: large numbers of small recruits were found in the middle of the lunar cycle, whereas small numbers of large recruits were observed just before the full moon (Mercier et al., 2000a). Morgan (2000a) reported that spawning induction was most successful around new or full moons in H. scabra in Australia, whereas Battaglene (1999b) found that 33% of H. scabra spawned 2 days after the new moon in outdoor tanks in the Solomon Islands. Finally, Conand (1993b) noted that H. scabra versicolor spawned 2 days after the first moon quarter in February 1980 in New Caledonia. In the apodids Patinapta ooplax and Polycheira rufescens, spawning was associated with the lunar cycle, beginning around the second half of July and lasting until the end of the breeding season (Kubota, 2000; Kubota and Tomari, 1998). Spawning events presumably occurred 1 or 2 days after every full and new moon in P. ooplax and 1 or 2 days before it in P. rufescens (Kubota, 2000; Kubota and Tomari, 1998). The former species spawned three times at semi-lunar intervals, the latter about five times (Kubota, 2000). These predictable spawnings involved most or many of the ripe individuals in the population studied, and each individual released all the gametes at one time (Kubota, 2000). A recent study in which several hundred newly collected Isostichopus fuscus were monitored nearly every month for 4 years in Ecuador revealed a lunar spawning periodicity, 0.7–34.9% of the individuals consistently spawning 1–4 days after the new moon (Mercier et al., 2007) (Fig. 3.4). Spawning was usually completed within one evening, although some gamete release was often recorded over 2–4 consecutive evenings. Individuals maintained in captivity for several months retained their spawning periodicity and timing with the lunar cycle whereas newly caught individuals that were shaded from the moonlight did not spawn, thus demonstrating the apparent lack of free-running endogenous rhythm and the prevalence of
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Figure 3.4 Isostichopus fuscus (Holothuroidea). Proportion of spawning males and females related to the lunar cycle between January and December 2002. Note the variable scale of the y-axis. Reprinted with permission from Mercier et al. (2007).
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lunar luminance over other cues (i.e., tidal cycle, barometric pressure) (Mercier et al., 2007). The gonads of individuals that did not spawn in any given month were at various levels of development, including post-spawning, growth and mature gametogenic stages, implying that the individual reproductive cycle is longer than the monthly spawning periodicity observed at the population level, enabling I. fuscus populations to reproduce year round (Mercier et al., 2004, 2007). Desurmont (2008) recently reported in situ observations in spawning Stichopus herrmanni in New Caledonia, three individuals aggregating and spawning over 3 days centered on the new moon of January 2008. 2.5.4. Asteroidea There are few examples of lunar periodicity in asteroid reproduction. According to Janssen (1991) who studied Archaster typicus in the Philippines, the well-known copulation behaviour of the genus Archaster was described for the first time by Boschma (1924) and studied several times thereafter ( Janssen and Holm, 1988; Janssen et al., 1984; Komatsu, 1983). Mating apparently does not occur continuously throughout the year, but may be restricted to periods of several days repeated at regular intervals. These limited observations are not unequivocal, but they do suggest that mating coincides with the new moon ( Janssen, 1991). Yamaguchi and Lucas (1984) also observed that spawning in Ophidiaster granifer from Guam coincided with the full moon. In situ observation of Acanthaster planci spawning on Davies Reef (Australia) revealed the occurrence of a mass spawning event during the three-quarter moon simultaneously with numerous other species of corals and echinoderms (Babcock and Mundy, 1992; Babcock et al., 1992). 2.5.5. Echinoidea Echinoids are by far the most studied echinoderms with respect to lunar rhythms in spawning activity. Semi-lunar spawning cycles have been reported at Seto ( Japan) for several species: Mespilia globulus (Kobayashi, 1967), Diadema setosum (Kobayashi and Nakamura, 1967), Anthocidaris crassispina, Echinometra mathaei, Echinostrephus aciculatus, Tripneustes gratilla (Kobayashi, 1969) and Hemicentrotus pulcherrimus (Kobayashi, 1992). Some echinoid species are known to exhibit lunar rhythms in some areas, but only poorly defined rhythms in other locations. This is particularly well illustrated in the genus Diadema (Pearse, 1990). The picture is complicated by reports that different populations of the same species spawn at different phases of the moon. Fox (1924a,b) suggested that spawning took place on each full moon during the breeding season of the sea urchin Diadema setosum in the Red Sea. He based this conclusion on the occurrence of ripe specimens at Suez mainly between the new moon and the first lunar quarter in 1920, and
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between the first lunar quarter and the full moon in 1921; in both years most animals were mature around the 20th of each month. Furthermore, he noted that a single individual could spawn repetitively during consecutive lunar periods. A few years later, Mortensen (1937) was unable to confirm Fox’s observations after noting that ripe specimens could be obtained irrespective of the full moon near Suez (Egypt). Mortensen (1938) reported that data for other populations in this region did not support lunar periodicity and considered that the periodicity of D. setosum in Egypt was an exception. At Misaki ( Japan), Yoshida (1952) determined from a histological study of the reproduction of D. setosum that individuals in a single population were ready to spawn near the full moon from July to September; however, the methodology used was later questioned (Pearse, 1970). With a limited number of samples (i.e., for 6 days around one full moon and two new moons), Kobayashi and Nakamura (1967) suggested that the populations of D. setosum at Seto ( Japan) spawned a few days before the full moon and perhaps on the day of one of the new moons. Later studies by Pearse (1968a, 1970) showed that reproduction of D. setosum in the Gulf of Suez and the northern Red Sea was not related to the lunar cycle, thus supporting Mortensen’s conclusion. Specifically, D. setosum in the west-central Pacific (Pearse, 1968a) and the northern Red Sea (Pearse, 1970) showed surprisingly close reproductive synchrony among individuals, suggesting welldefined reproductive rhythms. Conversely, populations from different localities exhibited different reproductive stages with respect to each other and to phases of the moon (Pearse, 1970). A similar absence of a lunar rhythm was reported by Hori et al. (1987) from a population in Singapore. Nevertheless, Tuason and Gomez (1979) reported that D. setosum exhibited monthly maturation peaks around the full moon in the Philippines, Muthiga (2003) noted a lunar periodicity during the breeding season in Kenya, and Kobayashi (1994) mentioned that this species apparently displays a semi-lunar rhythm in the Gulf of Thailand and the Andaman Sea, with peak spawning around full and new moons. The evidence is compelling at some sites and rather inconclusive at others, suggesting that the reproductive rhythm of D. setosum may not be directly regulated by the lunar cycle throughout its distribution range. A lunar cycle of gametogenesis is well known in Diadema antillarum (Bauer, 1976; Iliffe and Pearse, 1982), although the presence of a lunar periodicity does not always explain reproductive synchrony. Randall et al. (1964) noted that spawning was most common within the first quarter of the moon, but that it could occur as late as the 19th day of the cycle. These data were confirmed by Iliffe and Pearse (1982), who examined both the gonad index and the size frequency distributions of ova and sperm during the new and full moons. Contrary to Bauer (1976), who suggested from five observations that aggregative behaviour was more pronounced at the new moon, Iliffe and Pearse (1982) determined that there were no significant
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differences between gonad indices at the new and full moons. Nevertheless, they found that oocytes were significantly larger at the new moon and that significantly more animals shed gametes upon dissection at the new moon (Iliffe and Pearse, 1982). Data based on the success rates of KCl-induced spawning showed that while individuals in the US Virgin Islands were more likely to spawn at the new moon than the full moon, spawning activity was not limited to the time of the new moon (Levitan, 1988). Even at a single location, spawning occurred throughout the lunar cycle (Levitan, 1988), supporting the earlier data of Randall et al. (1964). Lessios (1991), using the response to KCl injections as a measure of readiness to spawn, found that D. antillarum, on the Caribbean side of Panama, released gametes more readily just after the new moon, while D. mexicanum, on the Pacific side of Panama, released gametes more readily near the full moon. Similar lunar patterns have also been found for other diadematid species (reviewed in Pearse, 1975). Drummond (1995) showed in Diadema savignyi from eastern South Africa that both December and January new moon samples were dominated by spent gonads, whereas full moon samples contained only growing and premature gonads. The author admitted that there was no conclusive evidence for a lunar spawning rhythm, but argued that the fact that all other members of the genus Diadema show lunar cycles (Pearse, 1975) suggested that D. savignyi on the South African coast probably had such a cycle. Muthiga (2003) found that the reproduction of this species exhibited a lunar periodicity, as spent gonads were observed a few days after the full moon during the breeding season. The study by Coppard and Campbell (2005) reported distinct monthly breeding periodicities associated with the lunar cycle in four species of sea urchins in Fiji. Diadema savignyi and Echinothrix diadema had gametogenic rhythms linked to the full moon, while D. setosum and E. calamaris had a reproductive cycle attuned to the new moon. Reproduction in Centrostephanus coronatus followed the lunar cycle in southern California (Kennedy and Pearse, 1975; Pearse, 1972). For C. rodgersii in New South Wales (Australia), short days and lunar conditions coinciding with the winter solstice appear likely proximate factors which might cue the onset of spawning across its range (Byrne et al., 1998). Evidence of lunar breeding periodicity exists for species other than diadematids. Tennent (1910) indicated that during three summers of laboratory observations, the gonads of Toxopneustes variegatus taken after a night of full moonlight were empty. Moore et al. (1963a) reported that Lytechinus variegatus in Bermuda followed a semi-lunar spawning periodicity but that the pattern was not clear in populations from Florida, although the investigator implied that the sampling sites in Florida were more dispersed, which might have masked the pattern. Spawning every full and new moon has also been deduced from the effectiveness of KCl-induced gamete release in L. variegatus from Panama (Lessios, 1991). At the same location and using
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the same technique, Lessios (1991) found that the spawning of Eucidaris tribuloides was concentrated around the full moon. One of the most convincing pieces of evidence for a semi-monthly reproductive rhythm in a sea urchin comes from Kobayashi (1967) who worked on Mespilia globulus at Seto ( Japan). He found that during the summers from 1958 to 1961 this species spawned near both the new and full moons. The spawning dates each year were different, and corresponded to the calendar shift in the lunar rhythm. Kobayachi (1969) later observed changes in the gonad index of Anthocidaris crassispina during the spawning season in July and August at Shirahama, Wakayama ( Japan), and concluded that the sea urchins spawned at both new and full moon. However, the sea urchins at Minammizu, Shizuaka ( Japan), spawned only at full moon during the spawning season from June to August (Horii, 1997). Kobayashi (1992) proposed that Hemicentrotus pulcherrimus and Pseudocentrotus depressus also spawned in synchrony with the new and full moons. Dotan (1990) indicated that spawning in Heterocentrotus mammillatus from the Northern Red Sea in June and July exhibited a lunar or semi-lunar pattern. Very fragmentary information was provided by Olson et al. (1993), who observed a single male of Phyllacanthus imperialis spawning at Lizard Island (Australia) at night, 4 days after the full moon, together with scleractinian corals. Lamare and Stewart (1998) recorded a 42–56% drop in the gonad index of Evechinus chloroticus from Doubtful Sound (New Zealand) at full moon during spring tides, and concluded that spawning was synchronized at this time but also occurred during an extended period of decreasing sea temperatures. The authors recognised that it was difficult to determine which environmental factors functioned as cues, since the variables were not independent, and suggested that: (1) lunar phases provide proximate cues for spawning, with full gonad maturity reached at full moon; (2) spawning is specifically triggered by changes in seawater temperature; (3) inter-individual cues enhance spawning synchrony. Muthiga (2005) conducted a histological study of the gonads of Tripneustes gratilla along the coast of Kenya, and found many different stages of gametogenesis present throughout the year, suggesting ‘‘continuous’’ reproduction. While a significant correlation between gonad index and lunar day was observed, spawning occurring between lunar days 7 and 21, spawning was not perfectly synchronous within the population. The reproductive periodicity of T. gratilla seemed to follow the phases of the moon, gonad index peaking just after the first quarter and reaching a minimum around the third quarter, when spawning presumably occurred. Gaudette et al. (2006) carried out a time series of fertilization assays, measurements of gonad index, and environmental monitoring, and suggested that a combination of cues influenced spawning in Strongylocentrotus droebachiensis along the coast of Maine (USA). First, synchrony in
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fertilization between the two sites studied suggested that male spawning was triggered by a large-scale environmental cue. Spawning events at Pemaquid Point were correlated with the lunar cycle, with peak intensity at the new and full moons. However, at Little Cove, the model revealed a semi-lunar cycle with a significantly stronger spawning peak around the full moon. There has been much speculation about the adaptive significance of lunar reproductive patterns in echinoids. Some authorities believe that the reproductive activity of adults may be restricted to particular lunar phases by other environmental factors (Kobayashi, 1969; Pearse, 1972), whereas others (Iliffe and Pearse, 1982; Kennedy and Pearse, 1975) view lunar periodicity as a means of achieving reproductive synchrony. After studying eight echinoids from the San Blas Archipelago (Panama), Lessios (1991) found that these explanations failed to account for the occurrence of a lunar rhythm in some species but not in others, and suggested that such rhythms were an adaptation to the particular reproductive requirements of the species. Comparisons of life history traits and reproductive output may lend support to this hypothesis (Drummond, 1995). The question as to whether lunar spawning in echinoids and other marine invertebrates is linked directly to moonlight or is a result of tidal cycles remains open. In his review of lunar breeding rhythms, Korringa (1947) distinguished those apparently related to moonlight from those related to tides. Synchronization of gamete release with tides has not been shown in echinoids and remains speculative for other echinoderms (see Section 2.6). Pearse (1972) originally argued in favour of tides to explain lunar spawning periodicity in Centrostephanus coronatus, but a later study provided evidence to support the primary role of lunar luminance (Kennedy and Pearse, 1975). A similar conclusion was reached by Lessios (1991) based on the fact that photosensitivity had been documented for many echinoid species and that variations in water levels in Panama were slight and not always due to tides. However, few investigations have ever considered that variations in barometric pressure could provide the effective cue.
2.6. Tides and currents The periodic rise and fall of tides profoundly affect coastal marine organisms. Distribution, abundance, reproduction, feeding and other activities may vary as a function of the tidal cycle or tidal amplitude cycle. The former refers to the semi-daily or daily sequence of high and low tides, and the latter is the biweekly cycle of the daily difference in the height of high and low tides that is usually synonymous with the spring neap cycle (Morgan, 1996). Spawning at low tide may increase the concentration of gametes, and hence maximize fertilization success, by reducing the volume of water into which gametes are released (McDowall, 1969).
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2.6.1. Ophiuroidea Several authors have proposed that tides and currents contribute to the selective pressure leading to adaptations in the reproductive periodicity of ophiuroids (Hendler, 1991; Singletary, 1970; Smith, 1940b), but such a correlation has never been investigated in depth and only speculations have been reported in the literature. Hendler (1979) suggested that seasonal changes in water circulation patterns and water turbulence, and their effect on larval dispersal, might be important in the timing of the reproductive cycle in ophiuroid species he studied along the Atlantic and Pacific coasts of Panama. Finally, Morgan and Jangoux (2002) indicated that strong currents might be essential for gamete release in Ophiothrix fragilis from the Netherlands. 2.6.2. Holothuroidea In addition to temperature, lunar cycles and light, current speed and tidal patterns may affect the reproduction of intertidal holothuroids (Billett and Hansen, 1982; Costelloe, 1985; Engstrom, 1980; Rutherford, 1973). During field observations in Puget Sound (eastern USA), Engstrom (1982) noticed that gamete release in Pseudocnus lubricus (¼Cucumaria lubrica) usually coincided with periods of minimal tidal currents and suggested that such conditions could trigger spawning in this brooding species. Following combined field and laboratory studies of several intertidal species from the northeast Pacific, McEuen (1988) suggested that the correlation between spawning behaviour and type of habitat depended on the conditions appropriate for gamete mixing and fertilization. Sea cucumbers living in dynamic rocky habitats influenced by strong tidal currents would be likely to spawn during periods of slack water, whereas those on shallow mud bottoms would release their gametes in a weak current rather than in still water to ensure adequate suspension of the gametes in the water column (McEuen, 1988). The in situ observations compiled by McEuen (1988) indeed indicated that large populations of sea cucumbers inhabiting high current areas in the San Juan archipelago (USA) released their gametes during periods of slack water. Hamel and Mercier (1995a) also observed spawning at low tide in the dendrochirotid Cucumaria frondosa from the St. Lawrence Estuary (Canada), and suggested that this would increase gamete concentration and favour fertilization success. In species that regularly experience periods of high and low current velocity, the lack of seawater circulation may enhance spawning in the laboratory (McEuen, 1988). Another view is that temperature and desiccation are critical factors affecting intertidal species (Boolootian, 1966; Cameron and Fankboner, 1986; Harriott, 1985) and tidal oscillations can expose these species to sudden changes in these two factors (Catalan and Yamamoto, 1994).
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2.6.3. Asteroidea The possible influence of tides or currents on the spawning of asteroids has received little attention. Ohshima and Ikeda (1934) found that very few superposed couples of Archaster typicus were found deeper than 30–40 cm at high tide and that A. typicus searched for a mate as the tide receded. The spawning of Acanthaster planci at Davies Reef (Australia) was recorded just after low tide (Babcock and Mundy, 1992). Finally, upwelling currents may influence or control spawning in some tropical asteroids (Carvalho and Ventura, 2002). 2.6.4. Echinoidea Correlations between water movements and the reproduction of echinoids are even more tenuous. Boolootian et al. (1959) indicated that spawning of the deep-water sea urchin Allocentrotus fragilis in the Monterey Canyon area off the west coast of the USA was possibly initiated by the annual upwelling of deeper water. Based on gonad indices, spawning of Echinometra lucunter in Barbados occurred during a single discrete period from July to October in a wave-swept location, but twice annually in populations from a calmer environment (Lewis and Storey, 1984).
2.7. Salinity Salinity is not a commonly proposed environmental trigger of spawning activity, since fluctuations in salinity are typically minimal, short-lived and/ or irregular in most regions, although shallow coastal areas and estuaries may experience significant and extended variations in salinity (i.e., during heavy rainfalls or spring thaws). While the reproduction of some species may be correlated with salinity changes in certain coastal areas of India (Giese and Pearse, 1974), suggestions that salinity acts as a spawning cue remain largely speculative. 2.7.1. Ophiuroidea A brief reference was made by Valentine (1991b), who indicated that spawning in Microphiopholis atra and Hemipholis elongata in Mississippi Sound (USA) occurred when a salinity change was recorded. 2.7.2. Holothuroidea Some authors (Krishnaswamy and Krishnan, 1967; Ong Che and Gomez, 1985) have suggested that salinity is a spawning cue for the sea cucumber Holothuria scabra in India and the Philippines, although this has not been supported experimentally. Furthermore, no comparable semi-annual changes in salinity occur in New Caledonia and Australia where the species also occurs (Harriott, 1982). Ramofafia et al. (2003) reported that spawning
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of H. scabra in the Solomon Islands may be opportunistic in order to respond to ephemeral favourable conditions. Although H. scabra reportedly spawns year round, a spawning peak from September to December was consistently observed over the 3 years of their study. While spawning coincided with the dry season, suggesting a link with salinity, it was also concurrent with a period of increased day length and seawater temperature (Ramofafia et al., 2003), making it difficult to determine a specific cue. 2.7.3. Echinoidea A correlation between high breeding activity and the rainy season has been suggested to occur in Strongylocentrotus purpuratus (California, USA) and Stomopneutes variolaris (Madras, India) (Giese et al., 1964). Although Pillay (1971) suggested that favourable salinity conditions during the pre- and post-monsoon months could dictate the time of reproduction in a SW Indian population of S. variolaris, Drummond (1991) found that this species also reproduced at this time at Oslo Beach (South Africa) and in the Southwest Indian Ocean. High rainfall during the SW Indian monsoon might lower salinities at the latter location, but salinity cannot be evoked for Oslo Beach where the mean monthly rainfall in summer is three times less. Drummond (1991) therefore suggested that ecological factors such as fluctuations in food supply to adults or larvae, presence or absence of predators of larvae and/or current or tidal conditions which might affect settlement of larvae, may play a role in the timing of reproduction in S. variolaris. Moore and Lopez (1972) described a possible correlation between rainfall and reproduction in Lytechinus variegatus on the eastern cost of Florida (USA). An extended spawning period and greater gonad output were associated with higher than average annual rainfall, although appearance of young echinoids on the shore occurred in years of low rainfall. The authors could not predict whether rainfall acts through the lowering of salinity in Biscayne Bay or through an increase in river discharge bringing material into the area, which would augment the food available to the sea urchins. Furthermore, their data on gonad volume and occurrence of juvenile urchins in the field were not gathered during the same years. Lessios (1981) postulated that salinity could act as a proximate cue for controlling the timing of spawning as it coincided with increased salinity for Echinometra lucunter and E. viridis at Fort Randolph (Panama).
2.8. Inter-population and inter-individual communication Marine invertebrates can increase fertilization success by forming spawning aggregations, spawning synchronously, and spawning under favourable environmental conditions (e.g., minimal water movement to reduce the dilution of gametes) (Giese and Pearse, 1974; Levitan et al., 1992). Synchronous gamete release can increase fertilization success only if the spawning
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organisms are close enough to one another; synchronization alone may not be sufficient if gametes are emitted by individuals distant from each other (Levitan, 2004). Mechanisms involving detection of conspecifics, especially those of the opposite sex, may evolve under such selective pressures (e.g., Beach et al., 1975; Miller, 1989; Painter, 1992; Series, 1996; Soong et al., 2005; Zeeck et al., 1988). This section analyses four different types of evidence of chemical signalling related to reproduction: intra-specific breeding aggregation, asynchronous gamete release by males and females, inter-individual communication prior to or during spawning, and simultaneous heterospecific mass spawning events. 2.8.1. Aggregation The timing of spawning and the distribution of spawning individuals may have an important effect on the reproductive success of broadcast spawners (Levitan, 1988) in part because gametes have limited longevity and disperse quickly in seawater (Pennington, 1985). While periodicity in gametogenesis and spawning may increase reproductive success by favouring simultaneous gamete release, high population density and aggregative behaviour may have the same benefit, since individuals are releasing gametes in close proximity (Levitan, 1988). Such behaviour will influence fertilization success in echinoderm species that exhibit external fertilization (Lamare and Stewart, 1998). It is generally believed that aggregative behaviour, even if it is independent of spawning, will increase spawning success. General gregarious behaviour is common among echinoderms. It has been observed in ophiuroids (Hagman and Vize, 2003; Warner, 1979), holothuroids (Rodgers and Bingham, 1996), asteroids (De’ath and Moran, 1998; Himmelman and Dutil, 1991; Sloan and Aldridge, 1981), and echinoids (Levitan et al., 1992; Pearse and Cameron, 1991; Young et al., 1992). However, the function of aggregations is still not fully understood. Breeding aggregations have now been observed in a number of ophiuroids (Himmelman et al., 2008), asteroids (Hamel and Mercier, 1995b; Mercier and Hamel, 2008; Ormond et al., 1973; Scheibling, 1980; Slattery and Bosch, 1993), echinoids (Levitan et al., 1992; Young et al., 1992), and holothuroids (Mercier et al., 2000a; Tyler et al., 1992). Many authors have suggested that such behaviour enhances the synchronous final maturation of gametes, minimises sperm dilution, maximizes gamete viability and increases fertilization success. Extreme cases of pseudo-copulation have been observed in asteroids (Komatsu, 1983; Ohshima and Ikeda, 1934; Run et al., 1988; Slattery and Bosch, 1993). In their study of bathyal echinoid populations, Young et al. (1992) suggested that aggregations could be useful in overcoming the absence of the usual environmental cues (e.g., light, temperature) on which coastal populations rely to synchronize reproductive processes.
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(a) Ophiuroidea Although general displays of gregariousness may be related to reproductive behaviour (Hendler, 1991), breeding aggregations proper are rarely reported in ophiuroids. Thus, as stated by Brun (1969) many decades ago, there remains controversy over whether some aggregations are the result of true social behaviour, or whether the gregarious and concomitant behaviour is simply a result of an interaction with the physical environment (Allee, 1927; Reese, 1966). Nonetheless, evidence of sexually related aggregations has been presented. Associations between males and females of several species of ophiuroids have been described in the literature (reviewed by Hendler, 1991), such as for Ophiodaphne materna (¼formata) and Gorgonocephalus chilensis. Gorzula (1976) reported active male–female pairing for 1 day during the spawning season of Ophiocomina nigra but did not observe any spawning. This species reportedly avoids intersexual contact outside of the breeding season (Warner, 1979). Deheyn et al. (2000) studied luminescence in Amphipholis squamata in France and suggested that light emission normally associated with defense could also serve as an intra-specific visual signal that may help individuals aggregate at the time of reproduction, as suggested for luminous elasipod holothurians (Gutt and Piepenburg, 1991). While attempting to determine potential spawning inducers, Selvakumaraswamy and Byrne (2000) reported that five species of ophiuroids from New Zealand and Australia required aggregation of both sexes for spawning and fertilization to occur. Furthermore, pairing between females and diminutive males of small sexually dimorphic species has been reported and suggested to be an adaptation for mating success among individuals that live on a mobile infaunal host (Hendler, 1991). Although such a pairing is observed throughout the year in Ophiodaphne formata from the Sea of Japan, including in the non-breeding season, this behaviour is probably essential to reproduction, because spawning occurs during pairing according to Tominaga et al. (2004). From in situ observations in the Gulf of Mexico, Hagman and Vize (2003) found that males of Ophioderma nubicundum tended to aggregate on the apices of coral heads during spawning, whereas the less abundant O. squamosissimum did not form aggregates, although males were often observed within 3 m of each other. Aggregations of spawning males typically developed up to half an hour before the emergence of females, which were not gregarious (Hagman and Vize, 2003). In the cold-temperate waters of the Gulf of St. Lawrence (eastern Canada), divers observed spawning in paired individuals of Ophiopholis aculeata and Ophiura robusta (Himmelman et al., 2008). (b) Holothuroidea It has long been suspected that aggregation in holothuroids may be related to reproductive processes (Reese, 1966).
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Although pseudo-copulatory behaviour has not been observed very often in holothuroids, migration for the explicit purpose of reproduction has been suggested (Glynn, 1965; Jordan, 1972; reviewed by Smiley et al., 1991), and there is increasing evidence that the aggregative habits of some species are related to reproduction (Hamel and Mercier, 2004). Spawning in Cucumaria pseudocurata lasts no more than a few days for a given population, and for 2 or 3 weeks at the most for the entire range from Monterey (California, USA) to Vancouver Island (western Canada) (Rutherford, 1973). The investigator proposed that this might be related to the aggregation behaviour of the species, which would be conductive to mass spawnings lasting hours or days (Rutherford, 1973). McEuen (1988) reported that paired adults of Parastichopus (¼Stichopus) californicus wrapped their raised fore-ends around each other while spawning on the west coast of Vancouver Island (Canada). Groups of 2–4 intertwined individuals of the hermaphrodite Leptosynapta clarki have been observed during the reproductive season (Everingham, 1961; McEuen, 1988). Rodgers and Bingham (1996) proposed that aggregations of the sea cucumber Pseudocnus lubricus (¼Cucumaria lubrica) were a result of their subtidal zonation in response to light. Babcock et al. (1992) reported active clustering of spawning individuals of Bohadschia argus and Euapta godeffroyi on the Great Barrier Reef (Australia). Cyclic aggregations of adults, observed during experiments in outdoor tanks, closely followed the lunar spawning pattern of Holothuria scabra in the Solomon Islands (Mercier et al., 2000a). The formation of pairs, trios or larger groups increased during the new moon and was most common just before the full moon (Fig. 2.5). Since no clusters were observed in individuals <120 mm long, the size around which they reach sexual maturity (Mercier et al., 1999), and given that maximum aggregation usually occurred just before spawning events, aggregative habits of H. scabra appear to be related to reproduction (Mercier et al., 2000a). Male and female spawnings were observed in the tanks, generally around the full moon. Spawning occurred during the peak in aggregation and afterwards, when the individuals were more evenly distributed (Mercier et al., 2000a). Conversely, VandenSpiegel et al. (1992) did not observe any aggregative behaviour in H. scabra populations from Papua New Guinea. Interesting observations were reported by Desurmont (2008) during successive dives around New Caledonia in January 2008: an isolated individual of Stichopus herrmanni perched on a coral formation spawned on the first day; the next afternoon another individual had joined the first one and both were spawning, while a third specimen was releasing gametes ca. 50 m away. On the third day, the first spawner had ceased releasing gamete but remained in the same location, whereas the other two were still spawning. On the fourth and last day, all three animals had migrated back to the
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bottom of the reef and were no longer releasing gametes (Desurmont, 2008). Several authorities have suggested that deep-sea holothuroids can aggregate for reproductive purposes. Photographic evidence has been provided for various species by Barham et al. (1967), Heezen and Hollister (1971), Menzies et al. (1973), Pawson (1976, 1982), Ohta (1983) and Grassle et al. (1975). Furthermore, Billett and Hansen (1982) reported mean densities of 4–50 ind. m2 for Kolga hyalina in the deep ocean west of Ireland, with coefficient of dispersion varying from 1.1 (random) to 11.9 (clumped), and concluded that heterogenous patterns in the distribution resulted from temporal aggregations. Since these elasipod holothuroids often occur in submarine trenches, troughs or canyons, possible explanations for the observed aggregations include synchronized reproduction events and/or improved food conditions (Barham et al., 1967; Stanley and Kelling, 1968). Some deep-sea holothuroids occur in pairs more frequently than in larger aggregations. Species that form pairs are all hermaphroditic. For instance, individuals of the genus Paroriza have often been observed or photographed in pairs and triplets. Furthermore, P. prouhoi (Mauviel and Sibuet, 1985) and P. pallens (Tyler et al., 1992) occur both as singletons and pairs, although the tracks they leave on the seafloor suggest they move side by side for some distance. Oocyte size frequency distributions in P. pallens are consistent with ‘‘continuous’’ or aperiodic reproduction and do not differ significantly between paired and unpaired specimens collected during the same season (Tyler et al., 1992). The authors hypothesized that pairing increased the likelihood of external fertilization and that spawning in these species may be induced at any time by the presence of a conspecific rather than by seasonal cues. (c) Asteroidea Many authors have associated aggregation in asteroids with cooperative feeding or predation avoidance (Blankley and Branch, 1984; Ormond et al., 1973; Sloan, 1984), although the possible role of pheromones and other exudates (e.g., sperm solution) on clustering and spawning has been explored (Lewis, 1958; Miller, 1989). Pairing, aggregations and behavioural interactions related to spawning have been reported in several species. Early reports of inshore migration of sea stars prior to breeding in the North Pacific (Verrill, 1914) are in accordance with many later accounts that are further described below. Breeding aggregations are common in species that exhibit demersal lecithotrophic development, with or without brooding. Ludwig (1882) described a case of arm interlocking while spawning in the sea star Asterina gibbosa. Similarly, males of the brooding species Leptasterias ochotensis similispinus twist their arms with those of the females before spawning (Kubo, 1951). Males and females of other brooding Leptasterias spp. have often been reported to simply congregate before or during spawning, for example,
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L. hexactis (Chia, 1968), L. littoralis (O’Brien, 1976) and L. polaris (Hamel and Mercier, 1995b). Pseudo-copulation preceded by exploration, contact, and mounting of a female by individual or multiple males has been documented in Neosmilaster georgianus (Slattery and Bosch, 1993). Free-spawning species also form aggregations at the time of reproduction. Komatsu et al. (1979) described annual breeding assemblages of the hermaphroditic sea star Asterina minor in the laboratory in Japan. Although spawning was not observed in the field, clustering of individuals was often seen in May. Instability in the groups lasted ca. 10 days before the assemblage became stable and individuals no longer seemed to move between groups. Clustered individuals clung to each other along the margins of their bodies, or overlapped one another to some extent. Spawning by members of a group was quite synchronous within a period of 6 h, after which the assemblage disintegrated (Komatsu et al., 1979). Tominaga et al. (1994) also observed spawning aggregation in the sea star A. minor from the Echizen Coast ( Japan). During the breeding season, only mature individuals aggregated, and did so for about 2 weeks. The authors proposed that grouped individuals were waiting for their numbers to increase before they spawned, in order to maximize fertilization success. They dispersed quickly after spawning without cleaning or brooding their eggs (Tominaga et al., 1994). Minchin (1987) observed several individuals of Marthasterias glacialis aggregating at the time of spawning in Ireland. Aggregated individuals showed no sign of recent feeding, whereas solitary individuals were frequently seen to feed. The author postulated that aggregations might be elicited by a pheromone released by females, which could explain the greater proportion of males (1.6:1) present throughout the study site (Minchin, 1987). Examination of the dispersion index revealed that Astropecten irregularis was significantly more aggregated during the summer months in Red Wharf Bay, North Wales (UK) (Freeman et al., 2001). Spawning assemblages of this species have also been reported during the summer months in Japanese waters (Nojima, 1983). To explain the fact that the gonad index did not always correspond with the highest population density of A. irregularis, the authors stated that the sea stars might have already aggregated and released most of their gametes between successive sampling periods (Freeman et al., 2001). In the Gulf of St. Lawrence (eastern Canada), in situ observations of Asterias rubens (¼vulgaris) revealed that many individuals were tightly aggregated during gamete release, especially during the mass spawning event (Himmelman et al., 2008; Raymond et al., 2007). Other free-spawning dioecious species such as Archaster typicus (Ohshima and Ikeda, 1934; Run et al., 1988) and Acanthaster planci (Beach et al., 1975; Komatsu, 1983; Ormond et al., 1973) also aggregate for breeding. In a laboratory study of the bathyal sea star Henricia lisa, Mercier and Hamel (2008) found that clustering occurred twice a year during the summer and winter breeding periods, presumably to ensure that males
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and females came together to finalize gamete maturation, synchronize spawning, and promote fertilization success.
(d) Echinoidea Inshore migration of Echinus esculentus has been observed at Port Erin (Isle of Man, Irish Sea) prior to the breeding period (Stott, 1931). Ripening Tripneustes esculentus in Barbados also tend to aggregate before spawning (Lewis, 1958). A recent review of Paracentrotus lividus (Boudouresque and Verlaque, 2007) indicates that aggregations and simultaneous spawning of both sexes are known to occur. Around PortCros Bay (France), spawning aggregations of 10–20 individuals lasted a few hours at sunset on prominent stones or at the top of leaves of the seagrass Posidonia oceanica (Boudouresque and Verlaque, 2007). Spawning is reportedly partial at the population level (Allain, 1975). Lewis (1958) observed that the sea urchin Tripneustes esculentus, which is usually dispersed over rocky surfaces and Thalassia sea grass beds in Barbados, aggregated under rocks and ledges in groups of up to 12 specimens prior to the spawning season in March–April. Y-maze experiments suggested that chemical attraction between individuals plays a significant role in aggregation behaviour in the echinoid Evechinus chloroticus (Dix, 1969). Pennington (1985) reported that four out of eight reports of sea urchins spawning in the field were associated with aggregations, for example, in Diadema antillarum, Heliocidaris erythrogramma, Strongylocentrotus franciscanus and an unidentified species. Aggregative behaviour in species of Diadema has often been documented. Thus, Randall et al. (1964) observed D. antillarum spawning in cohesive groups in the West Indies between 1959 and 1964. Bauer (1976) suggested that such aggregative behaviour in D. antillarum was more pronounced during the new moon. Aggregations in this species were also observed by Levitan (1988), but only 5% of the specimens were spawning simultaneously. As the author pointed out, it is possible that major spawning events were missed, although the chance of this occurring at the site at which spawning was induced by KCl is small, since reproductive readiness slowly decreased from a peak (Levitan, 1988). Although it was not verified, the possibility exists that sporadic spawning of a relatively small number of gametes might signal reproductive readiness and lead to a major spawning event (Levitan, 1988). Observations made in Doubtful Sound (New Zealand) suggested that individuals of Evechinus chloroticus formed patches in shallow water. They released gametes in a mass spawning event that lasted ca. 1 h in late January 1994 (Lamare and Stewart, 1998). The aggregation of individuals at the low-salinity boundary may have further enhanced gamete concentration (and hence fertilization rate), as the upper depth distribution of gametes was apparently bounded by the low-salinity layer (Lamare and Stewart, 1998). Furthermore, the percentage of individuals spawning in the population
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increased from 10% to 90% over the study period, suggesting the possible role of conspecific-induced spawning (Lamare and Stewart, 1998). The brief occurrence of homosexual and heterosexual pairing was random in Lytechinus variegatus in Biscayne Key (Florida, USA) according to the sex ratio found in each population census (McCarthy and Young, 2002). There was no evidence of aggregations that lasted throughout the reproductive season (McCarthy and Young, 2002). The authors suggested that given the relatively high population density, individuals may be able to release some gametes during each conspecific encounters, thereby ensuring genetic variability in the population despite the loss of 50% of the gametes to homosexual pairings. They concluded that intermittent spawning should occur frequently during a relatively long breeding period in the spring and a shorter one in the fall in the L. variegatus population off the southeast shore of Virginia Key in Biscayne Bay, and deemed it more likely that short-term aggregations, such as those observed in Sphaerechinus granularis (Unger and Lott, 1994), rather than long-term (seasonal) aggregations should occur in L. variegatus. The density and movement of this species is presumably high enough to result in numerous intra-specific encounters which may improve fertilization success when the appropriate external cues, such as gametes, induce spawning (McCarthy and Young, 2002). In a later study, McCarthy and Young (2004) observed that individuals of Lytechinus variegatus occurred either alone or in small aggregations at both Virginia Key and Jupiter Inlet (Florida, USA). Immature specimens were occasionally found in pairs at Virginia Key, whereas all pairs were composed of ripe individuals at Jupiter Inlet. The sex ratio and number of ripe individuals in both upstream and downstream groups of urchins were similar at both sites. Aggregated sea urchins failed to respond to waterborne gametes, although some of them were triggered to spawn by KCl injections (McCarthy and Young, 2004). The authors suggested that mature individuals: (1) may not easily find each other, (2) stayed together when they randomly encountered each other, (3) were responding to a localized cue to aggregate temporarily, or (4) did not aggregate for the purpose of reproduction. In situ observations in an Irish inlet revealed that Paracentrotus lividus formed compact groups during spawning events involving tens to hundreds of individuals. The sea urchins climbed on rocks or on each other during gamete release and resumed their normal activities after spawning (Minchin, 1992). According to a recent review by Young (2003), a number of deep-water Bahamian-slope echinoids, including Aspidodiadema jacobyi, Cidaris blakei, Salenia goesiana and Stylocidaris lineata form tight aggregations or pairs during the breeding season (Fig. 2.11), presumably to circumvent the problem of isolation at spawning. In the latter species, homosexual and heterosexual pairs occurred at the relative frequencies predicted by the sex ratio at depths
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of 513–640 m (Young et al., 1992). All individuals examined in February possessed developing gametes, regardless of their spatial distribution. In contrast, most isolated individuals had spent gonads during the May breeding season, whereas grouped individuals largely displayed gonads with mature or nearly mature gametes. Furthermore, aggregations were not observed when gonads were spent or immature during the autumn months (Young et al., 1992). 2.8.2. Asynchrony between the sexes While spawning of echinoderms has been the focus of many investigations, the timing difference between males and females of a given species is not always reported (Giese and Kanatani, 1987; Hamel and Mercier, 1995b; Minchin, 1987; Ormond et al., 1973; Pearse et al., 1988; Pennington, 1985), but males usually begin spawning before females in echinoderm species (see below), although in some cases the opposite occurs. It is possible that a chemical compound associated with sperm, or another component of the male spawn, acts as a spawning inducer in females (see Section 2.8.3 for details). (a) Crinoidea In several crinoids, males begin to spawn shortly before females, suggesting that pheromones from the former stimulate the latter (Clark and Clark, 1967; Dan and Kubota, 1960; Fishelson, 1968; Mortensen, 1938; Seeliger, 1892), but there is no supporting experimental evidence. Males of Oxycomanthus japonicus usually spawn for several days, releasing sperm every afternoon starting a few days before the date when most females spawn (Kubota, 1981). Gamete release in females extends over a few days, although there is usually one main event (Holland et al., 1975; Kubota, 1981). Furthermore, some females spawn while in complete isolation from males and other females, implying that communication between individuals is not necessarily a requirement for spawning synchrony in this species (Holland, 1991). (b) Ophiuroidea Observations of either sex spawning first, males and females spawning simultaneously and females spawning alone have been recorded in ophiuroids (reviewed by Hendler, 1991). Since the first report of male-first spawning, which was for Ophiura ophiura (Selenka, 1892), the behaviour has been observed in many other species, for example, Amphiura filiformis, Ophiocoma echinata, Ophioderma brevispinum, Ophiopholis aculeata, Ophiothrix fragilis and Ophiothrix orstedii (Grave, 1916; Hendler, 1991; Litvinova, 1981; Mladenov, 1976, 1979; Morgan and Jangoux, 2002; Mortensen, 1920b; Ockelmann and Muus, 1978; Olsen, 1942; Taylor, 1958). Mladenov (1976, 1979) noted that when Ophiothrix oerstedi and O. suensoni spawned in the laboratory in Barbados, males generally initiated
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spawning, followed by females and then more males. From field observations, Hagman and Vize (2003) determined that males of both Ophioderma rubicundum and Ophioderma squamosissimum from the north-western Gulf of Mexico (USA) started releasing their gametes 30 min before females. Numerous exceptions to this general pattern of males initiating spawning include females spawning before males in Amphioplus abditus, Ophiocoma echinata, and Ophiopholis aculeata, both genders spawning simultaneously (Ophionereis squamulosa) and isolated females spawning (Allee and Fowler, 1932; Hendler, 1977; Holland, 1979; Mortensen, 1938). Soong et al. (2005) suggested that female-first spawning in Ophiocoma dentata and O. scolopendrina may serve to offset sperm limitation and minimise outbreeding (Soong et al., 2005). (c) Holothuroidea As in many other echinoderms, males of holothuroids often spawn before females, suggesting that the latter respond to the presence of spermatozoa or to other chemicals released with sperm. A slightly different interpretation of the male–female asynchrony is that females exude a pheromone during or after oocyte maturation or ovulation (stimulated by a so-called ‘‘maturation-inducing substance’’), triggering male spawning, and that the seminal fluid of males could thereafter act as the proximal cue for female gamete release (Smiley et al., 1991). Males of Aslia lefevrei in Galway Bay (Ireland) and Pseudocnus lubricus (¼Cucumaria lubrica) in Puget Sound (USA) generally spawn before the females (Costelloe, 1985; Engstrom, 1982). The latter study revealed that male and female spawnings were separated by several hours both in the field and in the laboratory. Nyholm (1951) reported that when several specimens of the hermaphroditic sea cucumber Labidoplax buskii were kept together in a tank, sperm release in some individuals was followed shortly by oocyte release in others. In situ observations of several species of holothuroids on the Great Barrier Reef (Australia) over several years have also shown that males typically spawn first (Babcock et al., 1992). For Bohadschia argus, this pattern was consistent among the 34 individuals observed on eight separate occasions (Babcock et al., 1992). Hamel and Mercier (1995a) observed in situ massive spawning of the sea cucumber Cucumaria frondosa in the Lower St. Lawrence Estuary (eastern Canada). The first individuals to spawn were males and the peak of male spawning occurred ca. 45–60 min before the mass spawning of females, so that when the oocytes were released the water column was almost entirely filled with a whitish cloud of sperm (Hamel and Mercier, 1995a). Fertilization success was thus very high (Hamel and Mercier, 1996d). The ‘‘epidemic’’ nature of the spawning was emphasized by the timing of the entire event, male spawning having begun on 17 June at 05:00 h, when only a few isolated males released their gametes. Seven hours later, the proportion of spawning individuals had increased, reaching
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5% of the 300 observations made. However, spawning by males only became generalised in the entire population around 14:00 h, when more than 65% of males were spawning. The highest number of spawning individuals (83% of the total) was recorded at 15:00 h. Female spawning began at 14:00 h, with numerous isolated individuals starting to release oocytes. The first spawnings of isolated females always occurred within 5 m of a spawning male. Maximum female spawning (87%) was observed at 17:00 h following a decrease in male spawnings to less than 32%. Around 18:00 h, <12% of females were still releasing gametes. A small proportion of males and females continued to spawn until 07:00 h the next morning (Hamel and Mercier, 1995a). (d) Asteroidea Chia (1968) indicated that gametes from congeners could induce spawning in Leptasterias hexactis at Friday Harbor (Washington, USA). O’Brien (1976) noted that males of L. littoralis along the coast of Maine (USA) spawned before females and that individuals of both sexes were in close proximity to one another during spawning. McClary and Mladenov (1988) suggested that females of Pteraster militaris spawned in response to sperm or substances released with it. They mentioned that this species from the NW Atlantic may thus be opportunistic by releasing gametes only when the probability of fertilization is relatively high. Conversely, spawning by a female Archaster typicus in Taiwan was closely followed by spawning of its paired male; male spawning, however, did not induce spawning in the female (Run et al., 1988). Spawning in Leptasterias polaris from the St. Lawrence Estuary (eastern Canada) was not synchronous during experimental trials conducted under controlled conditions (Hamel and Mercier, 1995b), and males began releasing sperm before any female spawning was detected. The behaviour of L. polaris sperm may explain the need for aggregation and male–female asynchrony. Upon release, only a portion of the sperm are dispersed by currents and remain active as long as they are maintained in the water column, possibly providing a stimulus for females to spawn (Hamel and Mercier, 1995b). The negative buoyancy and stickiness of the sperm causes most of them to settle on the substrate, where they gradually become inactive (Hamel and Mercier, 1995b). This settlement ensures at least some dispersion of sperm but makes fertilization dependent on the proximity of individuals, which is achieved by aggregation; sperm inactivation seems to be an effective energy-saving mechanism, extending the viability of settled sperm to 6 or 7 days, compared with the 2- to 3-day longevity of sperm in the water column (Hamel and Mercier, 1995b). The longevity of sperm is probably an advantage given the asynchronous spawning of the sexes in L. polaris. Once a female has spawned on the sperm-covered substrate, the oocytes can reactivate the inactive sperm, allowing fertilization to take place (Hamel and Mercier, 1995b). Experimentally, the best
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success (>75%) was achieved when the delay between the male and female spawnings was no more than 11 h, although success was still good (ca. 50%) after as long as 30 h (Hamel and Mercier, 1995b). Sperm inactivity followed by reactivation appears to be very rare in marine invertebrates. Although sperm chemotaxis occurs in echinoderms (Miller, 1985), no significant velocity increase in, or activation of, the attracted sperm has ever been recorded. In a monitoring study of the deep-sea asteroid Henricia lisa for nearly 2 years in the laboratory, males in a reproductive cluster always spawned first and females usually responded within 30–60 min, suggesting that females respond to a cue emitted by males (Mercier and Hamel, 2008). (e) Echinoidea In Strongylocentrotus franciscanus off the coast of British Columbia (western Canada), males spawned for an hour and a half before females commenced, and both stopped spawning simultaneously about 1 h later (Levitan, 2002b). Levitan (2005) also indicated that the interval between the onset of male and female spawning should be correlated with the duration of sperm release by males, selection favouring males that spawn before and during egg release but stop in near synchrony with females. 2.8.3. Evidence of chemical communication In spite of the increasing and convincing evidence for aggregative behaviour as a function of reproduction (Section 2.8.1), and the frequent asynchrony observed between male and female spawning (Section 2.8.2), the question of inter-individual chemical communication remains elusive. Twenty years ago, there was little evidence that echinoderms and other benthic invertebrates use chemical signals to recognise the opposite sex at a distance (Miller, 1989). In his review of echinoderm behaviour, Reese (1966) barely mentioned chemical interactions in free-spawning adults. More recently, correlative evidence has built up and a number of convincing experimental studies have been published, thus strengthening our understanding of interindividual communication at the time of reproduction. (a) Crinoidea Massive spawning of Oxycomanthus japonicus occurs once a year, mostly in the same afternoon for a given population (Dan and Dan, 1941; Dan and Kubota, 1960), implying a high degree of synchrony. Holland and Grimmer (1975) observed that the abundance of epidermal mucus increased noticeably in the 6–8 weeks prior to spawning in both males and females of O. japonicus, although the increment was about 10 times greater in the latter than in the former. The number of mucous cells declined abruptly in females and gradually in males after spawning, supporting the hypothesis that the mucus has some function in the reproductive biology. Emission of mucus in seawater may thus act as a
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pheromone to stimulate epidemic spawning (Holland and Grimmer, 1975), although gamete release has been observed in both sexes of O. japonicus maintained in isolation (Dan and Dan, 1941). Fishelson (1968) noted that males and females of Lamprometra klunzingeri spawned synchronously at sunset, possibly via the action of a spawning cue from the environment or some kind of inter-individual pheromonal exchange. Lahaye and Jangoux (1985) suggested that spawning entices nearby individuals to spawn in Antedon bifida. (b) Ophiuroidea At the time of the review by Hendler (1991), spawning aggregations, pairing and other overt displays of reproductive behaviour had seldom been observed in ophiuroids. Mortensen (1920b) noted that in Amphiura filiformis from Scandinavia the males were the first to spawn and that they induced spawning in females. He also made the significant observation that although temperature was high enough to induce spawning in an aquarium, salinity was too low to activate the sperm and no discharge of oocytes took place, strongly inferring that spawning in females is induced by active sperm only. Good accounts have recently been added to the scientific literature. Five species of brittle stars from Australia and New Zealand (Ophiactis resiliens, Ophionereis fasciata, Ophiothrix caespitosa, Ophiothrix spongicola and Ophionereis schayeri) were found to require an aggregation of males and females for spawning and fertilization to proceed (Selvakumaraswamy and Byrne, 2000). Moreover, females of Ophionereis schayeri released oocytes only in the presence of sperm, suggesting that the follicle-enclosed oocytes may require sperm in order to initiate a hormonal cascade (Byrne, 1994; Moloney and Byrne, 1994). In contrast, oocytes released by Ophiothrix spongicola in the absence of males were unfertilizable, whereas those released in the presence of spawning males were competent, possibly indicating that a male pheromone associated with spawning might be required for fertilizable oocytes to be produced after the final meiotic division (Selvakumaraswamy and Byrne, 2000). Males of Ophiothrix fragilis (Morgan and Jangoux, 2002) seem to be more sensitive to environmental spawning cues and generally spawn first, suggesting a role in inducing spawning in females. Hendler (1991) observed successive spawning of a male Ophioderma echinata and then a female under laboratory conditions. After the female deposited oocytes and moved aside, the male moved over them and spawned again. Homogenates of ovaries induced 15–60% of conspecific males to spawn in Ophiocoma dentata and O. scolopendrina from Taiwan (Soong et al., 2005). Presumably, the active compounds are released into the seawater together with the oocytes, acting as pheromones to trigger male spawning. The effect of the ovarian homogenate was species-specific and did not stimulate the females, while testis homogenate had no detectable effect (Soong et al.,
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2005). The authors proposed that the unidirectional induction was an indication of high selective pressure from sperm limitation in these species. Addition of ca. 7.8 107 g ml1 of ovarian homogenate induced 50% of male O. dentata to spawn (Soong et al., 2005). Furthermore, the investigators observed that males and females of both species were positioned close together during the spawning season, although O. scolopendrina often had high local densities, whereas O. dentata aggregated in patches of 2–3 individuals. Therefore, the absence of chemical cues for females in the spawn of males does not preclude the occurrence of other types of signals, such as contact (Soong et al., 2005). (c) Holothuroidea After observing that several species spawned together in situ, McEuen (1988) suggested that synchronization of spawning among sea cucumbers in the field could be enhanced by sex pheromones. The presence of sperm, or perhaps a factor released with them into the surrounding water, is a likely primary and/or secondary proximal signal for triggering female spawning (Smiley et al., 1991). Intermittent and incomplete release of sperm prior to major spawning events has often been observed and male holothuroids of many species are believed to be able to spawn repeatedly (Smiley et al., 1991). Furthermore, the fact that males of a species generally spawn before females supports this hypothesis (see Section 2.8.2). The bioactive properties of perivisceral coelomic fluid (PCF) during spawning have been demonstrated in four tropical species (Holothuria atra, H. leucospilota, Bohadschia argus, and B. marmorata) (Hamel and Mercier, 2004; Mercier and Hamel, 2002). Injection of PCF from a ripe individual showing spawning activity into a mature non-spawning individual triggered spawning behaviour and subsequent gamete release in 71–100% of individuals. The same PCF introduced into the immediate environment also induced spawning behaviour in 47–65% of individuals and gamete release in 20–31% of them. A broad interpretation of the data suggests that messages sent via the PCF could help holothuroids to synchronize and propagate spawning in the field (Hamel and Mercier, 2004; Mercier and Hamel, 2002). This might explain the epidemic spawning observed in numerous holothuroids, as well as in other echinoderms and marine invertebrates (Babcock et al., 1992). The authors also showed that the PCF of sexually active individuals is neither sex-specific nor species-specific among the holothuroids tested. However, PCF from echinoids and asteroids did not induce spawning (Hamel and Mercier, 2004; Mercier and Hamel, 2002). Furthermore, the time of PCF collection from the donor and the amount injected influence the stimulation of spawning posture and gamete release. However, PCF collected from a spawner just 1 h after gamete release had lost its effectiveness. Thus, PCF apparently acts as a carrier of one or more short-lived molecules involved in spawning (Hamel and Mercier, 2004; Mercier and Hamel, 2002).
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While the ability of PCF to induce spawning has been clearly established, whether it is injected or introduced into the water column, its transmission path and specific function in natural spawning events is not fully understood. PCF and/or the chemically active substance(s) it contains are normally retained within the coelomic cavity, but Doignon et al. (2003) observed that the coelomic cavity of Holothuria tubulosa is purged seasonally as an indirect result of gamete expulsion, which is accompanied by powerful muscle contractions. This behaviour increases the pressure on the pericloacal region, resulting in discharge of the coelomic contents into the environment via the coelo-cloacal ducts. This mechanism may also explain why sperm collected from spawning males can induce other individuals to spawn, since PCF in the semen may be the real trigger (Mercier and Hamel, 2002). Catalan and Yamamoto (1994) indicated that the ultimate factor affecting the spawning time of Eupentacta chronhjelmi was the presence of sympatric holothuroid species with spawning seasons overlapping that of E. chronhjelmi. Although this may result in cross-fertilization, McEuen (1988) reported that sympatric species Psolus chitonoides, Cucumaria miniata, and Eupentacta quinquesemita released their gametes at different times of the day/night presumably to avoid inter-specific gamete mixing. (d) Asteroidea Although the location of the stimulus responsible for the pre-spawning pairing of Archaster typicus has been investigated (Run et al., 1988), and a spawning pheromone in Acanthaster planci briefly described (Beach et al., 1975), no cue has been isolated or identified that would explain the pairing/aggregative behaviour of broadcast-spawning asteroids. Miller (1989) suggested the existence of chemically mediated sexual communication in the sea stars Orthasterias koehleri and Asterias forbesi via a potent long-lived sperm chemo-attractant produced only by the female. Although females of both species release sperm attractants into the surrounding seawater, a sex-specific release of sperm attractant has only been directly demonstrated for O. koehleri (Miller, 1989). The author hypothesized that release of the sperm attractant during spawning could initiate spawning in conspecifics, although the small quantities of attractant recovered experimentally implied that it was unlikely to be effective because of the large dilution in the sea. Heterosexual recognition by contact chemoreception has been demonstrated in Archaster typicus, which displays a superposition behaviour (Komatsu, 1983; Ohshima and Ikeda, 1934). Furthermore, males are stimulated to spawn directly onto the oocytes released by the females (Komatsu, 1983; Run et al., 1988), indicating that A. typicus is capable of initiating both mating behaviour in response to a contact stimulus and male spawning in response to female spawning.
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Male-on-female pairing has also been reported in Archaster angulatus (Mortensen, 1931) and Neosmilaster georgianus (Slattery and Bosch, 1993). Spawning behaviour and superposition of the common brooding species N. georgianus were observed in the field and the laboratory in Antarctica during the austral spring of 1991 (Slattery and Bosch, 1993). Pseudocopulation is generally preceded by exploration, contact, and mounting of a female by individual or multiple males. Pre-mating activity of males in the field was triggered by the spawning of a nearby conspecific female. In the laboratory, similar behaviour was elicited by the presence of spawning conspecific males, implying a lack of specificity in the putative induction. The intricate search and pseudo-copulatory behaviour exhibited by N. georgianus is apparently mediated by chemical signals released from spawners of both sexes (Slattery and Bosch, 1993). Chemoreception, particularly via terminal sensory tube-feet, has been well documented for asteroids and may account for intra and inter-specific responses (Mayo and Mackie, 1976; Sloan, 1984). In their study of Archaster typicus, Run et al. (1988) observed that pairings favoured contact of the marginal and furrow spines, a region believed to elicit escape responses in prey (Mayo and Mackie, 1976). In contrast, contact occurs between the arm tips of males and the gonopore region (i.e., arm base) of females in N. georgianus (Slattery and Bosch, 1993). However, the incidence of heterosexual pairings in N. georgianus was very high, even after contact, possibly because sex determination is enhanced by sex-specific pheromones. The fact that more than one male may be involved in pseudo-copulation suggests that males are attracted by a reproductively active pair. Contrary to the non-specific initiation of searching behaviour, sperm release is only elicited in the presence of females, presumably by a second sex-specific hormone (Slattery and Bosch, 1993). Attraction and spawning induction via gamete release in conspecifics has been described in Acanthaster planci (Ormond et al., 1973). A pheromone isolated from both testes and ovaries elicits an aggregative and spawning response in males and females (Beach et al., 1975). Babcock and Mundy (1992) described the mass spawning of A. planci on Davies Reef (Great Barrier Reef, Australia) and suggested that there must be a mechanism enabling individuals to ripen in the same season, but that such a mechanism does not explain the synchronous commencement of spawning at varying phases of the diel, lunar and tidal cycles. The final trigger for spawning of ripe sea stars is probably provided directly by some property or properties of the local water mass, such as a change in current direction or speed, a temperature change, pheromones borne by the currents, or a combination of factors (Babcock and Mundy, 1992). General pre-spawning aggregations of 4–10 individuals have been observed in Leptasterias pusilla and L. aequalis in January, February and March in Monterey Bay, USA (Smith, 1971). Commenting on this phenomenon in L. pusilla, Smith (1971) speculated that the released substance
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(neural extract) might act as a pheromone-like chemical attractant bringing members of the same species together to spawn. He argued that this hypothesis was attractive since: (1) the neuro-secretory-like vesicles are located on the external surface of the radial nerve (Unger, 1962; Uter, 1967), (2) the sea stars are capable of detecting chemical compounds in concentrations of a few parts per billions (Blumer, 1969) and (3) asteroids, like other echinoderms, are capable of absorbing molecules from the external environment at low concentrations by means of active transport (e.g., Ferguson, 1967a,b; Fontaine and Chia, 1968). Pain et al. (1982b) suggested that spawning in male deep-sea asteroids is stimulated by oocyte release during chance encounters with mature females. Alternatively, male spawning may elicit release of gametes by females, as indicated by a 2-year laboratory study of the NW Atlantic bathyal asteroid Henricia lisa (Mercier and Hamel, 2008). (e) Echinoidea Fox (1924b) and Lewis (1958) were among the first to report that sperm suspensions could stimulate conspecific echinoids to spawn, and it has often been suggested that materials released with sperm during spawning act as spawning pheromones in echinoids. However, some doubt was later raised after unsuccessful attempts to induce spawning in the laboratory with sperm suspensions (Palmer, 1937; Pennington, 1985). Nevertheless, the available evidence is compelling. Keckes et al. (1966) performed a series of experiments with the sea urchin Paracentrotus lividus in which a dilute gamete suspension was placed over sea urchins in the field. The animals were never disturbed, nor were gamete suspensions released from nearer than 10 cm. Spawning induction was successful in more than 90% of the trials, but was highly sex-specific, with females spawning when touched by a sperm suspension (Keckes, 1966). Kennedy and Pearse (1975) suggested that pheromones for inducing spawning should be especially effective when gametogenesis is synchronized. Randall et al. (1964) observed epidemic spawning of Diadema antillarum in the Virgin Islands, and a pheromone that stimulates spawning of ripe conspecifics has been found in crude extracts and partially purified chromatographic fractions of D. antillarum (Iliffe and Kittredge, unpublished data; see Iliffe and Pearse, 1982). Starr et al. (1990) published one of the most convincing sets of data. They studied eastern Canadian green sea urchins Strongylocentrotus droebachiensis under controlled conditions and found that sperm suspension from conspecific effectively stimulated spawning. According to the authors, phytoplankton can induce the most receptive males to spawn, and their gametes, together with phytoplankton, subsequently promote massive spawning (Starr et al., 1990). Furthermore, gamete release may occur in response to conspecific gonadal homogenates (Keckes, 1966), and perhaps to crushed sea urchins in the field (Pennington, 1985). Cochran and
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Engelmann (1975) isolated two factors from gonadal homogenates of S. purpuratus that successfully stimulated sperm release from testis fragments: one was a yellowish-brown polypeptide similar to the radial nerve factor in asteroids, the other a small molecule similar to 1-methyladenine. Whether either of these substances acts as a spawning pheromone has not been demonstrated. McCarthy and Young (2004) tested the ability of water-borne gametes to induce aggregation and spawning in Lytechinus variegatus in the field. The inconclusive results were attributed to the fact that other key exogenous factors may not have been present (e.g., phytoplankton, moon phase, tide or darkness), though the authors admitted that water-borne gametes may not be important in inducing spawning in L. variegatus. Alternatively, responses may have been obscured by interference from KCl or a reaction to handling, or the specimens may not have been given enough time to respond. Conversely, Unger and Lott (1994) were able to induce spawning in natural aggregations of Sphaerechinus granularis granularis by using waterborne gametes. Sea urchins were allowed a short acclimation, yet still spawned in response to water-borne gametes within 20 min of the start of the experiment. Young et al. (1992) suggested that the presence of sperm stimulates female spawning in the bathyal sea urchin Stylocidaris lineata. Furthermore, according to some authorities the simultaneous heterospecific spawning of echinoderms can be attributed to sperm suspended in seawater (McEuen, 1988; Pearse et al., 1988; Thorson, 1950) (see below). 2.8.4. Simultaneous heterospecific spawning Simultaneous spawning of the holothuroids, Cucumaria miniata (major spawning) and C. piperata (two males) and the asteroid Henricia sp. (two males) was observed in situ off British Columbia (Canada) by Sewell and Levitan (1992). A similar multi-species spawning event of echinoderms at low density was observed at the same location by Pearse et al. (1988). Spawning individuals were located within 1 m of each other in only two cases, and gametes were rapidly diluted (Pearse et al., 1988). In the nearby San Juan Archipelago (north-western USA), McEuen (1988) observed an analogous event, the nearly synchronous (within 2–3 days) mass spawning of C. miniata and C. piperata, on March 24–26, 1983. These two species and a third one (C. fallax) spawned simultaneously again a few days later on April 6 (McEuen, 1988). Minchin (1992) also reported in situ spawning events in several echinoderms and other invertebrates at Lough Hyne (Ireland) between July and September of 1976–1988. He stated that spawning occurred simultaneously in individuals of various species from different phyla, up to 10 species from three phyla being involved on one occasion (Minchin, 1992). This observation suggests either that all the animals react to the same environmental signal(s) or that some species receive a cue from
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the gametes of others or from associated water-borne compounds. In a similar series of in situ surveys on the Great Barrier Reef (Australia), Babcock et al. (1992) observed several multi-specific spawning events and noted that the sea cucumber Holothuria coluber only released gametes when other species were spawning. Furthermore, several species of holothuroids (i.e., Bohadschia argus, Euapta godeffroyi, Stichopus chloronotus) often spawned on the same night but not at exactly the same time (Babcock et al., 1992). This is consistent with heterospecific cueing of gamete release. Another example of ‘‘epidemic’’ spawning was reported by Scheibling and Metaxas (2008) from field observations in the Palau archipelago in May 2004. They did not provide any details but mentioned that an asteroid (Acanthaster planci) and two holothuroids [Pearsonothuria (¼Bohadschia) graeffei and Hothuria leucospilota] released gametes while acroporid corals were undergoing a mass spawning event around the full moon. Another sea star species (Protoreaster nodosus) was spawning in the laboratory at the same time. In situ observations reported by Himmelman et al. (2008) in eastern Canada include cases of several species, for example, the sea star Asterias rubens (¼vulgaris), the brittle stars Ophiopholis aculeata and Ophiura robusta, and the sea urchin Strongylocentrotus droebachiensis, spawning on the same day but at different times.
3. Evidence from Spatial and Inter-Annual Variation An analysis of the timing and patterns of reproduction in marine invertebrates suggests that where species have broad latitudinal ranges their breeding seasons vary, generally being most limited where the environment is highly seasonal and most extended in the essentially aseasonal tropics (Giese and Kanatani, 1987; Giese and Pearse, 1974). Although detailed studies are rare, some tropical echinoderms appear to show prolonged or continuous spawning throughout the year as their proximity to the equator increases (e.g., Hopper et al., 1998). Similarly, deep-sea echinoderms from the bathyal zone exhibit seasonal reproductive cycles more often than deeper abyssal species which tend to be predominantly aperiodic (Young, 2003).
3.1. Ophiuroidea Studies on ophiuroids reviewed by Hendler (1991) showed that the duration and seasonality of the phases of gametogenesis were more variable than previously thought. Investigations conducted over several years or in more than one population have generally indicated that warm-water and deep-sea
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species may reproduce continuously. Some tropical ophiuroids have a brief spawning season but there appears to be a trend toward longer spawning periods at lower latitudes (Hendler, 1979; Mladenov, 1976; Singletary, 1980). Simultaneous sampling of nearby populations, sampling between populations from different latitudes and sampling over several years has shown differences in the reproductive periodicity of ophiuroids (Hendler, 1991). 3.1.1. Spatial variability There are several examples of variations in the population reproductive cycle in ophiuroids from different locations/latitudes. A number of studies have demonstrated that annual breeding seasons become longer and less synchronous close to the equator, where changes in seawater temperatures are minimal (Giese, 1959b; Giese and Pearse, 1974; Hendler, 1991; Kojis, 1986; Oliver et al., 1988) (Fig. 3.5). Inter-population variations were reported for Ophiocten sericeum in Greenland (Thorson, 1934), for various species on both coasts of Panama (Hendler, 1979), and for Acrocnida brachiata in France (Bourgoin and Guillou, 1990). Specifically, Hendler (1979) showed that populations of both Ophiocoma aethiops and O. alexandri living ca. 5 km apart on the Pacific coast of Panama had different peak breeding periods, and that different populations of Ophioderma cinereum, Ophioderma rubicundum, Ophiocoma echinata and Ophiocoma wendtii spawned out of rhythm on the Caribbean coast. Spawning of Ophiocoma echinata was observed in July in Jamaica (Grave, 1898) as well as in Bermuda (Mortensen, 1931), the northern extreme of its distribution range. In the more southerly location of Barbados, Mladenov (1976) reported that the breeding period of O. echinata extended from March to October. Hendler (1979) claimed that spawning in O. echinata could shift from the rainy season (fall–winter) in Panama to the warmer months of the year in northerly locations such as Jamaica. For Ophiothrix oerstedi, spawning began earlier in Jamaica than in Barbados in 1975 (Mladenov, 1979, 1983). The variable spawning periods of Amphiura chiajei summarized by Fenaux (1970) are: middle of September in Sweden [although it could be earlier since the larvae were caught in August (Mortensen, 1920b)]; end of autumn in Port Erin (Isle of Man); May– September at Naples (Bianco, 1909), spring–summer at Villefranche (Fenaux, 1970); and October in the Adriatic Sea (Vatova, 1950). The observations reported by Blake (1978) on Ophiopholis aculeata are inconsistent: populations in Newfoundland (Canada) spawned earlier than a population in the more southern locality of Maine (USA) in one year, but spawning periods coincided the following year. A more striking contrast was observed between the spawning periods of O. aculeata in the western Atlantic (August–September) and on the coast of Norway (April–May) (Blake, 1978; Olsen, 1942).
Figure 3.5
Map of the world showing the equator and the main regions and countries mentioned in the text.
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Bourgoin and Guillou (1990) indicated that subtidal populations of Acrocnida brachiata spawned earlier than intertidal populations in Douarnenez Bay (France). In Ophiothrix fragilis, spawning reportedly occurred from June to early September in Plymouth (UK), while it was restricted to August and September in Sweden (Boolootian, 1966). A study of gonadal change in O. fragilis from the Dover Strait in 1995–1996 and off Roscoff (English Channel) in 1996 (Lefebvre and Davoult, 1998) revealed little inter-annual variability for the population of the Dover Strait, but high spatial variability between populations. Higher gonad indices were recorded in June–July and a resting phase in September–February for the population in the Dover Strait. The Roscoff population exhibited lower gonad indices presumably because of lower temperature and food availability (Lefebvre and Davoult, 1998). In spite of the different gonadal growth patterns, the major spawning period in July was synchronous in females and males in both areas (Lefebvre and Davoult, 1998). In Galway Bay (Ireland), Amphiura filiformis was found to reproduce between June and September, with peak activity in August (Bowmer, 1982), whereas Buchanan (1964) reported that the same species reproduced in July off the Northumberland coast of Britain, and Fenaux (1968) noted that the larvae were present in the plankton from October through March at Villefranche (southern France), possibly indicating a later spawning period. Spawning in the Adriatic was estimated to extend from August to October (Zavodnik, 1972), and spawnings in the laboratory were observed in February, July and September (Ockelmann and Muus, 1978). The data suggest that, with the exception of the February episode reported in the laboratory (see above), the breeding period of A. filiformis in northwest European waters occurs mainly in late summer/autumn. Brooding adults were usually present throughout the year in populations of the brittle star Amphipholis squamata from high and mid-latitudes: Scotland (Fell, 1946; Jones and Smaldon, 1989), Isle of Man (Bruce et al., 1963), northeast of England ( Johnson, 1972), North America (Hendler, 1975; Rumrill and Pearse, 1985), Brazil (Boffi, 1972) and New Zealand (Fell, 1946). However, populations in Devon (UK) and Jamaica seemed to exhibit more restricted reproductive periods (Emson et al., 1989). According to Emson et al. (1989), a latitudinal effect in A. squamata should bring forward the time at which a dominant proportion of energy in an individual is allotted to lifetime reproduction; higher temperature may also mean a shortened adult life, and earlier reproduction may be an inevitable consequence on the resultant need to achieve replacement in a shorter time. Estimates of gonad indices for deep-water Ophiomusium lymani were different for northern and southern study sites (Ahlfeld, 1977).
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3.1.2. Inter-annual variability Annual shifts in ophiuroid spawning seasons have been demonstrated by multi-year investigations of several species such as Ophiopholis aculeata, Gorgonocephalus eucnemis, Ophiocoma echinata and Ophiocoma wendtii (Hendler, 1979; Muscat, 1975; Patent, 1969; Taylor, 1958). Ophionephthys limicola spawned twice in one year and only once the following year (Singletary, 1970, 1980). A similar irregularity in the breeding of Ophiura ophiura was observed by Tyler (1977). Finally, Patent (1969) found that Gorgonocephalus caryi from the San Juan Islands (Washington, USA) showed a difference of three months in the spawning period in two consecutive years, without any apparent explanation. Consistent patterns in gonad index were observed over 4 years in Ophiura ljungmani, whereas peak index values occurred at different times in different years in Ophiopholis aculeata, although the general trends were similar throughout a 3-year study (Hendler, 1991; Tyler and Gage, 1980b). In the Antarctic species Ophionotus victoriae, annual timing of reproduction was consistent among years, but considerable inter-annual variation in reproductive effort was seen (Grange et al., 2004). Variation was also observed in the gonad and gut indices of both males and females and in female fecundity, which showed no discernible change in some years, but varied more than tenfold in others.
3.2. Holothuroidea The plasticity of the reproductive habits of holothuroids in relation to geographical location has been demonstrated in several studies. In general, shallow-water holothuroids from temperate and polar latitudes have a distinct, rather short spawning period in spring or summer (Boolootian, 1966; Cameron and Fankboner, 1986; Costelloe, 1985; Hamel and Mercier, 1995a; Hamel et al., 1993; Hyman, 1955; Inaba, 1930; McEuen, 1986, 1987, 1988; McEuen and Chia, 1991; Smiley et al., 1991), whereas tropical species usually exhibit a longer reproductive period, lasting throughout the warmer months or throughout the year (Chao et al., 1995; Conand, 1981; Harriott, 1982; Mercier et al., 2000a, 2007; Ong Che and Gomez, 1985; Pearse, 1968a; Smiley et al., 1991). 3.2.1. Spatial variability Several multiple-site studies have demonstrated breeding variability in temperate holothuroid species. For instance, Cucumaria frondosa displays different spawning periods throughout its distribution range (Table 3.3), although methods for establishing the breeding period vary in precision and reliability (see Section 4.1).
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Table 3.3 Spawning periods of the sea cucumber Cucumaria frondosa throughout its distribution range Location
Spawning period
Source
St. Lawrence Estuary (QC, Canada) Bay of Fundy (NB, Canada) Bay of Fundy (NB, Canada) Passamaquoddy Bay (NB, Canada) Avalon Peninsula (NL, Canada) St. Pierre Bank (NL, Canada) Avalon Peninsula (NL, Canada) Maine (USA)
Mid-June (massive spawning) April–June
Hamel and Mercier (1995a, 1996b,c,d) Singh et al. (2001)
Several times a year
Murdoch (1984)
April–May
Lacalli (1981)
February to early May
Coady (1973)
Early spring up to June
Grant (2006) Personal observation
New England (USA)
End of March to end of April Late March to midApril April–June
North Sea (Europe)
February–March
Northern Norway Arctic
April–May July
Jordan (1972) Medeiros-Bergen et al. (1995) Runnstro¨m and Runnstro¨m (1919) Falk-Petersen (1982) Runnstro¨m and Runnstro¨m (1919)
In Apostichopus (=Stichopus) japonicus, which occurs throughout Japan and from the western shores of Korea to Vladivostok, Russia (Levin, 1982), patterns of gonad development also vary with latitudes (Choe, 1963; Tanaka, 1958). The resting gonadal phase noted at Hokkaido (Tanaka, 1958) was not observed in southern Japan (Choe, 1963). The latter investigator suggested that the differences observed in the reproduction of A. japonicus in the two regions were related to lower seawater temperatures occurring in the summer in Hokkaido ( Japan). The reproductive cycle in Stichopus mollis followed a similar latitudinal trend, a resting phase occurring in the cooler waters of southern New Zealand (Sewell, 1992), although the author pointed out that the relationship between the reproductive cycle and depth needed to be considered. The same species in north-eastern New Zealand showed variability in the reproductive cycle between years that may have resulted from the lower seawater temperatures associated with an El Nin˜o event (Sewell and Bergquist, 1990). With such important effects of sea surface temperature at a single site, it is conceivable that the large
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differences in seawater temperature, latitude, and photoperiod between study sites in the distribution range of a species may be instrumental in explaining the variation in the timing of gametogenesis (Sewell, 1992). Even at lower latitudes, where environmental variation is usually less pronounced, there is evidence of shifted or longer/shorter breeding periods at different locations. Pearse (1968b) found that populations of Holothuria atra spawned throughout the year in sites near the equator, but hypothesized that populations in the higher latitudes should have restricted spawning seasons. Published data generally confirm this hypothesis. Populations at Heron Island, Great Barrier Reef (Australia) spawn in May–June and November–January (Harriott, 1982), whereas in Fiji, the main spawning period is longer, beginning in October and ending around February (Seeto, 1994), similar to New Caledonia populations (Conand and De Ridder, 1990). Conversely, populations of H. atra from Taiwan spawn from June to September (Chao et al., 1994). Longitudinal differences in the spawning period have also been reported, for example, individuals from New Caledonia and the Great Barrier Reef spawn earlier than those from Fiji (Conand and De Ridder, 1990; Harriott, 1982). Most of the species studied by Conand (1993b) in New Caledonia spawned in December–February, which corresponds to the warm-water season. This is consistent with findings in other tropical species, including Holothuria leucospilota (Franklin, 1980), H. impatiens (Harriott, 1980), and Actinopyga echinites (Shelley, 1981). However, the latter species exhibited more precisely defined reproductive periods in New Caledonia (Conand, 1982) than it did in Papua New Guinea, closer to the equator (Shelley, 1981). The reproductive pattern of Holothuria leucospilota differs according to location. It spawns annually in April in northern Australia (Purwati and Luong-van, 2003), in June–September in southern Taiwan (Chao et al., 1995), in July–August in Japan (Maruyama, 1980), and between November and April in the Cook Islands (Drumm and Loneragan, 2005). The species spawns twice a year in Hong Kong (Ong Che, 1990), India ( Jayasree and Bhavanarayana, 1994) and Vietnam (Nguyen and Britaev, 1993), and almost every month in the Solomon Islands (Hamel et al., 2001). The reproductive cycle of Holothuria fuscogilva is similar in the Solomon Islands (Ramofafia et al., 2000), New Caledonia (Conand, 1981, 1993b) and the Maldives (Reichenbach, 1999), spawning occurring in summer. However, the onset of the breeding season is variable: August in the Solomon Islands, November in New Caledonia, and December in the Maldives. Furthermore, ripe animals are present only for 3–5 months in the Solomon Islands, but throughout the year in the Maldives, the greatest numbers being recorded between August and December (Reichenbach, 1999). Breeding periods also vary considerably over the distribution range of Holothuria scabra. Mortensen (1937) reported spawning in the Red Sea
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around June, whereas breeding in Australia was estimated to be between November–January (Harriott, 1980) and November–December (Morgan, 2000b). A biannual reproductive mode has been observed in New Caledonia (i.e., August–September and December–January) (Conand, 1993b) and Indonesia (i.e., March–July and November–January) (Tuwo, 1999). In India H. scabra breeds between July and August (sometimes in October– November) (Krishnaswamy and Krishnan, 1967), between June and October in the Philippines (Ong Che and Gomez, 1985), and more or less continuously in the Solomon Islands with peak activity from September to December (Mercier et al., 2000a; Ramofafia et al., 2003). Holothuria scabra apparently exhibits a biannual cycle in India (Krishnaswamy and Krishnan, 1967), Australia (Harriott, 1980), Papua New Guinea (Shelley, 1981) and in the Philippines (Ong Che and Gomez, 1985), with a dominant peak occurring in the warm season and a weaker and more variable secondary peak (Conand, 1993b). The annual pattern of winter spawning in Holothuria whitmaei appears to be similar in Australian and New Caledonian populations (Conand, 1981, 1993b; Shiell and Uthicke, 2006), which although separated longitudinally lie within a relative narrow latitudinal range. Comparable cycles of breeding activity between populations at similar latitudes (i.e., the Great Barrier Reef in Australia and La Re´union Island in the western Indian Ocean) have also been reported in Stichopus chloronotus (Conand et al., 2002). The timing of spawning may therefore be under the control of broadly defined seasonal changes in abiotic factors (i.e., day length, seawater temperature), which could be expected to be latitudinally congruent (Conand et al., 2002). This is in contrast to the more widely documented cases outlined earlier of differing reproductive strategies between conspecific aspidochirotes of different latitudes (Chao et al., 1995; Hamel and Mercier, 1996a; Ramofafia et al., 2003; Sewell, 1992), and supports the hypothesis that abiotic factors are important cues entraining gonad development and spawning in tropical invertebrates (Shiell and Uthicke, 2006). Populations of Isostichopus fuscus from the Gulf of California (Mexico) do not reproduce in synchrony with those from Ecuador (near the equator), the former breeding between July and September when the sea surface temperature reaches 27 C (Herrero-Pe´rezrul et al., 1999), and the latter monthly according to the lunar cycle in a region where seawater temperatures are more or less constant (Mercier et al., 2007). The study in Mexico was based on histology of the gonads, whereas that in Ecuador employed direct monitoring of gamete release, so the difference in conclusions may be attributable to a methodological discrepancy. Nevertheless, it is conceivable that I. fuscus would have a temperature-restricted breeding season at higher latitudes. Investigations of gonad indices and histological sections indicated that spawning of Actinopyga mauritiana occurs between October and January in
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the Solomon Islands (Ramofafia et al., 2001), between December and January in New Caledonia (Conand, 1993b) and in summer in Guam (Hopper et al., 1998), although some mature individuals are found throughout the year. A similar correlation of reproductive periodicity with seawater temperature has been recorded in A. mauritiana from Guam (Hopper et al., 1998) and New Caledonia (Conand, 1989, 1993b), in spite of greater seasonal fluctuations in temperature and photoperiod at the latter location. If temperature and/or photoperiod mediate reproductive timing, they appear to work in an absolute (threshold) fashion rather than in a relative one (Hopper et al., 1998). According to this hypothesis, proximity to the equator should not result in prolonged periods of breeding activity at the locations studied, that is, longer periods of higher seawater temperature apparently do not influence the length of the breeding season (Hopper et al., 1998). 3.2.2. Inter-annual variability In Thyone briareus at Woods Hole (eastern USA) gamete release was observed in the laboratory mainly in June (Colwin, 1948). Similarly, Pearse (1909) reported spawning from 22 June to 5 July, Ohshima (1925) from 21 to 24 June, and Just (1929) throughout June in each of several years. The only report to the contrary is that of Mead (1898), who found that most males and females were ripe on 24 April in 1898, although Just (1929) later stated that oocytes obtained in April and May were unripe. The work of Hopper et al. (1998) on the reproductive biology of the aspidochirote Actinopyga mauritiana revealed that gonad indices reached a peak in spring and summer months, with a slight difference in reproductive peaks between 1988 and 1989, associated with a La Nin˜a event (Hopper et al., 1998). Sewell and Bergquist (1990) similarly found variation in the reproductive cycles of Stichopus mollis in New Zealand, possibly linked to lower temperatures caused by an El Nin˜o event.
3.3. Asteroidea The reproductive cycle of Asterias rubens (¼vulgaris) has been studied in various locations by numerous investigators. Nichols and Barker (1984a) reported maximum gonad development in April and May in Torbay (English Channel, UK), Guillou (1980) in May in Douarnenez Bay (western Brittany, France), Cognetti and Delavault (1962) in June–July at Roscoff (northern Brittany, France), and Jangoux and Vloebergh (1973) in May at Knokke (Belgium). According to G. F. M. Smith (1940), spawning in eastern Canada took place in May–June in the Gulf of St. Lawrence and in July in New Brunswick, but Himmelman et al. (2008) observed spawning in situ in early July in the Gulf of St. Lawrence. Costello and Henley (1971) recorded spawning of A. rubens in May–June in Woods Hole (USA),
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whereas Boolootian (1966) had previously reported that it occurred between March and May, depending on location and depth. Nichols and Barker (1984a) suggested that the time of maximum gametogenic development in shallow-water European populations of Asterias rubens is delayed in more northerly locations. Thus, spawning occurs principally in June in the Firth of Clyde, Scotland (Gemmill, 1914) and the North Sea (Kowalski, 1955), in July in the Baltic (Kowalski, 1955) and the White Sea (Mileikovsky, 1968), and in August in the southern Norwegian Sea and Barents Sea (Mileikovsky, 1968). However, in the deeper areas of the Looe-Eddystone Grounds (UK), spawning may commence in January– February (Nichols and Barker, 1984a). In a study of sea stars Henricia lisa living at bathyal depths off eastern Canada, marked differences were found between individuals from ca. 1300 and ca. 600 m (Mercier and Hamel, 2008). The former had a male biased sex ratio and an aperiodic reproductive cycle, whereas the latter displayed an equal sex ratio and a biannual breeding pattern. Furthermore, the maximum size was larger and female fecundity roughly five times higher in shallower than in deeper populations (Mercier and Hamel, 2008). This depth-related shift in reproductive strategies suggests adaptations to local food availability and environmental conditions.
3.4. Echinoidea Depth may be an important factor in the reproduction of echinoids. Leahy et al. (1981) observed that individuals of Strongylocentrotus purpuratus living in shallow subtidal areas in California (USA) exhibited a seasonal peak in the oogenetic cycle, whereas those from deeper locations (16–23 m) did not. Similarly, shallow-water populations (8–10 m) of Echinus esculentus in the English Channel (UK) showed higher gonad indices and more distinct spawning peaks than slightly deeper populations (20–22 m) (Nichols et al., 1985). However, this is probably the result of differences in nutritional quality rather than depth itself (Nichols et al., 1985). Conversely, Ferrand et al. (1988) observed that the annual gametogenic cycle of Brissopsis lyrifera was similar in individuals from 60 to 930 m in the Mediterranean Sea. Different habitats may also have an influence on reproduction. For instance, populations of Psammechinus miliaris were sampled over nearly 2 years at two replicate sites in littoral and subtidal habitats on the west coast of Scotland, where they exhibited defined annual cycles of gametogenesis with a single spawning period (Kelly, 2000). The cycle was similar to that described for sympatric species such as Echinus esculentus and Paracentrotus lividus (Byrne, 1990; Comely and Ansell, 1989), maximal gonad indices occurring prior to the onset of spawning in June–July. However, the gonad index of P. miliaris differed between habitat types, replicate sites within a habitat type, and years (Kelly, 2000). Different contrasts between
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littoral and subtidal populations would have been shown depending on the sub-sites compared, emphasizing the possible masking of trends due to intra-site variability (see Section 1.5 in Chapter 4). The other spawning periods reported for P. miliaris are June–August in the Clyde Sea area (Elmhirst, 1922), June–October near Bergen, Norway (Lindahl and Runnstro¨m, 1929), June–October and May–October in western Norway and Denmark ( Jensen, 1969), and July–August on the west coast of Scotland (Comely, 1979). Variations in the reproductive cycle of Lytechinus variegatus among populations have been attributed to differences in environmental conditions. The estimated peak spawning period in a population off Miami (Florida, USA) varies by as much as 4 months (Moore and Lopez, 1972), whereas the range of gonad volume increase varied considerably from year to year in the Gulf of Mexico (Beddingfield and McClintock, 2000). Significant differences have been observed even among populations that are in close proximity (Beddingfield and McClintock, 2000), possibly as a result of variation in food availability or abiotic factors (Watts et al., 2007). Furthermore, not all populations exhibit marked or synchronized reproductive cycles (Cameron, 1986; Junqueira, 1998; Lessios, 1985). In New Zealand, patterns of reproduction varied significantly within populations and from year to year in three sympatric species of Pseudechinus (McClary and Barker, 1998). The authors suggested that P. albocinctus exhibited an annual cycle in the first sampling year and a biannual cycle in the second year.
Table 3.4 Spawning periods of the sea urchin Evechinus chloroticus in New Zealand. Adapted from Barker (2007) Location
Spawning period
Source
Noises Island Rangitoto Island Crusoe Island Reef Bay Perano Heads Titi Bay Dieffenbach Point Kaiteriteri Anchor Island Deep Cove Espinosa Point Causet Cove
November–January November–January January–February December–February November–January November–March January–April December–April December–February November–April January–April January–April
Walker (1982b) Walker (1982b) Walker (1982b) McShane et al. (1996) Brewin et al. (2000) Brewin et al. (2000) Brewin et al. (2000) Dix (1970) McShane et al. (1996) Lamare et al. (2002) Lamare et al. (2002) Lamare et al. (2002)
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Male
Female
Causet cove
100 80 60 40 20 0 Espinosa point
Frequency (%)
100 80 60 40 20 0 Deep cove 100 80 60 40
1993
1994
Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
0
Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
20
1993
Recovery
Premature
Partially spawned
Growing
Mature
Spent
1994
Figure 3.6 Evechinus chloroticus (Echinoidea). Monthly changes in the percentage of males and females in each of the six gametogenic stages from various locations in Doubtful Sound, Fiordland (New Zealand), between 27 January 1993 and 28 February 1994. Reprinted with permission from Lamare et al. (2002).
Marked spatial and temporal disparities in reproductive potential (Table 3.4; Fig. 3.6) have been attributed at least in part to food quality and nutritional stress in another species from New Zealand, Evechinus chloroticus (Brewin et al., 2000; Lamare et al., 2002; Wing et al., 2001). On the other hand, Barker (2007) reported that E. chloroticus from New Zealand
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showed no clear latitudinal trend in the breeding season, despite the wide latitudinal range (36–45 S) and the differences in seasonal temperatures (13–22 C in the north and 8–15 C in the south). This is in contrast to data from the sea urchin species previously discussed. In the sea urchin Diadema setosum, which is widely distributed in the Indo-Pacific, reproductive activity in temperate zones is limited to a certain period of the year. According to Yoshida (1956), Japanese populations spawn once a year during summer, but not necessarily at the same time: those from Misaki Bay to the south spawn at the full moon, whereas those from Seto, also in the south, spawn during the semi-lunar period (Kobayashi and Nakamura, 1967). In the tropical latitudes, the species has been reported to spawn during summer when sea temperatures are >25 C (Pearse, 1970; Stephenson, 1934). An extensive compilation of data from many sources showed that populations of D. setosum usually spawn throughout the year at latitude 10–15 , but further north or south of the equator reproductive activity is more restricted to the warmer months (Pearse, 1968a). Investigations confirmed that spawning occurred throughout the year in the tropics, where sea temperatures were nearly always >25 C (Tuason and Gomez, 1979; Yonge, 1924). Hence, reproduction of this Table 3.5 Spawning periods of the sea urchin Echinometra mathaei. Adapted from McClanahan and Muthiga (2007) Location
Spawning period
Source
Honshu ( Japan) Minatogawa (Okinawa Island, Japan) Sakurajima (Kagoshima Bay, Japan) Shirahama (Kii Pen, Japan)
January–September May–December
Seto ( Japan) Sesoko Island ( Japan)
July–August September– October ‘‘Continuous’’ July–September ‘‘Continuous’’ November–March
January–March
Kobayashi (1969) Fujisawa and Shigei (1990) Fujisawa and Shigei (1990) Fujisawa and Shigei (1990) Onoda (1936) Arakaki and Uehara (1991) Kelso (1971) Pearse (1969b) Pearse (1969b) Muthiga (1996); Muthiga and Jaccarini (2005) Drummond (1995)
‘‘Continuous’’
Pearse and Phillips (1968)
Hawaii (USA) Gulf of Suez NW Red Sea Diani, Kanamai and Vipingo (Kenya) Eastern coast of South Africa Rottnest Island (Australia)
June–September July–August
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species does not show a constant pattern but varies according to geographical locality, sea temperature, lunar cycle and other environmental conditions. Echinometra mathei is another species that displays considerable latitudinal variability in the reproductive cycle (Table 3.5). In the Gulf of Suez and of Japan, populations are said to spawn in summer (Onoda, 1936; Pearse, 1969b), whereas in most of the remaining locations where the species occurs reproduction is continuous and asynchronous (Pearse, 1968a, 1969b; Pearse and Phillips, 1968). Pearse and Phillips (1968) suggested that sea temperatures in winter at Rottnest Island (Australia) were probably high enough (18–22 C) to maintain the continuous reproduction observed in this population. However, E. mathaei on the Kenyan coast (4 S) exhibits an annual cycle with gametogenesis initiated in July and spawning occurring in February–March (Muthiga, 1996). Hence, the seasonal spawning pattern in Kenya appears to be correlated with the maximum seawater temperature (ca. 25 C), which is influenced by the monsoon (Muthiga and Jaccarini, 2005). This contradiction suggests that temperature may not be the key factor controlling spawning in E. mathaei. Variability in the reproductive cycle was also reported in Echinometra lucunter, similar spawning periods occurring throughout different habitats in southern Florida (McPherson, 1969), and irregular spawning patterns shown in Panama Bay (Lessios, 1981, 1985). Specifically, spawning both in late summer and early fall was observed in Florida (McPherson, 1969), whereas spawning took place in late spring and early summer in two populations from Brazil (Ventura et al., 2003). Despite the reproductive asynchrony observed in the two Brazilian populations studied by Ventura et al. (2003), histological analysis of gonadal tissues in E. lucunter suggested that individuals from a coral reef had longer spawning periods than those from a rocky-shore. Similar variations in gonad development, with greater relative growth of gonads inshore than offshore, were reported in Florida populations of E. lucunter by McPherson (1969). For Centrostephanus rodgersii in New South Wales (Australia), northern populations have a short 1 month breeding period (Byrne et al., 1998; O’Connor et al., 1978), whereas spawning in the middle and southern parts of the range extends for several months (Andrew and Byrne, 2007). In a comprehensive review, Vasquez (2007) highlighted the latitudinally variable reproduction of Loxechinus albus from Chile, indicating that spawning occurred in June around 22–24 S (Gutie´rrez and Otsu, 1975; Zegers et al., 1983), between June and August close to 30 S (Zamora and Stotz, 1992), between August and November at 32–33 S (Buckle et al., 1978; Guisado and Castilla, 1987), and between October and December at ca. 40 S (Guisado, 1985). Spawning has been reported between November and December in Chiloe´ and the Guaitecas Islands (42–45 S) (Bay-Schmith et al., 1981). Populations of L. albus from Punta Arenas (56 S) do not follow the trend, their main spawning period occurring between September and
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October (Bay-Schmith et al., 1981). According to Zamora and Stotz (1992), the Punta Arenas populations are not affected by the Humboldt Current, unlike those between 22 and 45 S. However, the coast south of 48 S is influenced by the very different characteristics of the Cape Horn Current (Vasquez, 2007). Another disparity is that ripe individuals are present all year around in the Magallanes Region of southern Chile, but simultaneous spawning of female and males is limited to August–September at Dawson Island (53 S) and July–September in Cockburn Channel (53 S), suggesting that the Magallanes Region is an exception to the latitudinal pattern reported for most of the Chilean coast. Oyarzu´n et al. (1999) suggested that this striking large-scale variability results from the simultaneous occurrence of low temperatures and short days during late winter and early spring. Populations of L. albus between 22 and 45 S differ from those above 56 S in having a second gamete production phase during summer–fall (Bay-Schmith, 1982), which may be resorbed to serve as a nutrient storage for the autumn–winter fasting that precedes spawning according to Buckle et al. (1978). The absence of echinopluteus larvae in the plankton of southern Chile supports this explanation (Vasquez, 2007), as does the large number of nutritive phagocytes observed in summer–fall (Zamora and Stotz, 1992). The latter authors compared breeding seasons between high and low latitudes with similar seasonal variations in temperature and proposed that spawnings coincide with temperatures of 14 C (20 S) and 11 C (56 S). The reproductive cycle of Paracentrotus lividus varies widely across its distribution range (Table 3.6). While the annual cycle observed is generally similar throughout Spain, spawning episodes are restricted to spring or early summer in northern regions (Lozano et al., 1995), whereas Sa´nchez-Espan˜a et al. (2004) observed mature gonads during almost all periods studied in southern areas, with a peak in spring–summer. Furthermore, both P. lividus in Europe (Runnstro¨m, 1927) and Arbacia punctulata in eastern North America (Harvey, 1956) have shorter spawning periods in the northern part of their distribution than in the southern part. Runnstro¨m (1927) reported that breeding in Strongylocentrotus droebachiensis occurred in January and February in Bergen, while it was postponed until summer in the Arctic (Thorson, 1946). See Table 3.2 for a comparison of various spawning periods. Breeding of the red sea urchin Strongylocentrotus franciscanus was suggested to occur from February to July at Pacific Grove, California (USA) (35 N) (Newman, 1923), from May to September in southern (Canada) (49 N), and from April to October in the Queen Charlotte Islands (52 N) (Bernard, 1977). An earlier study established the approximate spawning period to be March–May in California (Bennett and Giese, 1955). The spawning season of Strongylocentrotus intermedius, off the eastern Pacific coast and off the Okhotsk Sea coast in Japan, was determined to extend from June to October (Tomita and Tada, 1988; Tomita et al., 1984,
Table 3.6 Spawning of the sea urchin Paracentrotus lividus throughout its distribution range according to decrease in GI. Adapted from Guettaf et al. (2000) and Boudouresque and Verlaque (2007) Location
Spawning period
Source
Bantry Bay (Ireland) West Ireland Northern Brittany (France) Northern Brittany (France) Northern Brittany (France) Western Brittany (France) Marseilles (southern France) Villefranche (southern France) Ligurian Sea (southern France) Corsica (France) West Corsica (France) West Corsica (France) Barcelona (Spain) Northeast coast of Spain Strait of Gibraltar (southern Spain) Mediterranean (Adriatic Sea) SW Mediterranean (Algeria) SW Mediterranean (Algeria) SW Mediterranean (Algeria) Three sites in SW Mediterranean (Algeria)
January–March and August–September May/June–August/September March–April to July–August March–September June–August and September Late spring–early summer June and September–November June and late summer to November April–May and September–October March–April March–June and August–October March–June and August–October April/May–July May–July Spring–summer March–autumn March and August–September March–April and October–November April and October–December April–May and August–September April–June and October–December February–March March and July–August March–June
Crapp and Willis (1975) Byrne (1990) Neefs (2000) Allain (1975) Cherbonnier (1951) Spirlet et al. (1998) Re´gis (1979) Fenaux (1968) Pedrotti (1993) Leoni et al. (2003) Verlaque (1996) Fernandez (1996) Guettaf (1997) Lozano et al. (1995) Sa´nchez-Espan˜a et al. (2004) Zavodnik (1987) Semaud and Kada (1987) Sadoud (1988) Chitini and Sellal (1994) Guettaf et al. (2000)
Algiers (Algeria) Rabat/Casablanca (Morocco)
Semroud (1993) Bayed et al. (2005)
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1986). Elsewhere in Japan, off the coast of the eastern Tsugaru Strait, the Pacific Ocean, and Funka Bay, spawning reportedly occurred in April–May and August–November (Agatsuma and Momma, 1988; Agatsuma et al., 1989, 1994; Kawamura et al., 1983). The spawning pattern of S. intermedius around Japan can therefore be classified into three types, according to location: (1) a Sea of Japan type of intensive spawning in autumn, (2) a Funka Bay type of spawning in spring and autumn, and (3) an Okhotsk Sea and Pacific Ocean type of spawning from spring to autumn (Agatsuma, 2001). However, according to Fuji (1960), the spawning period in the eastern Tsugaru Strait and in Funka Bay is September–November, the same as in the Sea of Japan. The reproductive cycle of individuals of Strongylocentrotus intermedius remained unchanged after they were transplanted from the Sea of Japan to the Pacific coastal waters of eastern Hokkaido, spawning occurring in autumn (Tomita et al., 1986). Laboratory-reared individuals originating in the Sea of Japan and transplanted to the Pacific and eastern Tsugaru Strait waters also retained the original reproductive cycle (Agatsuma and Momma, 1988; Agatsuma et al., 1994), as did sea urchins produced from adults native to the Pacific coast and transplanted to the Sea of Japan (Agatsuma et al., 1994). The spawning season of Tripneustes gratilla varies significantly according to location (Lawrence and Agatsuma, 2007). It has been reported to occur in spring and fall on the Great Barrier Reef, Australia (Stephenson, 1934), in winter in the northern Red Sea (Pearse, 1974) and the Gulf of Aqaba (Kidron et al., 1972), in summer off Japan (Kobayashi, 1969; Onoda, 1936), and in autumn in the Philippines and Taiwan (Chen and Chang, 1981; Tuason and Gomez, 1979). Nunes and Jangoux (2004) recorded spawning between April and June in the spatangoid Echinocardium cordatum in northern France. Moore (1936) also noted that this species ripened at the end of spring in the English Channel (UK), but other authors have obtained different data from other locations. Thus, Hyman (1955) reported spawning in May–August along the Scottish coast, August–September in Sweden, and October–April in the Mediterranean Sea, whereas the same species spawns in June–July in the Sea of Japan (Yakovlev, 1987). In contrast, Nakamura (2001) claimed that spawning occurred between February and April in Japan. Published estimates of spawning in E. cordatum tend to show that the breeding season shifts from the end of the winter in lower latitudes (e.g., Mediterranean Sea) to the end of the summer in higher latitudes (e.g., Scandinavia). Seasonal variations in gonad index and gonad maturation stage revealed that spawning of Hemicentrotus pulcherrimus in Oshoro Bay ( Japan) took place from March to May, peaking in April (Agatsuma and Nakata, 2004). The pattern was slightly different in southern Honshu (November–April) and roughly similar at Matsumae in southern Hokkaido (April–June) (Agatsuma, 2007). Agatsuma (2007) concluded from this variable pattern
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that seawater temperature played an important role in gonad maturation of H. pulcherrimus. In contrast to the above examples, widely separated populations of the sea urchin Strongylocentrotus purpuratus along the western coast of North America from as far north as Coos Bay, USA (43 N) and as far south as Papalote Bay, Mexico (32 N) are relatively homogenous in terms of reproductive development and spawning. Gametogenesis is initiated in late summer at all locations, and spawning is fairly synchronous throughout the range (Bennett and Giese, 1955; Boolootian, 1963; Boolootian and Giese, 1959), although minor inter-locality and inter-annual changes have been reported (Bennett and Giese, 1955; Pearse, 1981). In the Antarctic sea urchin Sterechinus neumareyi studied at three sites over 2 years, major inter-population variations were noticed in the gonad index cycles but spawning appeared synchronous, based on competence to spawn (via KCl injections) and observation of natural gamete release in the field (Brockington et al., 2007). Furthermore, large inter-annual differences were observed, suggesting that the species may exhibit an annual reproductive periodicity overlaid by much longer cycles that yield more substantial spawning events over several years (Brockington et al., 2007).
4. Evidence from Artificial Induction The experimental testing of external cues (e.g., temperature, phytoplankton, etc.) as inducers of gamete release provides interesting insights into the mediation of spawning in echinoderms in the field. Techniques that make use of environmental conditions have been especially common in holothuroids due to the absence of a chemical that can reliably act on the gonads. Such compounds (e.g., potassium chloride, 1-methyladenine, etc.) are discussed in the chapter dealing with endogenous mediation (Section 5).
4.1. Holothuroidea In India, Holothuria scabra collected during the breeding season spawned without any external stimulus other than the stress of collection (James, 1994b, 1996). In fact, apart from spontaneous spawning following the stress of capture recorded in different species (Conand, 1993b; Hamel et al., 2001; Reichenbach, 1999), thermal shock remains the most common method for inducing spawning in holothuroids (Dolmatov and Yushin, 1993; Hamel et al., 2001; James et al., 1994a; Smiley et al., 1991; Yanagisawa, 1998). However, these methods give very inconsistent results, which vary with the protocol used, with the species studied and even among batches of individuals collected.
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Thermal shock is the most widespread technique for inducing Holothuria scabra to spawn (Battaglene, 1999a; Battaglene et al., 2002; Hamel et al., 2001; James, 1996; James et al., 1988, 1994a; Morgan, 2000a). Typically, mature individuals are transferred to water ca. 4 or 5 C warmer than that in the original holding tank, and maintained there for several hours if necessary. Morgan (1999) triggered spawning using temperature increases of 3–5 C with maximum success during the new and full moons. Battaglene et al. found that the easiest time to induce spawning was September in the Solomon Islands, males being more responsive than females, although results varied according to the thermal stimulation protocol, gonad maturity and lunar periodicity (Battaglene, 1999a; Battaglene et al., 2002). Thermally shocked females can be induced to spawn even in the absence of sperm, but males usually spawned first, suggesting that thermal stress might trigger male spawning and that females are stimulated by the presence of sperm in the water column ( James et al., 1994b). Spawning was triggered in mature females of Holothuria scabra and H. fuscogilva by adding a suspension of the dried alga Schizochytrium sp. (Battaglene, 1999a; Battaglene et al., 2002; Ramofafia et al., 2000). The use of a powerful jet of water on drying individuals was also successful, whereas stripping gonads was only partially effective (Hamel et al., 2001). Mercier and Hamel (unpublished data) and Battaglene (unpublished data) failed to achieve fertilization with gametes collected by stripping gonads. Final maturation (oocyte competency) invariably took place during spawning (Hamel and Mercier, 2007; Ong Che and Gomez, 1985). Hamel and Mercier (1996c) induced gamete release in Cucumaria frondosa by manipulating environmental factors. Females spawned when exposed to a severe change in light regime combined with increasing temperature. This procedure stimulated spawning in up to 55% of individuals, and no other technique was successful. Ohshima (1925) was able to induce individuals of Thyone briareus to release gametes during the day by placing them in dim light. Once returned to bright light, they ceased spawning but resumed if replaced in subdued light. Finally, Ohshima (1925) found that females did not spawn spontaneously, but released gametes only after the emission of sperm by nearby males in the same container. A number of accidental spawnings have been observed after individuals were submitted to stressful conditions, including collection and transport or maintenance in aquarium conditions. Uthicke (1994) noted that Stichopus chloronotus collected at Lizard Island (Australia) spawned in the holding tanks during the period when naturally occurring broadcast spawning was observed in the field, and at the same time of the day. Other examples from various locations have been reported: Reichenbach and Holloway (1995) summarized many observations from the Maldives, where Holothuria nobilis and Thelenota ananas spawned when disturbed. Bell (1994) also
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described spawning of Holothuria atra from the Solomon Islands in holding tanks. Mohan (1999) described several cases of spawning of the sea cucumber H. atra in southern India under laboratory conditions. In many cases, these spawnings resulted in good fertilization success and larval development, suggesting that the animals had been ripe and ready to spawn. Mature holothuroid oocytes arrest at the meiotic prophase-I stage (Maruyama, 1985) and undergo ovulation, germinal vesicle breakdown and further maturation during spawning, at which stage they can be fertilized. They are therefore not easy to fertilize prior to their natural release (Smiley, 1988a,b, 1990). Most of the known physical, chemical or biological treatments used to induce spawning or to activate the final maturation of oocytes in other marine invertebrates act at the cellular level (Smiley et al., 1991); and their effects are species-specific (Maruyama, 1980). They are therefore ineffective or only partially effective in holothuroids. No reliable maturation-inducing substances have been extracted from holothuroids, unlike sea urchins and sea stars. Nonetheless, Maruyama (1980) used dithiothreitol (DTT), 2,3-dimercapt-1-propanol (BAL) and L-cysteine to induce ovulation in surgically collected oocytes of Holothuria leucospilota, H. pardalis and Actinopyga echinites. Furthermore, Ikegami et al. (1976) induced spawning in males and females of Leptosynapta inhaerens with 1-methyladenine (see Section 5 for further details).
4.2. Echinoidea Injection of potassium chloride (KCl) is a very simple and reliable way to induce spawning in sea urchins, and has been used extensively in both field and laboratory experiments on gamete dispersal and fertilization rates (Appendix A10). In contrast, natural spawning inducers have received little attention. Experimental trials conducted with Strongylocentrotus droebachiensis showed that spawning in this species is triggered by phytoplankton (Himmelman, 1975), even at natural spring bloom concentrations (Starr et al., 1990). This work led to the partial characterization of a spawn-inducing substance extracted from the diatom Phaeodactylum tricornutum (Starr et al., 1992). Sperm suspensions in seawater can also trigger the release of gametes in S. droebachiensis (Starr et al., 1990) (see Section 2.4 for further details).
5. Endogenous Mediation 5.1. Crinoidea Bickell et al. (1980) suggested that 1-methyladenine (see details on this substance in the discussion on asteroids below) causes contractions of the gonadal musculature in crinoids. In some species, spawning may also
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involve localized histolysis of gonadal tissues and nearby parts of the body wall and epidermis. Goyette (1967) discussed possible hormonal and neurosecretory factors that might control spawning in crinoids. Although lacking quantitative data, he proposed that cells in the aboral nervous system (especially in pinnular nerves and their branches) might suddenly release neuro-secretions to induce spawning.
5.2. Ophiuroidea Reproduction in ophiuroids is believed to be under some sort of neurosecretory control, though neuro-secretory products have yet to be isolated and characterized in this class (Hendler, 1991). Nevertheless, 1-methyladenine and extracts from the radial nerve of asteroids can induce contraction of the gonadal wall and spawning in some brittle stars (Buckland-Nicks et al., 1984; Strathmann and Rumrill, 1987). When asteroids were induced to spawn by a gonad-stimulating substance (GSS), Kanatani and Ohguri (1966) observed a time lag between stimulus and effect that was similar in duration to the delay in spawning induced by temperature shock in Amphipholis kochii. Yamashita (1985) concluded from this observation that the temperature shock induced the radial nerve to release the GSS, but he correctly pointed out that it remained uncertain whether oocyte maturation and spawning in ophiuroids were controlled by the neuro-secretory system, as in the asteroids, even though neuro-secretory cells are present in the radial nerve of Ophiopholis aculeata (Fontaine, 1962). While steroidal compounds or their precursors are known from a few species of ophiuroids (Colombo and Belvedere, 1976; Goad et al., 1972; Gupta and Scheuer, 1968), their role has not been studied to date.
5.3. Holothuroidea Various compounds have been proposed to induce maturation in holothuroids, in a similar manner as 1-methyladenine (1-MA) in asteroids (see 5.4 below): Kishimoto and Kanatani (1980) successfully induced final oocyte maturation in Parastichopus (¼Stichopus) californicus with disulfide-reducing agents such as dithiothreitol (DTT) and 2,3-dimercapto-1-propanol (BAL). DTT, BAL and L-cysteine also induced ovulation in surgically collected oocytes of Holothuria leucospilota, H. pardalis (Maruyama, 1980), H. scabra (Rasolofonirina et al., 2009) and Actinopyga echinites (Chen et al., 1991), although subsequent rates of fertilization of the oocytes were generally low and development of the embryos abnormal. A natural complex called ‘‘nirina’’ has recently been found to be highly effective (up to 95%) in inducing maturation of extracted oocytes in several aspidochirotid species from the Indian Ocean and the Mediterranean Sea
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(Rasolofonirina et al., 2009), and fertilization rates of >90% were usually obtained. However, ‘‘nirina’’ was ineffective on the gonadal tubules or via injection into the coelomic cavity (Rasolofonirina et al., 2009). Kato et al. (2009) purified a gonadotropic neural peptide (NGIWYamide) from the buccal ring nerve of Apostichopus japonicus which induced gamete release after injection into mature males and females. A synthetic derivative (NGLWYamide) was 10 times more potent than the natural NGIWYamide. The gametes obtained through this induced spawning were successfully fertilized, developed normally and metamorphosed into young holothuroids. Unlike ‘‘nirina’’, the peptides were ineffective in directly inducing maturation and germinal vesicle breakdown in follicle-enclosed or follicle-free oocytes, requiring the ovarian wall to induce oocyte maturation (Kato et al., 2009), much like the radial nerve factor (RNF) in the asteroid Pisaster ochraceus (Schuetz, 2000). The data suggest that ‘‘nirina’’ and the neural peptide act at different levels of the spawning cascade. Stevens (1970) reported that 1-MA (which induces oocyte maturation in asteroids) failed to induce spawning of Parastichopus (¼Stichopus) californicus. In the sea cucumber Leptosynapta inhaerens, immature oocytes connected by a thick follicular envelope inside the ovotesticular fragments neither spawned nor were induced to mature by 1-MA, whereas the ovotestis shed sperm immediately upon treatment (Ikegami et al., 1976). Thus, during gamete shedding in Leptosynapta, 1-MA seems to act on the gonadal nerve cells or at the neuromuscular junctions. Using extracted oocytes, Smiley (1984, 1988a) and Maruyama (1985, 1986) determined that an RNF acted through the follicle cells to produce a maturation-inducing substance (MIS) leading to germinal vesicle breakdown (GVBD) in several holothuroids: Parastichopus (¼Stichopus) californicus, Holothuria leucospilota, H. moebi, H. pardalis, H. pervicax and Apostichopus (=Stichopus) japonicus. Maruyama (1985) noted that follicle-free oocytes in H. leucospilota did not undergo GVBD when exposed to tissue extracts containing RNF. Oocytes of P. californicus exhibited higher levels of GVBD when isolated ovarian tubules were incubated in an aqueous extract containing RNF from asteroids (Maruyama, 1986; Strathmann and Sato, 1969) or conspecific holothuroids (Smiley, 1988a). Furthermore, according to Maruyama (1985), the maturation-inducing properties of RNF were neither species-specific nor sex-specific, and were only effective on oocytes with intact follicle cells, suggesting that a secondary factor (MIS) produced by the follicle cells was necessary for oocyte maturation to proceed. This MIS would be the equivalent of 1-MA in sea stars. Hufty and Schroeder (1974) demonstrated that the ovaries of Parastichopus (¼Stichopus) californicus produced a substance similar to 1-MA when incubated in vitro with an extract containing RNF from the sea star Patiria miniata. This holothuroid MIS induced GVBD in oocytes of both the sea star and the sea cucumber, although the reaction of the latter was less
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marked and less consistent. The investigators stated that the endocrine significance of the holothuroid MIS remained unclear. Indeed, it has been shown that sea star RNF can induce maturation of follicle cell-free oocytes of sea cucumbers (Maruyama, 1986), although this response may be due to the contamination of RNF extracts by a true MIS or other stimulating agent(s) (Smiley et al., 1991). Similarities between 1-MA and the holothuroid MIS were supported by preliminary characterization (Hufty and Schroeder, 1974) and only one report of spawning induction by 1-MA in the sea cucumber Leptosynapta inhaerens (Ikegami, 1976). Most investigators failed to induce maturation in holothuroid oocytes with 1-MA (Hufty and Schroeder, 1974; Kishimoto et al., 1982; Maruyama, 1980, 1986; Smiley, 1988a). Smiley (1988a) further purified the MIS in P. californicus, found it to be clearly different from 1-MA, and suggested that it might be a 2,8disubstituted adenine. The pathway through which RNF acts on the gonad is unclear, although the anatomy of holothuroids and asteroids suggests that the radial haemal sinus is a possible mode of transport (Smiley et al., 1991). While the discovery of RNF in the radial haemal sinus of a sea star by Caine and Burke (1985) lent some credibility to the hypothesis, some reservations have been expressed concerning the ability of these minute passages to translocate RNF efficiently (Smiley et al., 1991). Alternatively, transport through the peritoneal nerve cells has been proposed (Smiley and Cloney, 1985; Smiley et al., 1991), but the issue of RNF action has yet to be resolved in echinoderms. Because GVBD induction by RNF reportedly takes 2–4 h in holothuroids (Maruyama, 1985, 1986; Smiley, 1988a), Smiley et al. (1991) suggested that a proximal signal would have to be perceived several hours before gamete release. However, shorter delays have been reported for hormonally activated ovulation, GVBD and maturation to occur in holothuroids. For instance, the oocytes of Holothuria leucospilota consistently required ca. 85 min to achieve competency, from the natural onset of ovulation to the final broadcast (Hamel and Mercier, 2007). Similarly, a recently purified neural peptide induced spawning within 70–90 min in females of Apostichopus japonicus (Kato et al., 2009). Furthermore, stress of capture and the induction methods used in aquaculture resulted in the release of fully fertilizable oocytes in ca. 60 min by individuals that had not previously shown any signs of spawning activity (Hamel and Mercier, 2004; Hamel et al., 2001; Mercier and Hamel, 2002; Reichenbach, 1999). Smiley et al. (1991) proposed that a concerted contraction of actin microfilaments promotes extrusion of oocytes from the follicle, but it is unclear how this can be triggered within the ovaries. Furthermore, spontaneous ovulation occurs in Parastichopus californicus but not in most other sea cucumbers. This species also possesses a very distinctive ovarian tubule recruitment mechanism (Smiley, 1988b) which is shared only by a small
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number of anatomically similar species (Sewell et al., 1997). Hence, although holothuroid oocytes are normally ovulated before spawning, the factors involved remain poorly understood. Experiments with RNF usually involve extracted gametes and/or a number of manipulations, which can influence oocyte maturation and the time needed for it to be completed. Smiley (1984, 1988a) and Maruyama (1985, 1986) used such methods to predict that an RNF acted on the follicle cells to produce the MIS leading to GVBD in holothuroids. However, a recent in vivo study (Hamel and Mercier, 2007) suggests a different mechanism as (1) GVBD was completed well after extrusion of oocytes from the follicle cells and (2) GVBD was never observed in oocytes collected in the lumen of the ovarian tubules or in the gonad basis after ovulation but before passage through the proximal constricted section of the oviduct, no matter how long they were left to soak in seawater (Fig. 3.7). Two hypotheses can be offered: (1) the action of RNF via follicle cells must be combined with mechanical activation (i.e., passage through the constricted duct, or pipetting in the case of in vitro studies) and (2) RNF acts through another pathway inside the gonoduct (Hamel and Mercier, 2007). Oocytes of several sea cucumbers, including Holothuria leucospilota respond to sea star RNF by undergoing GVBD even when denuded of their follicle cells (Maruyama, 1986), suggesting that other ovarian components may indeed produce the MIS. Such inconsistencies stress that in vitro studies of oocytes, which can involve manipulations such as squeezing, pipetting, rinsing, soaking in seawater and other media, centrifugation, and injection provide valuable data for elucidating cellular processes but do not necessarily reflect the actual in situ sequence. Further in vivo investigations may shed new light on the fine control of oocyte maturation in the hours or minutes before spawning and on the sequential involvement of RNF, MIF and other factors, but it is becoming clear that we must not expect to find a uniform pattern among holothuroids. The perivisceral coelomic fluid of several tropical holothuroids becomes bioactive immediately prior to and during spawning, eliciting gamete release in non-spawning individuals when injected or spread in the surrounding water (Mercier and Hamel, 2002). See Section 4.2 for details.
5.4. Asteroidea Mechanisms of final oocyte maturation and spawning have been mainly investigated in asteroids (Kanatani and Nagahama, 1983). As a result, the gonad-stimulating hormone of sea stars is among the better studied endogenous factors in echinoderms. Chaet and McConnaughy (1959) were the first to report that the injection of a hot-water extract of the radial nerve of Asterias forbesi induced gamete release in ripe females and males. The presence in the radial nerve of a substance responsible for inducing gamete
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(1)
(2)
(3)
o GP OT
FC GV
L
B o L GV
C o L
D o
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Figure 3.7 Holothuria leucospilota (Holothruoidea). Schematic representation of oocyte maturation and passage through the gonoduct during spawning (not to scale). Sections of the reproductive tract are divided into: (1) gonad basis (and attached ovary), (2) proximal section, and (3) distal section of the gonoduct. Transient deformations are illustrated by dashed lines, and insets show an enlarged view of the oocytes. T0 marks
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shedding was suspected, and later confirmed. Similar data have since been obtained for several sea star species (Kanatani, 1979). Cross-assays among different species have shown that the radial nerve factor acts, with some exceptions, in a non-species-specific manner (Kanatani, 1973). Positive responses were noted in whole animals receiving the nerve extract (Chaet, 1964; Kanatani and Noumura, 1962; Noumura and Kanatani, 1962) as well as in isolated ovary, testis or gonad fragments to the RNF (Chaet, 1966; Kanatani, 1964). The substance was thus believed to act directly on the gonad, an assumption that was confirmed by partial application of RNF to the whole ovary, in which case the treated portion alone released the oocytes (Kanatani, 1964). The substance was called the ‘‘gamete-shedding substance’’ (GSS), and is apparently present in the radial nerve throughout the year in nearly equal amounts, irrespective of the breeding season (Chaet, 1967). A number of manipulations have been conducted to localize the GSS. An extract prepared from male nerves induced gamete release in both sexes (Chaet, 1964). Furthermore, the GSS level in the radial nerve when assayed with isolated ovarian fragments in vitro in the presence of isolated ovarian fragments was equal in both sexes and also constant along the radial nerve and circumoral nerve ring (Kanatani and Ohguri, 1966). Other body components that are rich in nervous tissue such as the epidermis, tube feet, and cardiac stomach, have also been found to contain GSS, although its activity in these tissues is much lower than in the radial nerve (Kanatani and Ohguri, 1966). The fact that GSS is present in the coelomic fluid only when sea stars are undergoing natural spawning suggests that GSS is a hormone (Kanatani and Ohguri, 1966; Kanatani and Shirai, 1970). According to data from granules isolated from homogenates of the radial nerves of Asterina pectinifera by differential centrifugation and sucrose density gradient ultracentrifugation, and to histological studies using neuro-secretory staining in several asteroid species, granules containing GSS have been determined to occur in the supporting cells located just beneath the outer sheath of the radial nerve (Atwood and Simon, 1971; Imlay and Chaet, 1967; Unger, 1962). Similar structures were also found in the subepithelial plexus the onset of side-to-side sweeping movements in spawning females. (A) T0 15 min: mature oocytes in the ovarian tubules (OT), just before ovulation. FC, follicle cells; GV, germinal vesicles; GP, gonopore; L, lumen. (B) T0 þ 20 min: following ovulation, oocytes are transferred from the ovarian tubules to the gonad basis, where they are still not fertilizable. (C) T0 þ 30 min: oocytes are moving from the gonad basis through the proximal section of the gonoduct into the distal section, where they complete germinal vesicle breakdown, although most are still not fertilizable unless presoaked in seawater. (D) T0 þ 55 min: oocytes are lying in the distal section of the gonoduct, which begins to form a bulge under the gonopore. Seawater begins to enter, hydration of the jelly coat ( JC) occurs, and the majority of the oocytes become fertilizable. Broadcast will occur within ca. 15 min. Reprinted with permission from Hamel and Mercier (2007).
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of the tube feet, body wall, and cardiac stomach where GSS activity had been detected. In contrast, no GSS granules or GSS activity were found in the pyloric caecum, presumably because its extensive nerve plexus has no supporting cells (Atwood and Simon, 1971; Kanatani and Ohguri, 1966). Unger (1962) studied the transport of the fuschinophilic granules present in supporting cells along the fibres and suggested that GSS could be conveyed in a similar fashion to the radial and transverse haemal canals and through the water vascular system to the coelomic cavity, where the gonads are suspended. During the early investigations, GSS was believed to be a direct inducer of spawning in sea stars (Chaet, 1967), but later experiments have revealed that the action of this hormone is indirect, and that it acts on the ovary to produce a second active substance which induces oocyte maturation and spawning (Kanatani and Shirai, 1968; Kanatani et al., 1969; Schuetz and Biggers, 1968). GSS was shown to enter the ovary and act on the follicle cells around the oocytes to produce this second hormone (Cloud and Schuetz, 1973a,b; Hirai and Kanatani, 1971; Hirai et al., 1973), which has been isolated from ovarian fragments of Asterias amurensis and identified as 1-methyladenine (1-MA) (Kanatani et al., 1969). The gamete-shedding substance was later renamed the gonad-stimulating substance (GSS), retaining the same acronym (Kanatani, 1967). Isolated ovarian fragments undergo spawning in seawater containing 1-MA and ripe sea stars are induced to spawn when 1-MA is injected into the coelomic cavity (Kanatani, 1969). This author found that oocyte release in Marthasterias glacialis and A. forbesi occurred within ca. 30 min of injection of 30 mg 1-MA, whereas sperm release began after a slightly shorter latent period. The short interval preceding discharge of gametes after injection of GSS indicates that 1-MA production, presumably in the follicle cells, begins immediately after GSS is detected (Kanatani, 1969; Kanatani and Shirai, 1970). Mita (1993) confirmed that the amount of 1-MA produced by the follicle cells of Asterina pectinifera was sufficient for meiosis initiation and release of oocytes, and Mita and Nakamura (1994) concluded that the 1-MA content of sea star ovaries was sufficient to induce GVBD and ovulation. On the other hand, Schuetz (2000) provided evidence of extra-follicular mediation of oocyte maturation by RNF in Pisaster ochraceus, suggesting that other ovarian components could be a source of 1-MA. The effectiveness of 1-MA in inducing ovulation and spawning, either through intra-coelomic injection or soaking of the extracted ovaries, appears to be universal in asteroids, and has been shown in many species, for example, Patiria miniata, Pisaster brevispinus, Pisaster giganteus, Pisaster ochraceus, Pycnopodia helianthoides, Mediaster aequalis (Stevens, 1970), Pteraster militaris (McClary and Mladenov, 1989), Patiriella regularis (Byrne and Barker, 1991), Acanthaster planci (Babcock et al., 1994), Leptasterias polaris (Hamel and Mercier, 1995b), Coscinasterias muricata (Babcock et al., 2000),
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Smilasterias multipara (Komatsu et al., 2006) and several Antarctic species (Bosch and Pearse, 1990; Stanwell-Smith and Peck, 1998). The role of 1-MA in spawning induction is reportedly due to its capacity to dissolve the cementing substance that lies between the follicle cells and between the follicles and the oocytes (Kanatani and Nagahama, 1983). Ripe oocytes isolated from Asterina pectinifera and treated with 1-MA begin follicular envelope breakdown within half and hour; shrinkage of the envelope into a small clump may be due to contraction of the individual follicle cells which seem to be in an extended state (Kanatani and Shirai, 1969, 1970). Cytochalasin B, which is an inhibitor of certain contractile processes, immobilizes the follicle cells on the surfaces of oocytes treated with 1-MA (Schroeder, 1981), suggesting that cell contraction is the cause of the breakdown of the follicular envelope. Whether the action of 1-MA on the cementing substance is direct or indirect (i.e., activating an enzyme responsible for dissolving the cement) is not yet known (Kanatani and Nagahama, 1983). Once the follicular envelopes around the oocytes are removed by the action of 1-MA, the denuded oocytes become free within the lumen of ovary and are expelled by contraction of the ovarian wall (Kanatani and Shirai, 1969). When ovarian fragments of sea stars Asterias amnurensis were placed in seawater devoid of Mg2þ, they began to release oocytes after ca. 30 min (Kanatani and Shirai, 1969). Furthermore, ovarian fragments kept in Ca2þfree seawater for more than 30–45 min shed oocytes when Ca2þ was added, implying that lack of Ca2þ causes dissolution of the cementing substance and breakdown of the follicular envelope and that contraction of the ovarian wall, caused by the addition of Ca2þ, then forces out the loosened oocytes. Since bivalent cations such as Ca2þ and Mg2þ are known to stabilize intercellular cementing substances, spawning induced by the absence of these ions is attributable to the breakdown of the follicular envelope due to dissolution of the cementing substance. Isolated ovaries do not release oocytes when placed in seawater devoid of Ca2þ even in the presence of GSS (Mecklenburg and Chaet, 1964; Schuetz and Biggers, 1968), indicating that while contraction of the ovarian wall appears to be essential for carrying out the discharge of oocytes, dissolution of the cementing substance leading to follicular disintegration is a prerequisite for such contraction (Kanatani and Shirai, 1969). Tension has been detected in the ovarian wall of Asterina pectinifera after treatment with 1-MA (Shirai et al., 1981), suggesting that a jelly-like substance presumed to come in contact with the ovarian wall as a result of breakdown of the follicular envelopes may act as a direct inducer of tension in the ovarian wall. Since isolated ovarian walls that are stretched do not generate tension immediately when the jelly substance from mature oocytes is applied, 1-MA possibly induces ovarian contraction indirectly by allowing contact between the jelly and the ovarian wall (Shirai et al., 1981).
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Ever since the natural mitogen that converts the vitellogenic oocytes of asteroids into fertilizable oocytes was identified as 1-MA, extensive investigations have failed to isolate its receptor and early transduction pathway. Nevertheless, several elements of the signalling pathway that link the 1-MA receptor to MPF activation and maturation have been reported (e.g., Sadler and Ruderman, 1998; Tadenuma et al., 1992).
5.5. Echinoidea Unlike the oocytes of other echinoderms, those of sea urchins attain full maturity within the ovaries. Gamete release can be easily induced through injection of contraction-inducing substances like potassium chloride (KCl) and acetylcholine, or by applying an electric stimulus. Gonads readily respond to these stimuli by contraction of the gonadal wall and discharge of gametes (Appendix A10). A substance similar to sea star GSS has been detected in sea urchin radial nerves. Cochran and Engelmann (1972) reported that an extract of the radial nerves of Strongylocentrotus purpuratus induced spawning within 1 min in this and other species of sea urchins. The same extract also triggered spawning in sea stars after an average delay of 45 min. The GSS of Strongylocentrotus, a heat-stable polypeptide, presumably stimulated sea urchin gonads to produce a non-protein gonad factor which, like 1-MA, caused testis fragments to spawn (Cochran and Engelmann, 1975). This gonad factor co-migrated with 1-MA in thin layer chromatography (Cochran and Engelmann, 1972) but was not identified definitively. Since oocyte maturation is continuous and asynchronous throughout the breeding season in S. purpuratus (Chatlynne, 1969), Cochran and Engelmann (1972) suggested that significant levels of this gonad factor must be constantly maintained to induce spontaneous oocyte maturation, but no seasonal values of this gonad factor have been reported. Currently, the mode of action and transfer of this radial nerve factor (RNF) is unknown. Wasson and Watts (2007) speculated that nutritive phagocytes synthesize and store this gonad factor and discharge it upon stimulation by the RNF. The gonad factor subsequently triggers the release of neighbouring gametes or stimulates the contraction of the muscular epithelium, forcibly releasing gametes from the gonad lumen. The authors further presumed that the gonad factor is synthesized and stored in the neurons or epithelial cells of the peritoneum and released to stimulate contraction of the muscular epithelium in the presence of the RNF. Stevens (1970) reported that 1-MA failed to induce spawning of the echinoid Dendraster excentricus. In contrast, Kanatani (1974) found that high concentrations of 1-MA increased the proportion of oocytes maturing into ova in isolated ovarian fragments of Anthocidaris crassispina. Furthermore, gonadal extracts of several echinoids (Aeudocentrotus depressus, Anthocidaris
crassispina, Hemicentrotus pulcherrimus, Clypeaster japonicus and Peronella japonica) that induced maturation of oocytes in the asteroids Asterina pectinifera and Asterias amurensis contained 1-MA. According to Kanatani (1974), the presence of 1-MA in the ovaries of echinoids, particularly at the peak of the breeding season, could explain how oocytes can undergo maturation long before the onset of spawning.
C H A P T E R
F O U R
Discussion Contents 170 170 172 174 175 176
1. Methodological Considerations 1.1. Gonad index 1.2. Histology 1.3. Laboratory observation and experimentation 1.4. Field observations 1.5. Sampling interval and replication 1.6. Possible impact of climate change and anthropogenic disturbances 2. Insights from the Deep Sea 3. Emerging Trends and Future Research 3.1. Perception of cues 3.2. Understanding the role of food supply, temperature and photoperiod 3.3. Latitudinal effects 3.4. Heterospecific simultaneous spawnings 3.5. Final remarks
179 181 182 183 184 188 190 191
In common with earlier reviews (Giese and Pearse, 1974; Giese et al., 1991), we are obliged to recognise that the timing of reproductive events is undeniably variable. In some species, reproduction is aperiodical and apparently ‘‘continuous’’ (at least at the population level, though not necessarily at the individual level), whereas in others it is periodical, ranging from biennial/annual to semi-monthly. Breeding seasons at the population level tend to be variable, sometimes according to latitude. Nevertheless, it is becoming increasingly evident that a number of exogenous factors synchronize reproduction in echinoderm species. While considerable progress has been made over the past decades, our understanding is far from complete and only more research into this field will allow us to paint a comprehensive picture of the forces that drive reproductive processes and strategies in echinoderms. The current state of knowledge may simply reflect our inability to evaluate the reproductive cycles properly, most studies being of insufficient duration and/or detail to measure reproductive variability in space and time. We will consider a few of the most important methodological limitations in
Advances in Marine Biology, Volume 55 ISSN 0065-2881, DOI: 10.1016/S0065-2881(09)55004-3
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this field of research before outlining the common trends and hypotheses emerging from this review and the questions that merit more attention in the future.
1. Methodological Considerations The types of data deemed useful in determining reproductive periodicity (Giese and Pearse, 1974) have not changed much over the past decades. They can still be summarized as (1) rough estimates of the amount of material expended during the reproduction, estimated from changes in the gonad index; (2) transformation of gonadal cells during the gametogenic cycle as revealed by light and electron microscopy; (3) time course of gametogenesis, measured in successive samples taken from a population of animals or, when feasible, from the same animal; and (4) time and conditions under which spawning occurs, from laboratory and/or field observations. Major flaws and inaccuracies emerge when only one of these elements is studied, independent of the others.
1.1. Gonad index The oldest and most widely used quantitative method for estimating reproductive activity is the gonad index (GI) (Giese and Pearse, 1974), also termed gonadosomatic index (GSI). Although not precise, the technique is particularly suitable for routinely handling large numbers of samples. The GI is calculated in several ways, but is usually defined as the ratio of the gonad wet weight (or volume) to the wet weight (or volume) of the body wall, test or whole animal, expressed as a percentage. Because the body cavity can hold variable amounts of water and the digestive tract may or may not contain food, variations of GI can occur that are unrelated to reproduction. Therefore, determining ratios for eviscerated body wet weight or dry weight is more meaningful. One assumption of the method is that GI is independent of body size. Correlation between GI and body size should always be checked by regression analysis and individuals of similar size selected for the determination of the index. In particular, the relationship between gonad size and body size varies between juveniles and adults (Giese and Pearse, 1974; Gonor, 1972). Another important limitation of the GI method is that unless it is combined with microscopic examination of the gonadal tissues, it provides little indication as to what is occurring within the gonads. Many investigators have cautioned against relying on the GI alone, because it gives little indication of the development of the gametes themselves, and consider that it should always be used in combination with
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histological techniques (Nichols and Barker, 1984b,d; Nichols et al., 1985). For instance, when nutritive tissue within the gonads is utilized to synthesize the gametes, the index may remain unchanged despite an increase in actual gametogenesis (Nichols and Barker, 1984a). In contrast, when cellular changes are also followed (i.e., oocyte size frequency distributions), a more accurate picture of gamete development at each phase of the cycle can be obtained. Nichols (1994) noted that the use of the GI technique is generally precluded in crinoids, since the gonad is subdivided into many hundreds of small units, one to each genital pinnule, and, furthermore, the arms are seldom intact after collection. Thus, it is impractical to obtain measurements of both gonad and body size over an acceptable time scale and with an adequate sample size. Crinoid reproductive cycles are therefore generally determined from oocyte size frequency data or, for males, from the identification of spermatocyte development stages or measurement of the thickness of formative layers within the testis. Byrne et al. (1998) stated that although the GI of sea urchins is often used in studies of reproduction, it is inappropriate in cases where it does not provide a clear indication of the reproductive cycle (King et al., 1994) and where a wide size range of individuals is used (Gonor, 1972; Grant and Tyler, 1983). Instead, Byrne et al. (1998) used the gonad retrieval rate, calculated as the slope of a regression of gonad weight against total weight. Seward (2002) also extensively discussed the limitations of GI for the study of spawning periodicities in sea urchins, and concluded that few studies on reproductive cycles have provided a quantitative definition of spawning (i.e., based on changes in GI), or have been corroborated by histological analysis. Studies that did meet these criteria showed that a sharp decline in GI could be indicative of spawning in some species [e.g., Strongylocentrotus droebachiensis (Meidel and Scheibling, 1998)], but not in all [e.g., Centrostephanus rodgersii (King et al., 1994)]. In many echinoids, such as Sphaerechinus granularis, some GI peaks may have no clear relationship with the gametogenic cycle (Byrne, 1990; Guillou and Michel, 1993; King et al., 1994). For instance, such peaks appeared in S. granularis off South Brittany (France) when the seawater temperature was abnormally low, indicating the possible use of nutrient resources from the gonad (Guillou and Michel, 1993). Byrne (1990) also suggested that decreases in GI can be due not only to spawning but also to utilization of nutrient resources stored in the gonad. Other problems with the GI technique include asynchrony in gonad development among individuals, partial spawnings in some species, and variations in spawning patterns at the population level. The GI method proved to be much better suited to that species display a pronounced and synchronous annual spawning, involving most of the population, than to species in which few individuals of a population spawn at intervals (biannualy, monthly, etc.). For instance, declining GI values can accurately
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identify spawning periods in populations where individuals release all their gametes synchronously during one spawning event, such as in some coldtemperate species of holothuroids (Hamel and Mercier, 1996a; Hamel et al., 1993). However, in the case of reproductively asynchronous individuals or individuals that emit a portion of their gametes during multiple spawning events, such a quantitative definition of spawning becomes more difficult (Seward, 2002). Specific spawning behaviour is often poorly known since spawning is rarely observed in nature (Giese et al., 1991), so the relevance of GI cannot generally be predicted and inferences about population-level spawning based on changes in GI may be weak or erroneous. The few accounts of natural spawning show that sea urchins can spawn in aggregations or as scattered individuals (Pennington, 1985), that males typically spawn first, that once spawning is initiated conspecifics are stimulated to spawn (Giese and Pearse, 1974), and that spawning is highly variable, both temporally and spatially (Levitan, 2002a; Pennington, 1985). A final drawback of the GI is that it is not equally precise in all species, depending on their morphology. For example, McClary and Barker (1998) found that three species of echinoids exhibited GI values of unequal magnitude due to the test thickness, the GI cycle being more pronounced in the species with a thinner test.
1.2. Histology Gonadal smears and/or histological sections of the gonads are widely used to estimate reproductive status. Such data are not quantitative when the developmental cycle is merely divided into a series of maturity stages in a manner which may differ from that used by other investigators. Furthermore, the intervals between stages are not equal or fixed (or even known), so that they cannot be treated as a continuous variable and compared statistically. However, more robust quantitative data can be extracted from the sections by measuring the diameter, surface or volume of germ cells and oocytes, and estimating their size frequency distributions over time. This method allows the assessment of the progressive development of successive oocyte cohorts, and of the associated reproductive cycle. Obviously, the reliability of both GI and histological analysis is largely dependent on the number of samples taken throughout the year and the sampling intervals, and this aspect will be more extensively examined below in Section 1.5. According to a review by Hendler (1991), histological determinations of GI and gonad maturity have proved more reliable in establishing breeding periods in ophiuroids than have gonad smears, records of spawning in the laboratory and larval counts in plankton samples. In contrast, Singh et al. (2001) were critical of GI and histological methods in their study of the holothuroid Cucumaria frondosa, since collection of similar-sized individuals did not allow the authors to meet the requirement of size independence of
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GI, indicating that GI was not a reliable indicator of reproductive condition in this species. Discrepancies can also arise from other factors such as the spatial scale of sampling individual animals and sub-sampling within an individual gonad (see Section 1.5 for a discussion of these potential biases). Singh et al. (2001) tested several other techniques and suggested that gonad volume fraction, gonad dry weight and cross-sectional tubule area provided more accurate determination of the spawning period. Furthermore, the proportion of the tubule respectively occupied by haemal fluid and spermatids or spermatozoa was another good indicator of spawning in males (Singh et al., 2001). Histological analysis of the gonads of the asteroid Asterina stellifera in Brazil showed that spawning started earlier than suggested by the GI, further highlighting the importance of using histological analysis in addition to GI in the investigation of reproductive cycles (Carvalho and Ventura, 2002). Similarly, a field study of pre- and post-spawning indices and biochemical composition in Asterias rubens (¼vulgaris) from eastern Canada, demonstrated the limitations of tissue indices, especially that of the pyloric caecum, since an increase in mass sometimes corresponded with a decrease in biochemical components (Raymond et al., 2007). According to Lozano et al. (1995), the maturity index, the thickness of the gonad wall and cellular composition of the gonad provide the most reliable indicators of the reproductive cycle of sea urchins, whereas the GI is less reliable, as it is significantly affected by the nutritive tissue of the gonad (Gonor, 1973c; Pearse, 1969b). Lozano et al. (1995) also emphasized that the GI method is often flawed because some inherent assumptions, especially the absence of a relationship between body size and GI, are not necessarily valid. Indeed, many studies do not specify whether analyses have been restricted to a particular range of sizes. Lozano et al. (1995) observed fluctuations in the temporal pattern of the GI and the presence of peaks that had little to do with the gametogenic cycle, according to all other indices measured. The authors suggested that successive storm events could have depleted nutrient stores in a manner similar to the decreases in GI recorded by King et al. (1994) that were related not to spawning but to changes in nutrients stored in the gonad. Bennett and Giese (1955) suggested that gametogenesis may be the last process to be interrupted in sea urchins. Similarly, Vaschenko et al. (2001) reported that the common assumption that GI values in sea urchins reflect the level of gonad maturity was not supported by a study of Strongylocentrotus intermedius at four stations in the Sea of Japan. Some individuals exhibited a fairly high gonad maturity yet very low GI value, while in others had the highest GI value coincided with the lowest gonad maturity index. This emphasizes the benefits of using other methods to complement GI measurements in studies of gametogenesis, since gonad growth is not always due to gamete synthesis and a decrease in gonad size is not necessarily the result of spawning.
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1.3. Laboratory observation and experimentation Although infrequently used, the long-term rearing and monitoring of animals in the laboratory provides another way of assessing reproductive processes and spawning periodicities. However, compiling data on gamete release in the laboratory constitutes a powerful tool only when the holding conditions simulate those of the natural environment (i.e., exposure to unfiltered running seawater under natural conditions of light, temperature and food supply). Spontaneous spawning under such conditions is especially reliable when occurrences are repeated and/or corroborated by observations in the field (through serial gonad samples or in situ sightings). For instance, excellent correlations between laboratory and field spawning events have been reported for the sea star Leptasterias polaris (Hamel and Mercier, 1995b), and the bathyal asteroid Henricia lisa repeatedly spawned in the laboratory at the time predicted from the examination of serial gonad sections (Mercier and Hamel, 2008). These two studies allowed the investigators to identify the most probable spawning cues. On the other hand, field and laboratory data on spawning are not always in agreement. For instance, in the Bristol Channel the asteroid Astropecten irregularis was fully ripe in June and spawned in July (Grant and Tyler, 1986), whereas a laboratory population of A. irregularis spawned earlier, in May–June (Christensen, 1970). Furthermore, Pearse and collaborators repeatedly witnessed gamete shedding in Pisaster ochraceus (Pearse and Eernisse, 1982) and Strongylocentrotus droebachiensis (Pearse et al., 1986b) in the laboratory well after spawning in the field, determined by regular sampling. Captive animals may be disconnected from the spawning cue and retain their mature gametes until the individuals become ultrasensitive to an unknown stimulus, in a process similar to stress-induced gamete release during collection and handling ( J. S. Pearse, personal communication). However, this hypothesis does not fully explain why spawning, when it eventually occurred, was synchonized between several unconnected tanks. Precocious or delayed spawning in laboratory-held echinoderms may thus be due to spatial, temporal or sub-population effects, or to the influence of laboratory conditions on potential cues (e.g., light intensity, temperature). With respect to the onset and progression of gametogenesis, periodic biopsies or in vivo investigation of the gonads of the same individual would provide valuable information. One of the disadvantages of this procedure is that results may be difficult to interpret due to possible effects of an invasive technique on the animal. Nevertheless, biopsies and in vivo observations are useful for some species (Hamel and Mercier, 1996b; Hamel et al., 2007; Pearse et al., 1986a), and radiographic methods may also merit consideration. There have been few comprehensive experimental investigations of the effects of biological or environmental factors on the reproduction of echinoderms. While very useful, experimental manipulation of reproductive
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activity may be misleading by emphasizing only one of many interacting time cues, and perhaps not those that are usually important in nature (Giese and Pearse, 1974). Nevertheless, as stated above for laboratory monitoring, experimental trials become powerful tools when properly designed, especially when they are supported by field data or in situ observations. Examples include the suite of studies conducted by Pearse and collaborators on the effect of photoperiod on gametogenesis in asteroids and echinoids (Pearse and Beauchamp, 1986; Pearse and Bosch, 2002; Pearse and Eernisse, 1982; Pearse and Walker, 1986; Pearse et al., 1986a,b) and the determination of phytoplankton as a spawning inducer in the sea urchin Strongylocentrotus droebachiensis (Starr et al., 1990, 1992). Furthermore, one of the first demonstrations of chemical communication between individuals during gametogenesis in echinoderms was achieved with experimental trials (Hamel and Mercier, 1996b, 1999). In echinoids, the determination of spawning periodicity (both in the laboratory and in the field) has commonly been achieved by evaluating the response of individuals to KCl injections (Appendix A1.). Although concern has been expressed about the possible side effects of this technique (e.g., McCarthy and Young, 2004), it has also been shown that peak induction of gamete release in Antarctic echinoids coincided with the presence of pluteus larvae in the wild (Stanwell-Smith and Peck, 1998). We believe that the response to KCl might be a suitable means of determining readiness to spawn in those species that exhibit annual spawning events involving a major portion of the population, but may not be appropriate for species in which partial spawning occurs on a biannual or monthly cycle, since ripe gametes may be released by some individuals at almost any time, thus masking the underlying trend.
1.4. Field observations The collection of eggs, embryos, larvae, or juveniles in the field during or following the breeding period is another approach in the study of reproductive periodicity, although the identification of offspring is sometimes difficult. Furthermore, such measures can only indicate the spawning time and periodicity when the embryonic development and duration of the larval phase under various environmental conditions are well known. In situ observations of spawning in the field provide the most reliable data, but correlations with environmental triggers are not easy to make unless the observations are repeated several times or the spawning event is massive. However, even the most fortuitous field observation can confirm or falsify data for breeding cycles obtained from laboratory observations and/or GI and histological analysis. For instance, according to gonad, histology spawning of the holothuroid Cucumaria frondosa occurs in February–May in Newfoundland (eastern Canada) (Coady, 1973), yet gamete shedding has
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been observed only in March–April of 2 consecutive years in the Avalon Peninsula, Newfoundland (personal observation). The same species spawns later in the spring in other areas of eastern Canada; direct observations in the Gulf of St. Lawrence consistently point to mid-June (Hamel and Mercier, 1995a, 1996a,c,d), whereas gonad indices indicate April–June in the Bay of Fundy (Singh et al., 1999, 2001). However, the data may be biased owing to heterogeneity in the gonad morphology of C. frondosa along the north-east American coast (Hamel and Mercier, 1996a). The gonad is divided into two distinct classes of gonadal tubules in northern latitudes, where gamete maturation requires 2 years (Fig. 4.1), while on the Grand Banks and south of mid-New Brunswick (Canada) tubule structure is homogenous and an annual cycle is evident. Different local environmental conditions may regulate this morphological disparity, including temperature and length of the vegetative season. Sea cucumbers in southernmost locations presumably benefit from a longer feeding period and higher mean annual temperature, which may favour an annual gametogenic cycle and also increase fecundity (Hamel and Mercier, 1996a).
1.5. Sampling interval and replication When using serial sampling to assess GI, gonad maturity or oocyte size frequency distribution, a major difficulty lies in the temporal resolution used to examine changes at the population level. Most studies of reproductive cycles sample populations at monthly intervals, sometimes less frequently, and may not capture spawning or other events that take place on a shorter time scale. Furthermore, a complete annual cycle is sometimes determined by assembling monthly samples from different years, especially when opportunities for collection are severely limited, such as for deep-sea species. Spatial variability is rarely considered in sampling protocols but can be important. For example, Kelly (2000) found significant variation in the GI of the echinoid Psammechinus miliaris among samples collected only ca. 200 m apart. The author emphasized that the conclusions of the study could therefore be very different depending on which sub-sites of the two distinct habitats investigated (intertidal and subtidal) were contrasted. Thus, comparisons among locations without adequate replication may not accurately reflect habitat effects (Kelly, 2000). However, single site comparisons remain the most widely used method of comparing reproductive variability between populations (e.g., Guillou and Lumingas, 1999; Konar, 2001; Lamare et al., 2002; Lozano et al., 1995). Another example of the importance of spatial sampling scales on the study of reproductive processes is provided by Seward (2002), who observed high variability in changes in GI in sea urchins (Strongylocentrotus droebachiensis) sampled without regard for spatial distribution. Local effects may have been involved, whereby individuals close to one another may
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Constant conditions 100
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J J A S O N D J F M A M J J 1992 1993 Postspawning
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J J A S O N D J F M A M J J 1992 1993 Advanced-growth
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Figure 4.1 Cucumaria frondosa (Holothuroidea). Relative frequencies of different gametogenic stages in the small and large gonadal tubules of males and females kept under constant environmental conditions and naturally varying conditions from May 1992 to November 1993. Reprinted with permission from Hamel and Mercier (1996b).
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have been spawning synchronously, while distant individuals may not yet have spawned. The author concluded that the lack of information regarding the spatial distribution of the sampled individuals, combined with temporal variability of natural spawning, made it difficult to define spawning from measurements of GI alone (Seward, 2002). Local or intra-site variability such as that reported by Kelly (2000) may bias the results of studies of reproductive cycles in most echinoderms, limiting the conclusions that can be drawn from comparisons of populations from dissimilar temperature or food regimes (see Section 3 in Chapter 3). Another source of sampling bias arises when gamete development is not uniform within the gonadal tissue and histological sections do not adequately take this into account. Homogeneity within the gonad was observed in several individuals of the echinoid Heterocentrotus mammillatus (Dotan, 1990), and although the author argued that such homogeneity is common in echinoids worldwide, he did not provide any supporting argument, referencing only the work of Pearse and Phillips (1968) on Echinometra mathaei. However, in some holothuroid species, the gonadal tubules are not homogenous (Hamel and Mercier, 1996a; Hamel et al., 1993; Smiley et al., 1991) and sub-sampling of the gonad can easily introduce a bias in the histological analysis (see discussion on Cucumaria frondosa in Section 1.4). The study of reproductive cycles in deep-sea echinoderms is complicated by additional problems that may compromise the data obtained. Because opportunities for sampling are scarce, data are often pooled from samples collected from stations distant from one another and/or from different depths (Tyler and Gage, 1984b; Tyler et al., 1990). For instance, after pooling data from sporadic collections made between 1973 and 1984 at stations up to hundreds of kilometers apart, Tyler et al. (1985) concluded that the deep-sea holothuroids Peniagone azorica and P. diaphana possessed a ‘‘continuous’’ reproductive cycle. A study on the asteroid Henricia abyssicola in the NE Atlantic was based on six samples collected between 1979 and 1984 from areas that were sometimes distant from one another, data from different months every year being combined to construct the annual cycle (Benitez-Villalobos et al., 2007). The impact of such constraints is not yet fully known. As noted earlier, sampling in shallow water over relatively large areas (and even within perimeters <50 km) may introduce large variation in data for gonad development and spawning periodicity. Inter-annual differences in maturation and spawning are also common. Thus, the frequent assumption that a given sampling protocol does not create bias has to be re-examined more closely. Reproductive cycles should preferably be determined over 2 years rather than the usual 12 months, and the practice of combining data from several years and different locations to analyse the annual trend in reproduction should be abandoned.
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1.6. Possible impact of climate change and anthropogenic disturbances How will the predicted changes in the physical and chemical properties of the oceans resulting from global climate change affect the seasonal or cyclical reproductive cycles observed in most echinoderms? Over a decade ago, Olive (1995) indicated that to answer this question in marine invertebrates would require a knowledge of elements such as: (1) patterns of reproduction of a range of species under different conditions and in various locations, (2) physiological linkages with environmental factors that are direct mediators of the observed seasonality, (3) molecular mechanisms involved in responses to environmental cues, and (4) the adaptive significance of cyclic reproduction. Some authors have suggested that temperature anomalies may influence population structure and the timing of reproduction in echinoderms (Barnes et al., 2001; Drumm and Loneragan, 2005; Hopper et al., 1998; McClary and Barker, 1998; Sewell and Bergquist, 1990). It remains to be verified whether large climate oscillations can affect or modify reproductive cycles, and if so, how. Lawrence and Soame (2004) suggested that global warming could have significant consequences for organisms that develop gametes during winter and spawn in the spring in temperate northern latitudes. Particularly vulnerable would be those species that cue reproductive processes on photoperiod. The authors concluded that extinctions were unlikely, but that local extirpations were possible, depending on the rate of adaptation to shifting conditions exhibited by each species (Lawrence and Soame, 2004). Acute and chronic perturbations of anthropogenic origin are another source of concern with respect to exogenously mediated reproductive patterns. Several chemical compounds are known or suspected to disrupt acquisition of energy reserves, gamete production and gonad growth in echinoderms. According to a recent review by Sugni et al. (2007) on endocrine disrupters in echinoderms, various compounds influence gonad maturation in different ways, nutritive phagocytes generally being much more affected than germ cells. Phagocytic activity in the testis is particularly stimulated by high concentrations of the anabolic steroid methyltestosterone (MET), the antiandrogen cyproterone acetate (CPA), and the organic pesticide triphenyltin (TPT). Furthermore, exposure to TPT can significantly inhibit oogenesis, reducing the number of individuals undergoing active oogenesis and slowing down oocyte maturation, thereby stimulating phagocytic and cellular rearrangement within the ovary (Sugni et al., 2007). The same review reported that TPT and MET considerably reduced oocyte diameter, whereas the pesticide fenarimol (FEN) had the opposite effect. Variations in estradiol levels were particularly evident after exposure to TPT and FEN (Lavado et al., 2006b), and the concentrations measured coincided with the changes in oocyte diameter reported by Sugni et al. (2007), who concluded that these
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compounds interfere with vitellogenic processes in echinoids, at least partially by interfering with the endocrine system. Furthermore, the expression of the major yolk protein (MYP) may be under estrogen control (Unuma et al., 2003). Although estrogen receptors have not been positively identified in echinoderms, Lutz et al. (2004) have reported specific estrogen and androgen binding sites in the crinoid Antedon mediterranea and the echinoid Paracentrotus lividus. Furthermore, maximum estrone levels occurred during early vitellogenesis in the asteroid Asterias rubens (Schoenmakers and Dieleman, 1981), and oocyte diameter and protein level increased in the ovaries of other species (Sclerasterias mollis, Asterina pectinifera) after in vivo and in vitro treatments with estrone and estradiol (Barker and Xu, 1993; Takahashi and Kanatani, 1981). These data strongly suggest the involvement of estrogen in the synthesis, transport and incorporation of proteins and nutrients in growing oocytes, supporting the contention that estrogen-interfering compounds may significantly affect reproductive processes (Sugni et al., 2007). Studies on asteroids have clearly demonstrated disruption of steroid metabolism by certain pollutants. For instance, cadmium and polychlorinated biphenyls (PCB) disrupt progesterone and testosterone levels in gonads and pyloric caeca (Den Besten, 1998; Den Besten et al., 1991). Furthermore, Mercier et al. (1994) showed that exposure of Leptasterias polaris to environmental levels of the biocide and plastic stabilizer tributyltin (TBT) via the food chain did not yield high concentrations in the tissues, but resulted in smaller mature oocytes and a thinner gonadal epithelium. These observations suggest that asteroids, and possibly other echinoderms, avoid immediate accumulation of TBT by dealkylating the toxicant to less harmful metabolites but that this natural defence mechanism induces subtle effects on reproductive organs by disturbing reserve acquisition in growing gametes (Mercier et al., 1994). Other authors have reported anomalies in sea urchin spermatogenesis and reduced sperm motility after long-term exposure to phenols (Au et al., 2003). Endocrine disrupting compounds in echinoderms appear to affect the immune system as well as reproduction, as they do in vertebrates, emphasizing their broad spectrum of action (Sugni et al., 2007). Because they occur in urban coastal environments at concentrations reported to interfere with endocrine mechanisms, various toxicants and disrupters have been suspected to be the source of variability in several studies of reproduction in echinoderms. For instance, Vaschenko et al. (2001) observed pathological changes in the ovaries of 80–100% of sea urchins Strongylocentrotus intermedius collected off Vladivostok (Russia) in 1997. The authors also indicated that the indices of various pathological changes in the gonads significantly increased between 1985 and 1997. particularly lipofuscin, a final product of lipid peroxidation that can accumulate in sea urchin gonads as a consequence of pathological processes (Vaschenko et al., 2001). In their study site, the main sources of pollution were presumed to be municipal and industrial wastewater draining heavy
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metals, hydrocarbons, phenols, and other inorganic and organic pollutants from the city of Vladivostok, and a neighbouring sea port. The authors suggested that the absence of correlation between the GI and gonad maturity index resulted from pollution-induced disturbance of gametogenic processes (Vaschenko et al., 2001). Similarly, Bo¨ttger and McClintock (2002) indicated that shallow-water populations of the sea urchin Lytechinus variegatus subjected to inorganic and organic phosphate pollutants were likely to exhibit decreased allocation of nutrients to gonadal growth and delayed or arrested gametogenesis. These are only a few examples from the growing number of publications on this topic.
2. Insights from the Deep Sea Deep-sea habitats have traditionally been considered to be among the least variable of all. However, recent evidence suggests that there are seasonal fluctuations in the physico-chemical environment of the deep sea, and that deep-sea invertebrates may exhibit annual reproductive periodicities (Tyler, 1988; Tyler et al., 1982b). Echinoderms were among the first deep-sea animals shown conclusively to exhibit seasonal reproduction (Lightfoot et al., 1979; Tyler et al., 1982b) and recruitment (Schoener, 1968), although it is now believed that seasonal breeding is the exception in this group rather than the rule (Young, 2003). In the Rockall Trough (NE Atlantic), where numerous species have been examined at various times of the year, only a small proportion of species reportedly breed seasonally. However, at shallower bathyal depths on the Bahamian Slope, the majority of species appear to be seasonal breeders (Young, 2003). Furthermore, Tyler et al. (1982b) followed the seasonal occurrence of larvae in the plankton and showed that four species of deepsea echinoderms have well synchronized reproductive cycles. It is likely that exogenous factor(s) control the synchrony of spawning and act as the ultimate selective agent determining reproductive seasonality. Evidence of periodical reproductive cycles in deep-sea echinoderms was obtained at about the same time that predictable environmental events were discovered at bathyal and abyssal depths. The traditional perception of the deep sea as a homogenous and stable environment has been seriously challenged during the last few decades, prompting a re-evaluation of the physical and chemical factors that control the ecology of benthic organisms in the deeper strata of the ocean (Tyler et al., 1994). These authors outlined two broad groups of ecological controls: (1) large-scale irregular events such as benthic storms that can rework and transport sediment and turbidity currents or debris flows that can smother benthic invertebrates; (2) predictable and unpredictable pulses of detritus which may have a profound effect
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on the ecology of deep-sea benthic organisms. The input of organic material can come from sizeable food falls (i.e., animal carcasses) which do not follow any seasonal trend but may provide up to 10% of the energy requirement to the deep-sea benthos (Smith, 1985). Macro-algae, seagrasses and wood form another type of large irregular food input (Tyler et al., 1994). A more predictable source of food to the deep-sea floor is phytodetritus and other particulate elements sinking from the euphotic zone. Sediment trap studies have revealed that such material does not reach the benthos as a slow, constant rain of particles, but rather episodically (Tyler et al., 1994). The transfer of surface production to deep water is both rapid and highly seasonal (Deuser and Ross, 1980; Deuser et al., 1981; Honjo, 1982). Such a cycle in the availability of surface-derived food should favour selection for annual reproduction, at least in species with planktotrophic larvae, since larvae produced outside the period of enhanced food supply would have a decreased chance of survival (Tyler et al., 1982b). Long-term analysis of current velocity has revealed that surface-generated kinetic energy oscillate with periods that range from semi-diurnal and diurnal tidal components to low frequency signals, with seasonal maxima in late winter and minima in summer (Tyler et al., 1982b and references therein). The seasonal effects of such phenomena rapidly diminish with depth but may nonetheless be transmitted to depths exceeding 2900 m (Tyler et al., 1982b). The possible role of low-frequency physical periodicities as proximate spawning cues in echinoderms remains speculative. Secondary effects such as episodic re-suspension of sediment above critical erosive current velocities at the benthic boundary may be more important than direct effects of water motion on echinoderms living on the deep-sea floor. Nevertheless, interindividual spawning cues may be more rapidly transmitted throughout a population at times of high water motion (Tyler et al., 1982b). It is becoming increasingly apparent that seasonal periodicities in the physical environment and in sedimentary organic flux from the surface within the deep sea can result in cyclic reproductive patterns in deepwater benthic organisms. It remains unclear how two or more sympatric species can exhibit very different reproductive patterns under the same environmental conditions (Tyler et al., 1994), a paradox which is also true for sublittoral species. In order to integrate data from various sources, the methods used to examine reproductive periodicity must be evaluated and possibly standardized in future studies (see Section 1.5).
3. Emerging Trends and Future Research A diversity of factors is required for entraining or cueing gametogenesis and spawning if synchronization of breeding periods is to be achieved among individuals of given species in different habitats (e.g., tropical,
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boreal, littoral, abyssal). Cue diversity is also crucial to the maintenance of reproductive isolation, since when species (especially congenerics) occur sympatrically they can then respond to slightly different signals, or somewhat differently to the same signals, thus avoiding wastage of gametes through interbreeding. Reproductive isolation would then become the ultimate factor shaping the reproductive periodicities through the determination of species-specific cues.
3.1. Perception of cues While external cues undoubtedly play a role in the control of reproductive processes in echinoderms, the mechanisms by which individuals perceive and interpret these cues (especially slight variations in light intensity, chemical factors and phytoplankton) are not fully understood. Nevertheless, phototaxis and diffuse photosensitivity in echinoderms have been discussed for more than half a century (Millott, 1955, 1975; Yoshida, 1966; Yoshida and Ohtsuki, 1968) and Shirai and Walker (1988) have suggested that the entire surface of the echinoderm body may respond to environmental stimuli. A large variety of stimuli-dependent behaviour has been described and a basic knowledge of putative sensory structures gathered, providing useful hypotheses for the study of environmental perception related to sexual activities in echinoderms. Various phototactic responses have been documented in the Echinodermata (Hendler, 1984; Yoshida and Ohtsuki, 1968). The general view is that sensitivity to light is mediated predominantly through extra-ocular photoreception (Hendler, 2004), although some asteroids and synaptid holothuroids possess ocelli, also called eye-spots or rhabdomeric eyes (Eakin and Brandenburger, 1979; Yamamoto and Yoshida, 1978). Pearse et al. (1986a) investigated the possible role of ocelli in the perception of photoperiod and its role in regulating the gametogenic cycle in the sea star Pisaster ochraceus. Although gonad maturation was not affected when ocelli were removed, individuals without ocelli were never observed to spawn, unlike the intact animals (Pearse et al., 1986a). This suggests that ocelli are not responsible for mediating the photoperiodic response in this species but that they may be involved in the detection of the spawning cue. Although the echinoid test is believed to be almost opaque to ultraviolet and visible light (Walker et al., 2007), adult sea urchins exhibit a wide range of responses to light intensity, including negative phototaxis leading to shelter seeking and covering reactions (e.g., Adams, 2001), daily migrations and light-dependent oriented movements (Barnes and Crook, 2001; Millott, 1975). There is increasing evidence that light intensity in echinoids and other echinoderms may be detected by photoreceptors located in the tube feet, pedicellariae, spines or other regions.
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Recent advances include the description of spatial vision in the echinoid genus Echinometra (Blevins and Johnsen, 2004) and of specialised photosensory organs in ophiuroids (Ophiocoma spp.), whereby the calcite ossicles of the dorsal arm plates act as microlenses transferring light to putative photoreceptors (Aizenberg et al., 2001). The presence of a visual pigment in echinderms was proposed by Johnsen (1997), who used biochemical and immunochemical techniques to determine that a protein homologous to rhodopsin occurs in the ocelli of asteroids (Asterias forbesi) and the arms of ophiuroids (Ophioderma brevispinum). Furthermore, a known regulator of eye development in vertebrates (Pax-6) has been detected in the tube feet of the sea urchins Strongylocentrotus purpuratus and Paracentrotus lividus (Czerny and Busslinger, 1995), suggesting that echinoderm ancestors possessed eyes and/or that the responsible gene is expressed in the extra-ocular photoreceptors of extant echinoderms. Furthermore, Raible et al. (2006) discovered opsins and clusters of sensory G-protein-coupled receptors (GPCRs) in the genome of S. purpuratus. Members of the GPCR superfamilies mediate chemoreception and photoreception in vertebrates and invertebrates (Ache and Young, 2005), suggesting that they act as chemosensory receptors in the sea urchin. Moreover, the number of rhodopsin-type GPCRs in S. purpuratus is similar to that found in mammals, exceeding that of many other invertebrates, which is consistent with a rich molecular inventory of sensory molecules in this species (Raible et al., 2006). Chemosensory responses in echinoderms have been well documented (e.g., Brewer and Konar, 2005; Hagen et al., 2002; Pisut, 2004; Sloan and Campbell, 1982; Valentincic, 1991), although studies to date have almost exclusively focused on foraging activities and prey–predator interactions. Nevertheless, their ability to track gradients of food stimuli indicates that echinoderms may also perceive variations in the concentration or nature of other chemical signals such as exudates from phytoplankton and pheromones emitted by conspecifics.
3.2. Understanding the role of food supply, temperature and photoperiod Most of the evidence for the influence of food supply on echinoderm reproduction refers to the metabolic costs of gamete synthesis and the effect of nutritional status on breeding. The published literature suggests that in most species nutrition influences the quantity and size of gametes synthesized rather than the timing of the breeding season. In some species, food availability may indirectly determine the beginning of gamete synthesis for purely energetic reasons and should therefore be considered a prerequisite rather than a cue. Nevertheless, a few cases have been found in which the chemical nature of the food may trigger reproductive processes, irrespective
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of the nutritional requirements of the breeding adult. Qualitative changes in the food, such as the presence of trace metabolites, could serve to synchronize reproduction. The chemical composition of many planktonic organisms varies seasonally, which may be detected by animals feeding upon them (Giese and Pearse, 1974). Such changes could serve as a proximate exogenous regulator of reproduction. Despite the accumulating experimental evidence for the roles of temperature and photoperiod on gamete synthesis, the data are largely confounded by synergistic effects. Anomalies in annual ocean temperature cycles possibly delay (e.g., Hopper et al., 1998; McClary and Barker, 1998; Sewell and Bergquist, 1990) or advance (e.g., Drumm and Loneragan, 2005) the breeding period, whereas considerable effects on gamete synthesis have been observed in some species when individuals were maintained in warmer or colder seawater (e.g., Cochran and Engelmann, 1972; Lares and McClintock, 1991; Pearse, 1981; Sakairi et al., 1989). Such responses can be attributed to the regulation of metabolic processes rather than to a direct effect of temperature on the reproductive cycle. Nevertheless, a few studies have shown that temperature can be a proximate cue. For instance, certain species require a degree of sequential temperature variation (i.e., from low to high values, or vice versa; Table 4.1) or exposure to a precise temperature range in order to initiate gamete synthesis (Ito et al., 1989; Kelly, 2001). More rarely, a specific temperature threshold has been identified as the trigger for final gamete maturation and/or spawning (e.g., Hamel and Mercier, 1995b; Mercier and Hamel, 2008). While severe temperature fluctuations associated with collection or handling and heat shock treatments frequently induce spawning in many echinoderm species, the role of temperature in this response remains difficult to evaluate due to the profusion of confounding variables. The broader role of sea surface temperatures in determining breeding activity is another much discussed topic (see Section 3.3). It is clear from numerous experimental trials that gametogenesis in certain asteroids and echinoids is directly influenced by photoperiod. Nevertheless, there is no general explanation for the observed intraspecific variation, or for the fact that species respond to photoperiod differently or not at all (Table 4.1). For instance, laboratory manipulations of photoperiod successfully modified the gametogenic cycle of Strongylocentrotus droebachiensis (Walker and Lesser, 1998) and S. purpuratus (Bay-Schmith and Pearse, 1987; Pearse et al., 1986b), whereas S. franciscanus remained unresponsive ( J. S. Pearse, personal communication). However, S. franciscanus is more closely related to the Japanese species Hemicentrotus pulcherrimus and Pseudocentrotus depressus, which do not respond to photoperiod (Table 4.1), than to any North American species (Biermann et al., 2003), suggesting the presence of phylogenetic constraints ( J. S. Pearse, personal communication). Indeed, more
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## in Japan (Ito et al., 1989; Sakairi et al., 1989; Yamamoto et al., 1988) $ in USA (McBride et al., 1997; Pearse, 1981)
$$ in Japan (Masaki and Kawahara, 1995; Yamamoto et al., 1988) # in Ireland (Byrne, 1990) # in France (Spirlet et al., 1998) ## or $$c in France and Israel (Shpigel et al., 2004; Spirlet et al., 2000) "" or $$d in Portugal (Luis et al., 2005) "" in UK (Kelly, 2001)
$$ in Japan (Ito et al., 1989; Sakairi et al., 1989; Yamamoto et al., 1988)
## in USA (Walker and Lesser, 1998) ## in Canada (Dumont et al., 2006) # in USA (Gonor, 1973c) ## in USA and Mexico (Bay-Schmith and Pearse, 1987; Pearse et al., 1986b)
$ in USA (Garrido and Barber, 2001) ##? in USA (Walker and Lesser, 1998) $ in USA (Gonor, 1973a; McBride et al., 1997) ##a in USA (Cochran and Engelmann, 1975; Pearse, 1981) " in Russia (Viktorovskaya and Matveev, 2000)
## in Japan (Masaki and Kawahara, 1995; Yamamoto et al., 1988) # in Ireland (Byrne, 1990) # in France (Spirlet et al., 1.998) ##a or $$b in France and Israel (Shpigel et al., 2004; Spirlet et al., 2000) $$b in Portugal (Luis et al., 2005) Psammechinus miliaris ##? in UK Kelly (2001) Echinometra mathaei " in Australia and Indo-Pacific (Pearse, 1968a; Pearse and Phillips, 1968) $ in Kenya (Muthiga, 2005)
Strongylocentrotus intermedius Hemicentrotus pulcherrimus Strongylocentrotus franciscanus Pseudocentrotus depressus Paracentrotus lividus
Photoperiod
Temperature
Temperature and/or photoperiod regimes that promote the onset and/or completion of gametogenesis in echinoids
Strongylocentrotus droebachiensis Strongylocentrotus purpuratus
Species
Table 4.1
187
##a,*b in USA (Lares and McClintock, 1991)
# followed by " in France (Nunes and Jangoux, 2004) " in the Indo-Pacific (Pearse, 1968a, 1974; Tuason and Gomez, 1979) "a in Bermuda (Iliffe and Pearse, 1982) $ in Panama (Lessios, 1981) # in Barbados (Lewis, 1966) and Florida (Bauer, 1976)
"" in Japan (Sakairi et al., 1989)
## in USA (McClintock and Watts, 1990)
# in Australia (Byrne et al., 1998)
$$ in Japan (Sakairi et al., 1989)
b
Inhibition of gametogenesis at high temperature. Maturation observed when animals kept at constant temperature. c Maturation observed when animals kept under constant short days (8–12L/16–12D, or darkness). d Maturation observed when animals kept under constant long days (14L:10D). * Spermatogenesis only, oogenesis not affected. " ¼ long days or increasing photoperiod; high or increasing temperature. # ¼ short days or decreasing photoperiod; low or decreasing temperature. $ ¼ no effect or no relationship. Species are listed according to phylogenetic relationships (Biermann et al., 2003; Littlewood and Smith, 1995). Double symbols indicate experimental studies.
a
Centrostephanus rodgersii Eucidaris tribuloides
Diadema antillarum
Anthocidaris crassispina Echinocardium cordatum Diadema setosum
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phylogenetic investigations may be required to examine clades of species, which may have common constraints in their reproductive strategies, and/or constitute the outcome of a specific transformation. Such analyses provide a reasonable rationalization of the different latitudinal trends observed in the modes of development of certain marine invertebrates in the Atlantic and in the Pacific (Pearse and Lockhart, 2004). For the time being, despite recent phylogenetic revisions (Biermann et al., 2003), Table 4.1 does not provide any clear evolutionary or latitudinal explanation to the apparent inter-specific inconsistencies in the response to photoperiod and temperature. Nevertheless, removing the correlative data and considering only experimental results does reveal a trend in strongylocentrotid species, falling or low temperatures marking the onset of gamete synthesis. In North American species, direct control is indeed exerted by decreasing or short day lengths, whereas in Japanese species temperature is the actual cue (Table 4.1). Patterns connecting other species are much more obscure, primarily due to the lack of empirical data, including that for the widely studied diatematid species. On the other hand, experimental trials on Paracentrotus lividus have yielded confounding results, suggesting that neither photoperiod nor temperature is the proximal cue for gametogenesis, although stimulation when a specific temperature is reached cannot be ruled out.
3.3. Latitudinal effects A review of the extensive literature reveals that several species of echinoderms have been studied at a number of locations from a restricted or wide latitudinal range. Keeping in mind the possible drawbacks of single-site sampling discussed earlier (Section 1.5), a comparison of the results may provide an insight into the factors controlling reproduction in these species, including the holothuroid Cucumaria frondosa, which inhabits seasonally variable temperate/cold areas of the North Atlantic. Predictable and pronounced environmental fluctuations likely provide individuals with a time reference to synchronize gametogenesis and spawning. Cucumaria frondosa illustrates the high variability frequently observed in spawning periods among populations throughout a wide distribution range (Table 3.3). Two main factors follow particularly striking trends: (1) temperature increase and (2) phytoplankton bloom. The late spawning observed in the Arctic and in the St. Lawrence Estuary can be attributed to delayed temperature and phytoplankton increases in spring compared with locations in the NW Atlantic such as Newfoundland and Maine. Data from the NE Atlantic seem to confirm that C. frondosa uses a common set of factors to determine the spawning period, which occurs even earlier in European locations such as the North Sea, where waters typically warm up and become productive much earlier in the year than in most regions of the NW Atlantic.
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Similar conclusions were reached by Scheibling and Hatcher (2007) for the echinoid Strongylocentrotus droebachiensis over a wide part of its range. However, temperature did not follow any consistent pattern, although spawning seemed to occur during the phytoplankton bloom. Spawning generally occurs earlier in the season when conditions at a given site are favourable for an earlier plankton bloom, such as in Nova Scotia, New England and earlier yet along the coasts of northern Europe (Table 3.2). Massive spawning occurs in Cucumaria frondosa and Strongylocentrotus droebachiensis, gamete release from most individuals being completed within a few days/weeks, emphasizing the importance and efficacy of synchronization. However, there are several examples in equatorial and tropical regions where the patterns observed are quite different from the NW Atlantic situation and vary significantly between latitudes, apparently reflecting a shift in the reproductive strategy. Striking differences have been noted among populations of many species in the gametogenic cycle and spawning periodicity at lower latitudes. Some species have been studied across broad latitudinal ranges, where major seasonal differences in environmental variables occur, for instance, between the equator and the tropics. Along the coast of Mexico, the holothuroid Isostichopus fuscus has a restricted breeding season between July and September, when temperatures reach ca. 27 C (Herrero-Pe´rezrul et al., 1999). On the other hand, temperatures remain around 22–24 C year long along the coast of Ecuador, where I. fiscus spawns once a month, following the lunar cycle (Mercier et al., 2007). Limitation of reproductive activity to certain times of the year in areas with a pronounced annual temperature cycle, compared with prolonged breeding periods at temperature-stable latitudes, is a trend common to many echinoderm species, including Diadema setosum (Muthiga and McClanahan, 2007; Pearse, 1968a, 1970, 1974; Stephenson, 1934) and Holothuria scabra (Hamel et al., 2001). While trends in sea surface temperature are undeniably important, other factors may play a role in regulating echinoderm reproduction, as shown by a latitudinal study of Loxechinus albus in Chile, which revealed a complex pattern of reproductive periodicities that temperature alone could not explain (Vasquez, 2007). Furthermore, ripe individuals were detected throughout the year in some regions where spawning was seasonal. Yet again, this emphasizes the limitations of determining spawning events from measurements of gonad size and development, and the potential drawbacks of correlative studies (see Section 1). Finally, transplantation experiments with Strongylocentrotus intermedius around Japan revealed that the original gametogenic cycle can be retained in the new location, at least for some time (Agatsuma and Momma, 1988; Agatsuma et al., 1994), suggesting that temperature and day length regimes may not be acting directly on the reproductive cycle. Further experiments of this nature in other species and classes are required to confirm these preliminary observations.
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3.4. Heterospecific simultaneous spawnings Occurrences of simultaneous multi-species spawnings on the Great Barrier Reef in Australia (Babcock et al., 1992), in Palau (Scheibling and Metaxas, 2008), in an Irish marine lake (Minchin, 1992), on the eastern and western coasts of Canada (Himmelman et al., 2008; Pearse et al., 1988; Sewell and Levitan, 1992) and in the north-western USA (McEuen, 1988) have provided investigators with two very important elements: (1) a means to validate predictors of breeding periodicity established for these species using serial gonad samples or laboratory experiments; (2) a framework to examine the possible existence of an inter-specific communication mechanism that can stimulate or inhibit gamete release in given species on various time scales (i.e., determining how simultaneous the spawnings really are). Several studies have shown that when individuals of different species are observed to spawn ‘‘together’’ on the same day, they tend to do so one after the other, at intervals of a few minutes or hours, rather than at the same moment. It is likely that individuals respond to the same general environmental factors to determine the day of spawning, but that other mechanisms act on a shorter temporal scale to define the precise time of gamete release. While these mechanisms may still possess diel components (e.g., tides, light intensity), chemical communication is probably involved. Free-spawning by the sea star Acanthaster planci and two holothuroids, Pearsonothuria (¼Bohadschia) graeffei and Hothuria leucospilota, was observed in situ in Palau around the time of the full moon in May 2004 (Scheibling and Metaxas, 2008). Either the lunar cycle or the concurrent mass spawning of acroporid corals may have provided a cue. During a mass spawning event on the Great Barrier Reef (Australia), Babcock et al. (1992) observed that the sea cucumber Holothuria coluber only spawned when other species were also doing so, providing an apparent example of positive entrainment. Conversely, several other holothuroids (i.e., Bohadschia argus, Euapta godeffroyi, Stichopus chloronotus) spawned on the same night but not exactly at the same time (Babcock et al., 1992). This suggests a lagged heterospecific cueing of gamete release, possibly through the decreasing concentration of some sort of a chemical inhibitor in or around the gametes. The observations of Himmelman et al. (2008) on the east coast of Canada are consistent with this hypothesis, since they reported that the sea urchin Strongylocentrotus droebachiensis started spawning at 09:00 h and continued for an hour, followed by the brittle star Ophiura robusta at 10:00 h, followed by Ophiopholis aculeata at 10:45 h (5–10 min after O. robusta had stopped releasing gametes). We have observed the spring spawning of more than 25 species of marine invertebrates maintained in large communal flow-through tanks submitted to natural fluctuations of photoperiod and food supply in Newfoundland (eastern Canada). From daily records over 2 months, we
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noted that up to 11 species sometimes spawned in a single day, including several species of echinoderms, molluscs, and cnidarians, but peaks in gamete release never overlapped. The echinoderms contributing to these ‘‘epidemic’’ events included the holothuroids Cucumaria frondosa, Psolus fabricii and P. phantapus, the asteroids Crossaster papposus, Solaster endeca and Pteraster militaris and the echinoid Strongylocentrotus droebachiensis. In cases where we monitored subsequent embryonic development, progress appeared normal, suggesting that the slight temporal barrier was sufficient to prevent complete or massive wastage of gametes. However, this does not exclude the possibility that some gametes were lost to inter-specific cross-fertilization.
3.5. Final remarks There is a large body of evidence confirming the role of environmental cues in the reproduction of echinoderms, but with variable levels of certainty. Photoperiod has been shown experimentally to be the major factor responsible for synchronizing gamete development, or gametogenesis, in shallowwater sea urchins, sea cucumbers and sea stars. Temperature, food supply and the lunar cycle seem to be the other most important determinant factors. Moreover, a growing number of studies are providing strong evidence that secondary cues such as chemical compounds released by individuals into the seawater, with or without the assistance of pairing or aggregation among individuals of the same species, can fine-tune the process of gamete synthesis, without which the reproductive cycle cannot be properly coordinated. Precise spawning triggers have only rarely been demonstrated unequivocally, and have come from controlled laboratory trials, field studies or a combination of both. Much more common are correlative studies that make weaker approximations of spawning periods and underlying factors, due to long or irregular sampling intervals (see Section 1) and/or inaccurate measurements of relevant physical and biological variables. Furthermore, correct identification of spawning cues ideally requires the monitoring of numerous episodes of gamete release. Although very useful in identifying general responses to specific factors and possible inter-specific cues, multi-specific studies are uncommon. Important insights are provided by comparing various spawning observations in the field and through multi-year studies, which are rare. Additional consideration should be given to multi-level interactions in spawning induction. Indeed, a number of factors may be prerequisites in the sense that the proximate cue will not have any effect until a suite of underlying conditions are met. For example, a specific temperature range may be required for spawning to be triggered, either by phytoplankton, day length or lunar phases. Another largely unanswered question is how
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individuals in low density populations find compatible mature conspecifics and how they synchronize the release of their gametes on the finest scale. As pointed out in a review by Himmelman (1999), a large gap remains between research on endogenous pathways that lead to spawning and studies on the behavioural and ecological aspects of spawning. Furthermore, ultimate selective pressures are very rarely identified. In those rare cases where good correlations between abiotic factors and reproduction have been determined for a species, the spatial scale on which they apply is probably limited. Within-site variation is generally overlooked, although often recorded, suggesting that inter-individual synchrony in the reproduction of some species may occur only at very local scales, sometimes within small aggregates. Hence, more attention should be given to the presence/absence of depth-related or site-related variability, especially in eurybathyal or widely distributed species. For instance, depthrelated variation in reproductive activity has been demonstrated in the asteroid Henricia lisa (Mercier and Hamel, 2008) and the echinoids Strongylocentrotus purpuratus (Leahy et al., 1981) and Echinus esculentus (Nichols et al., 1985). The general trend is that seasonal peaks are more pronounced in shallower populations and either weak or absent in deeper populations. In contrast, Ferrand et al. (1988) observed low variation among populations of the echinoid Brissopsis lyrifera in the Mediterranean Sea, both males and females in all populations exhibiting the same distinct annual cycle at all depths studied from 60 to 930 m. Similarly, Hamel and Mercier (1996b, 1999) did not find differences in gametogenesis among individuals of the sea cucumber Cucumaria frondosa living at 10 and 110 m in the St. Lawrence Estuary (eastern Canada). Besides exposure to different local conditions (depth-related or otherwise), inter-individual variability may also be explained by significant contrasts between individual and population-level breeding periods. Species that display an annual breeding cycle may have short or long spawning periods and exhibit synchronous or asynchronous individual reproductive cycles throughout the year. In fact, for most ‘‘continuous’’ spawners, it is difficult to determine whether individuals exhibit continuous gametogenesis and synchronized spawning episodes or asynchronous cycles which overlap. Evidence of gamete development leading to repeated spawning events has been obtained from ophiuroids, including the regeneration of ripe gonads within 24 days in Amphiodia pulchella and the possible monthly spawning of 36% of the individuals in a population of Amphipholis gracillima (Hendler, 1991; Mladenov, 1983; Singletary, 1970). The latter pattern may provide evidence of rapid gamete synthesis, or longer overlapping cycles. For instance, between 1% and 35% of the individuals consistently spawn every month in equatorial populations of the holothuroid Isostichopus fuscus (Mercier et al., 2007). Since the gonads of individuals that do not spawn in a given month display a variety of maturity levels, including post-spawning, developing and
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193
mature gametogenic stages, the individual reproductive cycle appears to be longer than the monthly spawning periodicity observed at the population level, enabling populations to reproduce year round (Mercier et al., 2007). A similar trend occurs in the basket star Gorgonocephalus caryi, which displays an annual reproductive cycle and spawns for 6 months of the year, each animal spawning more than once (Patent, 1969). Asynchronous gonad development among individuals of a population has also been reported for the brittle star Ophiothrix suensoni (Mladenov, 1976), suggesting that continuous reproduction in this species is due to overlapping individual cycles. Another recurrent observation is that some species identified as year-round breeders may display more intense peaks of gamete release (Cunningham, 1977; Hamel et al., 2001; Rumrill, 1984; Rumrill and Pearse, 1985; Stancyk, 1974). An analogous situation may occur in annual breeders that exhibit gametogenic cycles longer than a year, generating major inter-annual variations in reproductive output and more substantial reproductive events at intervals of several years. Such multi-year patterns have been proposed for Antarctic echinoderm species (e.g., Brockington et al., 2007; Grange et al., 2004). It is clear that the reproductive periodicities of echinoderms cannot fit a single universal model, although they may be explained by a series of hypotheses, which are non-exclusive and can apply to the breeding cycles of other marine invertebrates (Olive, 1995): Non-functional hypotheses based on:
Physiology: seasonal reproduction is primarily the result of a speciesspecific physiological relationship between gamete synthesis and temperature (Orton’s rule). Energetic balance: seasonal reproduction is restricted to times of energy surplus. Genetic selection: seasonal reproduction is the result of selective pressure. Functional hypotheses based on: I. Fertilization success. Synchronous reproduction maximizes the concentrations of oocytes and sperm in the seawater at the same time and minimises gamete wastage. Synchronization maximizes outbreeding in species with external fertilization. II. Offspring survival. Reproduction occurs at times when environmental conditions are optimal for the survival and development of embryos, larvae and/or juveniles. Synchronous reproduction favours survival of larvae by ‘‘swamping’’ predation. Synchronous reproduction restricts over-dispersal and hence favours recruitment.
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All of these mechanisms may contribute to the maintenance of reproductive timing despite annual or other short-term oscillations in temperature or other environmental factors. It is probably reasonable to assume that where spawning cues exist, they may or may not be perceived in due course, or they may or may not be heeded for some unknown reason. This would help to explain temporal variations, due to absent or weak cues in certain months or years, and inter-individual asynchrony, resulting either from variable perception, especially in topographically inconsistent habitats, or from differences in physiological condition among individuals. The existence of ‘‘sentinel’’ members of a group (i.e., those more sensitive to environmental signals) that could subsequently transfer the message to conspecifics via pheromones has been evoked (Hamel and Mercier, 1996b, 1999). More research is required to assess the inter-individual effectiveness of known cues and the possible occurrence of ‘‘decisional’’ mechanisms that could influence the final response to these signals.
Appendix A1 Summary of correlations suggested for the exogenous control of gametogenesis in crinoids. GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Locality
Methods
Control
Source
Antedon bifida
English Channel (UK) English Channel (UK)
H, OSFD
Low oocyte productivity possibly linked to fluctuations in food supply Decreasing day length and sea surface temperature in August coincide with onset of oogenesis. Low oocyte productivity possibly linked to fluctuations in food supply Fluctuations in breeding period possibly due to variations in food availability Absence of genital pinnules may be related to cyclic reproduction in a marginal environment depending on seasonal food supply Onset of gametogenesis in early fall correlated with increasing temperature and shortening day length Early stages of gametogenesis possibly influenced by decreasing day length and surface temperature in the fall
Nichols (1991)
Onset of oogenesis in winter coincides with lowest water temperature. Gonad differentiation in last week before spawning possibly triggered by full or new moon
Holland (1981a)
Antedon bifida
H, OSFD
Florometra serratissima Hyocrinus foelli
West coast (Canada) Horizon Seamount (deep sea Eastern Pacific)
H, OSFD, thickness of spermatogenic layer Anatomical description
Nemaster rubiginosa
Jamaica
H, MI, OSFD
Oxycomanthus japonicus
Japan
Oxycomanthus japonicus
Japan
H, OSFD, ovarian lumen and male germinal cells, Volume fluctuation in oocytes Model
Nichols (1994)
Mladenov (1986) Roux and Pawson (1999)
Mladenov and Brady (1987)
Holland (1991); Holland et al. (1975)
195
196
Appendix A2 Summary of correlations suggested for the exogenous control of spawning in crinoids. GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Methods
Control
Source
Antedon bifida
UK
Abrupt change in temperature
Dimelow (1958)
Heterometra savignii Lamprometra klunzingeri
Red Sea
Laboratory observations –
Lunar cycle
Field observations
Simultaneous spawning at dusk, suggesting that the declination of the moon acts as a cue, or pheromonal exchange between individuals Seasonal repeated (i.e., trickle) spawning in October–March correlated with short day lengths Once a year in October at first or last quarter of moon, at neap tide. Good correlation with tidal phase, although individuals removed from tidal influence for 7–10 days prior to spawning still spawn on cue with those in the field As temperature drops below 22 C. High temperature days before spawning correlated with poor or aborted gamete release. Temperature influences choice of first or last quarter moon. A lower declination of the moon correlates well with non-spawning years. Solar time responsible for specific time or date Moonlight entrains a biological rhythm
Mortensen (1938) Fishelson (1968)
Red Sea
Nemaster rubiginosa Jamaica
H, MI, OSFD
Oxycomanthus japonicus
Japan
Field observations, H, laboratory observations
Oxycomanthus japonicus
Japan
Field observations
Oxycomanthus japonicus
Japan
Model
Mladenov and Brady (1987) Dan and Dan, (1941); Dan and Kubota, (1960) Kubota (1981)
Holland (1981a)
Appendix A3 Summary of correlations suggested for the exogenous control of gametogenesis in ophiuroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution
197
Species
Location
Methods
Control
Source
Acrocnida brachiata
Douarnenez Bay (France)
GI, OSFD (limited)
Bourgoin and Guillou (1990)
Amphiodia occidentalis
Monterey Bay (USA)
Amphipholis kochii
Hokkaido ( Japan)
Amphiura filiformis
Galway Bay (Ireland)
F, gonad size/ ripeness, reproductive effort Cell counts in testis, H. Under natural and experimental conditions. Spermatogenesis only. H, MI, OSFD
Temperature differences may account for slight asynchrony in gonad cycle between intertidal and subtidal populations Influence of food supply also suggested: if not enough food, gonad growth does not occur Seasonal changes in temperature (increasing) and perhaps other factors From March to June, duration of spermatogenesis is influenced by temperature irrespective of time of collection
Bowmer (1982)
Asteroporpa annulata
Gulf of Mexico (FL, USA)
Gonad growth linked with annual rise in temperature; beginning of annual maturation coincides with spring plankton bloom Gametogenesis could be entrained by photoperiod and later gametogenic stages could coincide with maximum food availability
H
Rumrill (1984)
Yamashita and Iwata (1983)
McClintock et al. (1993)
(continued)
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Appendix A3
(continued)
Species
Location
Methods
Control
Source
Astrobrachion constrictum
Fiordland (New Zealand)
GI, H, MI
Hemipholis elongata
Mississippi Sound (USA) Mississippi Sound (USA)
GI
Increased gametogenic activity correlated with increasing temperature Changes in GI correlated with change in temperature Near-bottom temperature fluctuation influences gametogenesis Timing of gametogenic proliferation possibly influenced by increasing temperature and day length; however, renewal of gametogenesis could be the result of empty gonad Fluctuation may be due to pulses of phytodetritus falling to the deepsea floor
Stewart and Mladenov (1995) Valentine (1991a)
Microphiopholis atra
GI
Ophiactis resiliens
South-east Australia
H
Ophiocten hastatum
Rockall Trough and Porcupine Seabight (deep sea NE Atlantic) Massachusetts (USA)
OSFD
Bermuda (deep sea NW Atlantic)
Presence of oocytes, size of gonad
Ophioderma brevispinum
Ophiura ljungmani Ophiomusium lymani
GI, H, OSFD
Initiation of gametogenesis in late summer and winter with acceleration in May and June could be regulated by temperature fluctuations Sinking of particles from primary surface production could modulate seasonal reproduction
Valentine (1991a)
Falkner and Byrne (2003)
Gage et al. (2004)
Hendler and Tyler (1986)
Schoener (1968)
Ophiomusium lymani
Rockall Trough (deep sea NE Atlantic) Conch Key (FL, USA)
F. H. OSFD
Ophionotus victoriae
Antarctic Peninsula
F, GI, H, MI, OSFD
Ophiopteris papillosa
Monterey Bay (USA)
F, gonad size/ ripeness, reproductive effort
Ophiothrix fragilis
Strait of Dover (France)
MI, OSFD
Ophiothrix fragilis
Netherlands
GI, H, MI
Ophionereis olivacea
H, OSFD
199
Downward flux of food particles from the surface regulates reproductive cycle Succession of various oocyte maturation stages may be regulated by temperature and day length cycles Clear inter-annual reproductive effort may be related to nutritional conditions (organic sedimentation event) depending on ice cover and thickness. Oocyte size correlated with temperature pattern Seasonal changes in temperature (decreasing) and perhaps other factors. Predictable food availability may initiate gametogenesis Year-round reproductive activity with maxima coinciding with highest temperature, longest photoperiod and phytoplankton bloom. GI higher when temperature ca. 17 C Growth and maturation linked to increase of temperature and photoperiod
Gage and Tyler (1982) Byrne (1991)
Grange et al. (2004)
Rumrill (1984)
Davoult et al. (1990)
Morgan and Jangoux (2002) (continued)
Appendix A3
(continued)
200
Species
Location
Methods
Control
Source
Ophiothrix fragilis
Pas-de-Calais (France)
H, MI
Gounin and Richard (1992)
Ophiothrix fragilis
GI
Ophiothrix spiculata
English Channel (France) Monterey Bay (USA)
Ophiura albida
Bristol Channel (UK)
Ophiura ljungmani
Rockall Trough (deep sea NE Atlantic)
Period of increasing temperature, phytoplankton and photoperiod may be determinant factor during the maturation process Temperature and food availability may explain the cycle Seasonal changes in temperature (increasing) and perhaps other factors Oocyte proliferation but low gonad production correlated with lowest feeding activity. Maximum gonad production during peak food consumption and day length Spring–summer surface production may provide energy later in season by partially sinking to the bottom, helping population to synchronize vitellogenesis
F, gonad size/ ripeness, reproductive effort H, MI, OSFD
OSFD
Lefebvre et al. (1999) Rumrill (1984)
Tyler (1977)
Tyler and Gage (1980b)
Appendix A4 Summary of correlations suggested for the exogenous control of spawning in ophiuroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Methods
Control
Source
Acrocnida brachiata
GI, OSFD
Related to temperature
Amphipholis kochii
Douarnenez Bay (France) Hokkaido ( Japan)
Related to temperature
Amphipholis kochii
Hokkaido ( Japan)
Sudden change in temperature
Yamashita (1985)
Amphipodia occidentalis
Monterey Bay (USA) Villefranche Bay (France) Scandinavia
Increasing temperature and late phytoplankton blooms in spring End of summer; correlated with increasing temperature Males that spawn first induce females to spawn In June–September with peak in August (warmest months) In fall and early winter; may be correlated with decreasing temperature Induced by decreasing temperature in May–June Occurs in both species in summer and early fall when salinity is high or very low May be influenced by decreasing temperature and day length Spawning spontaneously as well as after temperature and light shocks
Rumrill (1984)
Amphiura chiajei
Spawning induction (laboratory) Laboratory observations F, gonad size/ripeness, reproductive effort H, larvae in the field, OSFD –
Bourgoin and Guillou (1990) Yamashita (1983, 1985)
Amphiura filiformis Amphiura filiformis
Galway Bay (Ireland) Gulf of Mexico (FL, USA)
OSFD, MI, H
H, MI, GI
Microphiopholis atra, Hemipholis elongata
Fiordland (New Zealand) Mississippi Sound (USA)
Ophiactis resiliens
SE Australia
H
Ophiactis resiliens
Australia
Laboratory observations
Asteroporpa annulata
Astrobrachion constrictum
H
GI
Fenaux (1970) Mortensen (1920b) Bowmer (1982) McClintock et al. (1993) Stewart and Mladenov (1995) Valentine (1991b)
Falkner and Byrne (2003) Selvakumaraswamy and Byrne (2000)
201
(continued)
202
Appendix A4 (continued) Species
Location
Methods
Control
Source
Ophiocantha bidentata Ophiocoma dentate, Ophiocoma scolopendrina
White Sea Taiwan
H Spawning trials
Kaufmann (1974) Chang (1999); Soong et al. (2005)
Ophioderma brevispinum
Massachusetts (USA)
GI, H, OSFD
Ophioderma rubicundum
Gulf of Mexico (USA)
Field observations
Ophioderma squamosissimum
Gulf of Mexico (USA)
Field observations
Ophionereis fasciata
Leigh (New Zealand)
Ophionereis olivacea
Conch Key (FL, USA)
Laboratory observations H, OSFD
Ophiopholis aculeata
Maine (USA), Newfoundland (Canada) White Sea
GI, gonad volume, H
Maximum temperature Ovary homogenate induced conspecific, competent males to spawn but had no effect on conspecific females. Testis homogenate had no effect Temperature may be the critical exogenous factor Occurred at night a few days after full moon Massive event, after August full moon, in the evening In January with temperature and light shocks In January–February, could be correlated with temperature and day length cycles During decreasing temperature period
Mileikovsky (1960)
Woods Hole (MA, USA) Gulf of St. Lawrence (QC, Canada)
Laboratory work
When temperature between 5 and 5.6 C Temperature shock
Ophiopholis aculeata Ophiopholis aculeata Ophiopholis aculeata
–
Field observations, GI
Massive events coincided with major increase in temperature in summer
Hendler and Tyler (1986) Hagman and Vize (2003) Hagman and Vize (2003) Selvakumaraswamy and Byrne (2000) Byrne (1991)
Blake (1978)
Costello and Henley (1971) Himmelman et al. (2008)
Ophiopteris papillosa
California (USA)
Ophiothrix caespitosa
Australia
Ophiorhrix oerstedi
Barbados
Ophiothrix fragilis
Strait of Dover (France)
Bimodal OSFD, larvae in the field
Ophiothrix fragilis
Netherlands
GI, H, spawning induction
Ophiothrix fragilis
Netherlands
GI, H, MI
F, gonad size/ripeness, reproductive effort Laboratory observations Laboratory observations
Between January and March correlated with minimum mean temperature In July and December, spontaneously at collection Hypotheses: (1) exposure to artificial illumination beyond sunset; (2) exposure to a brief period of temperature fluctuation during transport; (3) handling during collection; (4) overcrowding in finger bowls; (5) agitation of water caused by air stones Same individual believed to spawn twice. Also, one large and 3 small recruitment pulses observed every year for 2 years. The main event in June–October. Indicates year-round reproductive activity with peak during highest temperature, longest photoperiod and phytoplankton bloom When temperature >16 C and long days (>15 h); also strong current and induction by release of gametes from congeners (generally males) A mix of temperature increase (>16 C) and conspecific spawning (synergistic effects) induces and propagates spawning
Rumrill (1984) Selvakumaraswamy and Byrne (2000) Mladenov (1979)
Davoult et al. (1990); Lefebvre and Davoult (2000)
Morgan and Jangoux (2002)
Morgan and Jangoux (2002)
203
(continued)
204
Appendix A4
(continued)
Species
Location
Methods
Control
Source
Ophiothrix fragilis
Pas-de-Calais (France)
H, MI
Ophiothrix schayeri
Australia
Laboratory observations
Gounin and Richard (1992) Selvakumaraswamy and Byrne (2000)
Ophiothrix spiculata
California (USA)
F, gonad size/ripeness, reproductive effort
Ophiothrix spongicola
Australia
Ophiura albida
Bristol Channel (UK)
Laboratory observations H, MI, OSFD
Ophiura albida Ophiura albida Ophiura gracilis
Oresund (Denmark) North Sea NE Atlantic (deep sea)
– Larvae in the field Larvae in the field
Ophiura robusta
Gulf of St. Lawrence (QC, Canada) Bristol Channel (UK)
Field observations, GI
In summer when maximum temperature is reached Various times of the year, spontaneously and after temperature change and stimulation by light In spring, correlated with increasing temperature and late phytoplankton blooms From March to June, spontaneously and after stimulation by light In May and early June, when temperature >12.5 C When temperature >12.5 C When temperature >12.5 C Correlation between presence of phytodetritus from surface primary production and larvae Massive events coincided with major increase in temperature in summer From June to November when temperature reaches 12.5 C, but also in coldest month (7.25 C)
Ophiura texturata
H, MI, OSFD
Rumrill (1984)
Selvakumaraswamy and Byrne (2000) Tyler (1977) Thorson (1946) Rees (1954) Sumida et al. (2000)
Himmelman et al. (2008) Tyler (1977)
Appendix A5 Summary of correlations suggested for the exogenous control of gametogenesis in holothuroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Gametogenesis
Control
Source
Actinopyga echinites
New Caledonia
GI, MI, OSFD, gonad morphology
Conand (1982)
Actinopyga echinites
New Caledonia
GI
Actinopyga echinites
New Caledonia
GI, gonad morphology
Actinopyga mauritiana
New Caledonia
GI, gonad morphology
Actinopyga mauritiana
Guam
GI, gonad morphology
Actinopyga mauritiana
Solomon Islands
GI, H, tubule length and diameter
Amperima rosea
Porcupine Abyssal Plain (NE Atlantic, deep sea) Galway Bay (Ireland)
GI, H, OSFD
Temperature increase corresponds to growing and maturing phases Temperature decrease corresponds to post-spawning or regression Onset of gametogenesis linked to increase in temperature Temperature seems to modulate gametogenesis with resting period during coolest period of the year and maturation stage when water is warming up Temperature seems to modulate gametogenesis with the resting period during coolest period of the year and maturation stage when water is warming up Variation of reproductive peak between years dependent on La Nin˜a event Annual cycle with early phase of gametogenesis when day length decreasing Flux of phytodetritus from surface productivity High oxygen concentrations and low temperature coincide with active gametogenesis. Feeding in warmer months build-up nutrients in winter months
Costelloe (1985)
Aslia lefevrei
GI, H, OSFD
Conand (1989) Conand (1993b)
Conand (1993b)
Hopper et al. (1998) Ramofafia et al. (2001) Wigham et al. (2003a)
205
(continued)
Appendix A5
(continued)
206
Species
Location
Gametogenesis
Control
Source
Cucumaria frondosa
St. Lawrence Estuary (QC, Canada)
Initiation of gametogenesis correlated with increased photoperiod; acceleration of synthesis in spring coincides with increase in temperature and food availability
Hamel and Mercier (1996a)
Cucumaria frondosa
St. Lawrence Estuary (QC, Canada)
Body wall thickness, energy contents of various organs, GI, gonad morphology, H, intestinal-muscle band-respiratory tree indices, intestinal contents, tubule diameter Laboratory experiments
Hamel and Mercier (1996b, 1999)
Cucumaria frondosa
Passamaquoddy Bay (NB, Canada)
Chemical communication among congener to fine-tune progression of gametogenesis toward spawning; body wall mucus is the apparent carrier of the active molecule Feeding has little influence on reproductive cycle
Gamete dry weight, GI, gonadal tubule surface area, H, haemal fluid space, OSFD Comparison of different methods
Ekmocucumis steineni
Weddell Sea (Antarctica)
F, relative gonad weight
Holothuria atra
Fiji
GI, gonad morphology, OSFD, sperm activity
Haemal space increases greatly after spawning in May–June and decreases rapidly by September No correlation found, but data suggest a potential role for environmental factors in control of reproductive biology Gametogenesis correlated with temperature fluctuation (onset in August; ripe gametes around September)
Singh et al. (2001)
Gutt et al. (1992)
Seeto (1994)
Holothuria (¼Microthele) fuscogilva Holothuria fuscogilva
New Caledonia
Holothuria fuscogilva, Holothuria fuscopunctata Holothuria fuscopunctata
New Caledonia
Gamete feature, GI, gonad morphology GI, H, gonad morphology, tubule length and diameter GI
New Caledonia
GI, gonad morphology
Holothuria leucospilota
Hong Kong (China)
Calorimetry, GI, H
Holothuria (¼Microthele) nobilis
New Caledonia
Gamete feature, GI, gonad morphology
Holothuria scabra
Stradbroke Island (Australia) Southwest Sulawesi (Indonesia)
GI, H, OSFD
Holothuria scabra
Holothuria scabra
Solomon Islands
Calatagan (Philippines)
GI, H MI
GI, H, OSFD
Annual reproductive cycle correlated with seasonal temperature change Onset of gametogenesis possibly as photoperiod decreases
Conand (1981)
Onset of gametogenesis linked with increase in temperature
Conand (1989)
Temperature seems to modulate gametogenesis, the resting period occurring during the coolest period of the year and the maturation stage when water is warming up Initiation of gametogenesis when temperature increasing Maturing individuals between January and May correlated with annual temperature cycle Combination of photoperiod, temperature and food availability Post-spawning accentuated in two phases: one during dry season (temperature increase) and second at beginning of rainy season (temperature decrease) Reproductive pulse in May–June as temperature falls to annual minimum and salinity decreases due to rainy season. Increase in temperature and salinity (November–January) corresponds to another pulse
Conand (1993b)
Ramofafia et al. (2000)
Ong Che (1990) Conand (1981)
Morgan (2000b) Tuwo (1999)
Ong Che and Gomez (1985)
207
(continued)
Appendix A5
(continued)
208
Species
Location
Gametogenesis
Control
Source
Holothuria scabra
India
GI
Holothuria scabra
Solomon Islands
Krishnaswamy and Krishnan (1967) Battaglene (1999a)
Holothuria scabra
Madagascar
Sapwning induction (laboratory) GI, H, MI, OSFD
Holothuria scabra
New Caledonia
GI, gonad morphology
Holothuria scabra
Solomon Islands
Laboratory observations (outdoor tanks)
Holothuria scabra Holothuria scabra versicolor Holothuria scabra versicolor
New Caledonia
GI
Salinity variation may be modulating reproductive cycle Both salinity and temperature may regulate reproductive cycle Gametogenesis not synchronous in entire population. Maturity reached in November–April. Temperature may regulate gametogenesis, mainly in females (other factors like rainy period could also have an effect) Temperature weakly modulating gametogenesis with resting period during coolest period of year and maturation stage as water is warming up Lunar phase plays a role in pre-spawning pairing behaviour and gametogenic synchronicity Onset of gametogenesis when temperature increases
New Caledonia
GI, gonad morphology
Wrightsville (NC, USA)
H, OSFD
Leptosynapta tenuis
Temperature weakly modulating gametogenesis with resting period during coolest period of year and maturation stage as water is warming up Oocyte diameter peaked in May–June and August–October. In July and August there is no gametogenesis. Could be temperature fluctuation (very poor, no correlation). Absence of reproductive individuals in midsummer during highest temperature
Rasolofonirina et al. (2005)
Conand (1993b)
Mercier et al. (2000a) Conand (1989)
Conand (1993b)
Green (1978)
Parastichopus (¼Stichopus) californicus
Woodlands Bay (BC, Canada
GI, gonad volume displacement, H
Peniagone vignoni
West Antarctic Peninsula (deep)
F, GI, H, OSFD
Protelpidia murrayi
West Antarctic Peninsula (deep) St. Lawrence Estuary (QC, Canada)
F, GI, H, OSFD
Stichopus chloronotus
Straits of Malacca (Malaysia)
GI, H, OSFD
Stichopus herrmanni
Kish Island (Iran)
GI, H
Stichopus japonicus
Southern Hokkaido ( Japan)
GI, H
Stichopus mollis
NE New Zealand
GI, H, MI, OSFD
Psolus fabricii
GI, H, OSFD, tubule diameter
209
Largest gonad in June–July and smallest in November–December. Temperature fluctuation and stratification? Vitellogenetic oocytes present year round but more intense production during greater food input from phytodetritus pulses Onset of vitellogenesis coincides with phytodetritus pulse Initiation of gametogenesis possibly related to increasing photoperiod. Acceleration of gamete synthesis later in spring as temperature and food availability increase Rapid development of gametogenesis with increase in salinity and chlorophyll a Active stage of gametogenesis coincides with increasing photoperiod In November, gametogenesis resumes and continues to increase until next spawning. Could be regulated by temperature Environmental factors may explain the difference observed between two latitudes/populations studied. Temperature and photoperiod may regulate gametogenesis
Cameron and Fankboner (1986) Galley et al. (2008)
Galley et al. (2008) Hamel et al. (1993)
Tan and Zulfigar (2001) Tehranifard et al. (2006) Tanaka (1958)
Sewell (1992)
(continued)
210
Appendix A5
(continued)
Species
Location
Gametogenesis
Control
Source
Stichopus mollis
NE New Zealand
GI, H
Sewell and Bergquist (1990)
Stichopus variegatus
New Caledonia
GI, gonad morphology
Stichopus variegatus
New Caledonia
GI, gonad morphology
Stichopus variegatus
New Caledonia
GI
Thelenota ananas
New Caledonia
Gamete feature, GI, gonad morphology
Thelenota ananas
New Caledonia
GI
Thelenota ananas
New Caledonia
GI, gonad morphology
Lower temperature in second year of the study prolonged reproductive cycle. Extended reproductive season could be due to El Nin˜o Maturing seems to occur during temperature increase, post-spawning during cooling period and a long resting stage during cool season Temperature seems to modulate gametogenesis with resting period during coolest period of year and maturation stage when water is warming up Onset of gametogenesis linked to increase in temperature Maturing individuals noted in October–December. GI declines from January–June followed by low values in July–October (correlated with annual temperature cycle) Onset of gametogenesis with increase in temperature Temperature seems to modulate gametogenesis with resting period during coolest period of year and maturation stage when water is warming up
Conand (1993a)
Conand (1993b)
Conand (1989) Conand (1981)
Conand (1989) Conand (1993b)
Appendix A6 Summary of correlations suggested for the exogenous control of spawning in holothuroids. This table completes the field observations (Table 3.1) for which supplementary data are available. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Methods
Control
Source
Actinopyga echinites Actinopyga echinites
Taiwan New Caledonia New Caledonia
Phytoplankton production In January–February with warm-water temperature (peak) In January–February during warm season
Chao et al. (1995) Conand (1982)
Actinaupyga echinites Actinopyga mauritiana
New Caledonia
Actinopyga mauritiana
Solomon Islands
GI, H GI, MI, morphology of tubules, OSFD GI, morphology of gonad GI, morphology of gonad GI, H, tubule length and diameter
Afrocucumis africana
Taiwan
GI, H
Apostichopus (=Stichopus) japonicus Apostichopus (=Stichopus) japonicus Aslia lefevrei
Southern Hokkaido ( Japan) Japan
GI, H
Galway Bay (Ireland)
Artificial induction (laboratory) GI, H, OSFD
Bohdschia argus, Bohadschia marmorata
Solomon Islands
Laboratory experiments
Caudina chilensis
Japan
Laboratory experiments
In December–January during warm season In October–December. Correlation during increasing temperature and day length Gametes released at beginning of warm months (March–April), during spring plankton production and temperature increase From middle June for 2 months. May be related to temperature Thermal shock (5–6 C increase) and addition of sperm Between end of February and beginning of April (correlated with temperature and light cycles) Perivisceral coelomic fluid involved in inducing and spreading spawning among congeners During high tide in the evening
Conand (1993b) Conand (1993b) Ramofafia et al. (2001) Chao et al. (1995)
Tanaka (1958) Yanagisawa (1995) Costelloe (1985)
Mercier and Hamel (2002) Inaba (1930)
211
(continued)
Appendix A6 (continued) 212
Species
Location
Methods
Control
Source
Cucumaria frondosa Cucumaria frondosa
Newfoundland (Canada) Maine (USA)
Related to phytoplankton bloom Related to phytoplankton bloom in spring
Coady (1973) Jordan (1972)
Cucumaria frondosa
St. Lawrence Estuary (QC, Canada)
GI, gonad volume, H GI, gonad volume, H, larvae in the field, MI Field observations and experiments
Hamel and Mercier (1995a)
Cucumaria miniata
San Juan Archipelago (WA, USA) San Juan Archipelago (WA, USA) Intertidal zone (CA, USA) Intertidal Aoshima Island ( Japan)
Field and laboratory observations Field and laboratory observations GI
Holothuria atra
New Caledonia
Holothuria atra
Solomon Islands
GI, morphology of gonad Laboratory experiments
Massive event in mid-June. Phytoplankton bloom seems to induce male; but female seems to react to presence of sperm; rapid temperature change also seems to play a role In March–May with phytoplankton bloom. Males spawn first In February after 2 days of sun. Males spawn first In January, could be linked to aggregative behaviour Low light intensity and possibly temperature may be inducers. Spawned in December (laboratory observation) from midnight to 04:00 h In correlation with warm season
Holothuria cinerascens
Taiwan
GI, H
Cucumaria populifera Cucumaria pseudocurata Eupentacta chronhjelmi
GI, H, laboratory observations, OSFD
Perivisceral coelomic fluid involved in inducing and spreading spawning among congeners In April–June with phytoplankton production
McEuen (1986) McEuen (1986) Rutherford (1973) Catalan and Yamamoto (1994)
Conand (1993b) Mercier and Hamel (2002) Chao et al. (1995)
Holothuria difficilis
Taiwan
GI, H
Holothuria forskali
Glenan Archipelago (France) Solomon Islands
GI, H, OSFD, tubule classes GI, H, tubule morphology-lengthdiameter
New Caledonia
Gamete feature, GI, gonad morphology GI, gonad morphology
Holothuria fuscogilva
213
Holothuria (¼Microthele) fuscogilva Holothuria fuscopunctata
New Caledonia
Holothuria leucospilota
Cook Islands
GI, gonad morphology, H
Holothuria leucospilota
Taiwan
GI, H
Holothuria leucospilota
Solomon Islands
Laboratory experiments
Holothuria (¼Microthele) nobilis Holothuria nobilis
New Caledonia New Caledonia
Gamete feature, GI, gonad morphology GI, gonad morphology
Holothuria scabra
Solomon Islands
Laboratory and field observations
Holothuria scabra
India
Laboratory experiments
Holothuria scabra
Solomon Islands
GI, H, tubule length and diameter
In August–September with phytoplankton production In April with increase in temperature Successful induction in the laboratory: thermal shock could be similar to short-term heat stress in situ: some results with dried alga Schizochytrium sp. In March–April during warmest months Between December and February during warm season Gametogenesis correlated with increasing temperature and longer days In June–September with phytoplankton production Perivisceral coelomic fluid involved in inducing and spreading spawning among congeners In May–July during coldest months Between June and August during cool season Pre-spawning aggregation and spawning seem to be linked to moon phases (full moon) Change of water and thermal shock (water temperature increase by 5 C) Peak of activity weakly linked to dry season, increased day length and temperature
Chao et al. (1995) Tuwo and Conand (1992) Ramofafia et al. (2000)
Conand (1981) Conand (1993b) Drumm and Loneragan (2005) Chao et al. (1995) Mercier and Hamel (2002) Conand (1981) Conand (1993b) Mercier et al. (1999, 2000a) James (1996) Ramofafia et al. (2003) (continued)
Appendix A6 (continued) 214
Species
Location
Methods
Control
Source
Holothuria scabra
South Sulawesi (Indonesia)
GI, H, MI
Tuwo (1999)
Holothuria scabra
Heron Island (Australia)
GI, H
Holothuria scabra
Anjuna (India)
Gonad morphology
Two main spawning periods; one during dry season and increase in temperature, the other during rainy season and decrease in temperature Gonad maturity peak twice a year in early winter and summer. Loosely linked to temperature Weak correlation with temperature and salinity
Holothuria scabra
India
GI
Holothuria scabra
India
Holothuria scabra
New Caledonia
Artificial spawning induction (laboratory) GI, gonad morphology
Holothuria scabra versicolor
New Caledonia
GI, gonad morphology
Holothuria tubulosa
Adriatic Sea
H, OSFD
Isostichopus fuscus
Coast of Ecuador
Laboratory experiments
Leptosynapta tenuis
Wrighsville (NC, USA)
H, OSFD
Opheodesoma grisea
Taiwan
GI, H
Salinity may be responsible for onset of breeding Thermal shock (increasing temperature by 5 C) From December to February and in August–September. During warm season except for August–September episode which occurs when water starts to warm up after the cool season From November to February during warm season When temperature increases and reaches 22–26 C Cycle of lunar luminance determines periodicity In spring and fall. Absence of reproductive individuals at highest temperatures in summer In June–July during phytoplankton production
Harriott (1982)
Jayasree and Bhavanarayana (1994) Krishnaswamy and Krishnan (1967) James (1994a); James et al. (1994a) Conand (1993b)
Conand (1993b) Despalatovic et al. (2004) Mercier et al. (2004, 2007) Green (1978)
Chao et al. (1995)
Parastichopus (¼Stichopus) californicus
San Juan Archipelago (WA, USA)
Laboratory observations
Patinapta ooplax
Southern Japan
GI, H, OSFD
Patinapta taiwaniensis
Taiwan
GI, H
Polycheira rufescens
Taiwan
GI, H
Pseudocnus lubricus (¼Cucumaria lubrica)
San Juan Archipelago (WA, USA)
Field and laboratory observations
P. lubricus
Puget Sound (USA)
Field and laboratory observations
Psolus chitonoides
San Juan Archipelago (WA, USA)
Field and laboratory observations
Psolus fabricii
St. Lawrence Estuary (QC, Canada)
GI, H, OSFD, tubule diameter
215
In April–May and July after successive sunny days and increase in air temperature. Males spawn first From mid-July to end of August once a year; gamete released in evening; occurs only some individuals of population every new and full moon In June–July with phytoplankton production In April and June. Gametes released at beginning of warm months, correlated with spring plankton production and temperature increase Males spawn first. In December–January after several days of sun and phytoplankton bloom From mid-day to early evening during periods of low or zero tidal current. Males spawn first. Temperature and day length may set months each year. Tides and time of day may be proximate factors In March–June after a sunny day or a series of sunny days (individuals maintained in darkness delay spawning for several weeks; when placed in sun, spawning occurs in 30 min). Males spawn first In early summer ( July). Possible role of phytoplankton bloom and decrease in freshwater runoff
McEuen (1986)
Kubota (2000)
Chao et al. (1995) Chao et al. (1995)
McEuen (1986)
Engstrom (1982)
McEuen (1986)
Hamel et al. (1993)
(continued)
Appendix A6 (continued) 216
Species
Location
Methods
Control
Source
Stichopus chloronotus
GI, H
Stichopus herrmanni
Straits of Malacca (Malaysia) Kish Island (Iran)
GI, H
Stichopus variegatus Stichopus variegatus Synapta maculate
New Caledonia New Caledonia Taiwan
GI, gonad morphology GI, tubule diameter GI, H
Tan and Zulfigar (2001) Tehranifard et al. (2006) Conand (1993b) Conand (1993a) Chao et al. (1995)
Thelenota ananas
New Caledonia
Thelenota ananas
New Caledonia
Gamete feature, GI, gonad morphology GI, gonad morphology
Thyone briareus
Woods Hole (MA, USA)
Laboratory observations
With slight increase in temperature and chlorophyll a In summer. Temperature may be the trigger In December and January (warm season) In December–January (warm season) In June and July with phytoplankton production From December to April with a peak during three warmest months From January to March during warm season In June for several days, between 08:00 and 10:00 h. Temperature manipulation induces spawning
Conand (1981) Conand (1993b) Colwin (1948)
Appendix A7 Summary of correlations suggested for the exogenous control of gametogenesis in asteroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Methods
Control
Source
Asterias amurensis
Derwent River estuary (Australia)
GI, H
Byrne et al. (1997)
Asterias rubens
Zeeland (Netherlands)
Field observations, laboratory experiments
Asterias rubens
North and Baltic Seas
OSFD
Asterias rubens (¼vulgaris) Astrobrachion constrictum
New Hampshire (USA)
H, laboratory experiments, OSFD GI, H, MI, OSFD
Reproductive cycle apparently under photoperiodic control; temperature could play a role Photoperiod induces gametogenesis, however, once gametogenesis has begun, static environment and lack of food will not prevent gonad from reaching maturity Influence of salinity on rate of gonad development (brackish conditions inhibit process) Controlled by photoperiod
Coscinasterias muricata
Coscinasterias tenuispina
Doubtful Sound (New Zealand) Port Phillip Bay (Australia)
Brazil
GI, OSFD, progesterone levels, pyloric caecum index
GI
217
Correlated with increasing temperature Reproductive cycle of female influenced by progesterone, which in turn appears to be coordinated by changes in photoperiod. Months with maximum and minimum temperature mark onset of gametogenesis and spring spawning event. Temperature and photoperiod may influence key periods of reproductive cycle Gonad development weakly correlated with temperature
Bouland and Jangoux (1988)
Schlieper (1957)
Pearse and Walker (1986) Stewart and Mladenov (1995) Georgiades et al. (2006)
Alves et al. (2002) (continued)
Appendix A7
(continued)
218
Species
Location
Methods
Control
Source
Cosmasterias lurida
Argentina
GI, H, OSFD
Ctenodiscus crispatus
Maine (USA)
GI, H, OSFD
Pastor-de-Ward et al. (2007) Shick et al. (1981)
Dytaster grandis
Porcupine Abyssal Plain (deep sea NE Atlantic) Procupine Seabight (deep sea NE Atlantic) Continental slope (deep sea NL, Canada)
OSFD
Possible correlation of gametogenesis with photoperiod Continuous reproduction with peaks possibly explained by pulses of phytodetritus to sea floor Availability of labile organic matter may fuel vitellogenesis Role of phytodetritus on gonadal growth
Benitez-Villalobos et al. (2007)
Populations at 600 m have seasonal cycles possibly related to temperature (and light?). Population at 1300 m shows continuous presence of maturity stage and no correlation with environmental factors Very rapid gametogenesis toward maturity in late fall within a single lunar cycle (probably barometric pressure change) Reproductive cycle influenced by food quantity and quality
Mercier and Hamel (2008)
Normal feeding in summer is a prerequisite for subsequent gametogenesis
Smith (1971)
Henricia abyssicola
Henricia lisa
F, GI, gonad morphology, H, OSFD GI, H, laboratory observations, OFSD
Hippasteria phrygiana
Continental slope (deep sea NL, Canada)
GI, H, OSFD
Hyphalaster inermis
Porcupine Abyssal Plain, Madeira Abyssal Plain and NW African Slope Monterey Bay (CA, USA)
GI, H, OSFD
Leptasterias pusilla
Laboratory work
Tyler et al. (1990)
(Baillon, Hamel and Mercier, unpublished data) Ramirez-Llodra et al. (2002)
Leptasterias sp.
Gonad morphology, H
Luidia clathrata
Pacific Grove (CA, USA) Block Island Sound (RI, USA) Tampa Bay (FL, USA)
Luidia clathrata
Tampa Bay (FL, USA)
GI
Odontaster validus
McMurdo Sound (Antarctica)
GI, H, oocyte abundance and volume, OSFD
Odontaster validus
Balleny Islands (deep, Antarctica)
H OSFD
Odontaster validus
McMurdo Sound (Antarctica) Monterey Bay (CA, USA) Barkley Sound (BC, Canada) Santa Cruz (CA, USA)
GI, H, laboratory experiments, OSFD GI, pyloric caecum index GI
Leptasterias tenera
Patiria miniata Patiria (as Asterina) miniata Pisaster ochraceus
Pisaster ochraceus
Intertidal (West coast USA)
Laboratory experiments
GI
H, laboratory experiments
Role of photoperiod in gametogenesis and brooding Greatest activity correlated with period of active feeding Correlation between decrease in temperature and onset of gametogenesis Peak digestive gland development corresponds to onset of gametogenesis Food abundance and quality may play a role in quantity of gametes synthesized, but temperature and salinity could be regulating factors Possible role of phytodetritus abundance from seasonal production in surface waters Demonstrated role of photoperiod on gametogenesis Availability of food may promote gamete production Seasonal fluctuation in temperature and food items Long day length (or short nightlength) apparently synchronizes or entrains initiation of gametogenesis and gonad growth Gonad development correlated with decreasing temperature
Pearse and Beauchamp (1986) Worley et al. (1977) Dehn (1980a)
Dehn (1980b)
Pearse (1965)
Pearse (1966)
Pearse and Bosch (2002) Gerard (1976) Rumrill (1989) Pearse and Eernisse (1982)
Feder (1956)
219
(continued)
Appendix A7
(continued)
220
Species
Location
Methods
Control
Source
Pisaster ochraceus
West coast (USA)
Laboratory experiments
Pearse et al. (1986a)
Protoreaster nodosus
Philippines
GI
Plutonaster bifrons
Rockall Trough (NE Atlantic) Passamaquoddy Bay (NB, Canada)
GI
Demonstrated role of photoperiod on gametogenesis (underlying endogenous rhythm) Increase in gonad development coincides with increased temperature and decreased salinity Seasonal input of food may result in seasonal reproduction Possible role of day length and temperature increase
Photoperiod control
Xu and Barker (1990a)
Reproductive cycle influenced by food quantity and quality
Ramirez-Llodra et al. (2002)
Pteraster militaris
Sclerasterias mollis
New Zealand
Styracaster chuni, Styracaster horridus
Porcupine Abyssal Plain, Madeira Abyssal Plain and NW African Slope
Effectiveness of 1-methyladenine injection, GI, H, Laboratory work, MI, OSFD GI, H, laboratory experiments, steroid levels GI, H, OSFD
Bos et al. (2008)
Tyler et al. (1993) McClary and Mladenov (1988, 1989)
Appendix A8 Summary of correlations suggested for the exogenous control of spawning in asteroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Methods
Control
Source
Acanthaster planci
Davies Reef (Australia)
Field observations
At low tide during third moon quarter
Archaster typicus
Japan
Field observations
During receding tide
Archaster typicus Asterias amurensis Asterias amurensis
Philippines Tokyo Bay ( Japan) Derwent River estuary (Australia) Sendai Bay ( Japan)
H Field survey GI, H
Asterias forbesi
Long Island (eastern USA)
Asterias forbesi Asterias forbesi, Asterias rubens (¼vulgaris) Asterias rubens
Long Island Sound (eastern USA) Woods Hole (MA, USA) Millport (UK)
GI, Perivisceral coelomic fluid volume, pyloric caecum index Field work
Mating may coincide with new moon Correlated with temperature Seems to correlate with longest and shortest days of year From January–March when temperature between 9.8 and 12.3 C but varying slightly in other locations In late June to early July when bottom temperature 16–18 C
Babcock and Mundy (1992) Ohshima and Ikeda (1934) Janssen (1991) Ino et al. (1955) Byrne et al. (1997)
Asterias rubens
Essex (UK)
Asterias rubens
Oresund (Denmark)
Asterias rubens
Balsfjorden (Northern Norway)
Asterias amurensis
Gonad morphology, OSFD
Laboratory experiments Laboratory experiments
Abundance of recently settled juveniles Larvae in the field
221
Examination of gametes, GI, H, larvae in the field
Hatanaka and Kosaka (1959) Franz (1986)
Starts when temperature rises to 15 C
Loosanoff (1964)
When exposed to direct sun and increase in temperature From April to June–July. Addition of sperm induces mature individuals to spawn Starts when temperature reaches ca. 15 C Seems to coincide with slight increase in temperature (spring) Correlates with last part of phytoplankton bloom and higher temperature
Costello and Henley (1971) Gemmill (1914)
Hancock (1958) Thorson (1946) Falk-Petersen (1982)
(continued)
Appendix A8
(continued)
222
Species
Location
Methods
Control
Source
Asterias rubens (¼vulgaris) Astrobrachion constrictum
Gulf of St. Lawrence (QC, Canada) Doubtful Sound (New Zealand) Rockall Trough (deep sea NE Atlantic) Port Phillip Bay (Australia)
Field observations, GI
Massive events coincide with major increase of temperature in summer Weak correlation with decrease in temperature Role of food availability in seasonality of reproductive cycle Months with the maximum and minimum temperature coincide with onset of gametogenesis and spring spawning event During period of maximum temperature, early decrease in photoperiod and increasing larval food supply High tide, 1 day after full moon
Himmelman et al (2008) Stewart and Mladenov (1995) Tyler et al. (1993)
Correlated with temperature threshold of ca. 3–4 C; heterosexual aggregations during spawning Presence of gametes from congeners
Mercier and Hamel (2008)
Males induced to spawn by decrease in temperature and female by presence of sperm Decrease in temperature to ca. 2 C induces males to spawn; presence of sperm possibly induces females to spawn Potential role of temperature
O’Brien (1976)
Bathybiaster vexillifer, Plutonaster bifrons Coscinasterias muricata
GI, H, MI, OSFD GI, Gonad ash-free dry weight GI, OSFD, progesterone levels, pyloric caecum index GI, H, OSFD
Cosmasterias lurida
Argentina
Dermasterias imbricate
Vancouver Island (BC, Canada) Continental slope (deep sea NL, Canada)
Dive in August 1987
Friday Harbor (WA, USA) Casco Bay (ME, USA)
Laboratory observations Field observations
Leptasterias polaris
St. Lawrence Estuary (QC, Canada)
Laboratory experiments
Leptasterias polaris
St. Lawrence Estuary (QC, Canada)
Field observations, H
Henricia lisa
Leptasterias hexactis Leptasterias littoralis
GI, H, laboratory observations, OSFD
Georgiades et al. (2006)
Pastor-de-Ward et al. (2007)
Pearse et al. (1988)
Chia (1968)
Hamel and Mercier (1995b)
Boivin et al. (1986)
Leptasterias pusilla
Monterey Bay (CA, USA) Ireland
Laboratory experiments
Odontaster validus
Signy Island (Antarctica)
Ophidiaster granifer
Guam
Orthasterias koehleri Patiriella calcar
Vancouver Island (BC, Canada) SE Australia
Effectiveness of inducing spawning artificially, GI, Larval density H, OSFD, laboratory observations Drive in August 1987 GI, H
Patiriella gunnii
SE Australia
GI, H
Patiriella parvivipara
Eyre Peninsula (South Australia) Otago Harbour (New Zealand) Vancouver Island (BC, Canada) Palau
Laboratory experiments
Marthasterias glacialis
Patiriella regularis Pisaster brevispinus Protoreaster nodosus
223
Pteraster militaris
Passamaquoddy Bay (NB, Canada)
Stylasterias forreri
Vancouver Island (BC, Canada)
Field observations
Field observations Drive in August 1987 Laboratory observations Effectiveness of 1-MA injection, GI, H, laboratory experiments, MI, OSFD Drive in August 1987
Weak demonstration of role of increased photoperiod In July–August during afternoon or early evening. Could be induced by local increase in temperature May correlate with decrease in phytoplankton abundance
Smith (1971)
At night during full moon
Yamaguchi and Lucas (1984) Pearse et al. (1988)
High tide, 1 day after full moon Temperature increase may cue gamete release Temperature increase may cue gamete release Release of juveniles when temperature reaches ca. 20–23 C During the day at slack tide High tide, 1 day after full moon At full moon in May May be induced in females by release of sperm or a chemical released with it
High tide, 1 day after full moon
Minchin (1987, 1992)
Stanwell-Smith and Clarke (1998)
Byrne (1992) Byrne (1992) Keough and Dartnall (1978) Byrne and Barker (1991) Pearse et al. (1988) Scheibling and Metaxas (2008) McClary and Mladenov (1988, 1989)
Pearse et al. (1988)
224
Appendix A9 Summary of correlations suggested for the exogenous control of gametogenesis in echinoids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Methods
Control
Source
Anthocidaris crassispina Anthocidaris crassispina
Hong Kong (China) Wakasa Bay ( Japan)
GI, H GI, H
Anthocidaris crassispina
Mera Bay ( Japan)
GI, H
Chiu (1988) Yatsuya and Nakahara (2004) Horii (1997)
Anthocidaris crassispina
Japan
H, laboratory experiments
Centrostephanus coronatus Centrostephanus coronatus
California (USA)
Centrostephanus rodgersii
Diadema antillarum Diadema antillarum Diadema savignyi
Barbados Florida Keys (USA) Kenya
Diadema savignyi
Fiji
Increased tempo in gametogenesis during decreasing day length Onset of gametogenesis correlated with increasing day length and temperature Temperature and lunar rhythms synchronize reproduction Peak at low temperature (April–May) Peak at low temperature Peak at high temperature and solar radiation. Monthly reproductive rhythms attuned to lunar cycle Monthly reproductive rhythms attuned to lunar cycle
Byrne et al. (1998)
Diadema antillarum
New South Wales (Australia) New South Wales (Australia) Bermuda
H, laboratory experiments H, OSFD, thickness of layer of spermatogenic cells Gonad retrieval rate, H
Food availability Maturation may be inhibited at 15 C but not at 20 and 25 C Gametogenesis may be linked to change in temperature Gametogenesis in mid-summer can be inhibited by holding individuals at 15 C, and triggered several months earlier by maintaining them at 20 or 25 C Reproductive rhythm may be related to monthly lunar (tidal) cycle Possible role of monthly moonlight cycle on reproductive rhythms
Centrostephanus rodgersii
Santa Catalina Island (CA, USA)
Effectiveness of KCl injections, GI, H GI, H, OSFD GI GI Effectiveness of KCl injections, GI, H, oocyte diameter GI, gonad smears, H
Sakairi et al. (1989)
Pearse (1972) Kennedy and Pearse (1975)
King et al. (1994) Iliffe and Pearse (1982) Lewis (1966) Bauer (1976) Muthiga (2003)
Coppard and Campbell (2005)
Diadema setosum
Fiji
GI, gonad smears, H
Diadema (¼Centrechinus) setosum Diadema setosum
Alexandria (Mediterranean Sea)
Laboratory experiments
Gulf of Suez
GI, H, OSFD
Diadema setosum
Indo-Pacific (various locations)
H, OSFD
Diadema setosum
Philippines
GI
Diadema setosum
Kenya
Effectiveness of KCl injections, GI, H, oocyte diameter
Echinocardium cordatum
Northern France
GI, H, MI
Echinocardium cordatum
UK
Echinometra mathaei
Gulf of Suez
Echinometra mathaei
Coast of Kenya
Morphometric and gonad phenotype GI, H, OSFD, thickness of nutritive phagocyte layer GI, H
Monthly reproductive rhythms attuned to lunar cycle More mature individuals found during full moon in summer
Coppard and Campbell (2005) Fox (1924a)
A critical temperature of 25 C required to stimulate gametogenesis; however, high temperature in summer may limit gametogenesis Observed latitudinal variations, and sexual activity when temperature >25 C Possible role of lunar cycle with peak maturation at full moon Annual breeding season negatively correlated with temperature and light. Monthly reproductive rhythms attuned to lunar cycle Marked drop in water temperature followed by a regular temperature increase initiates gametogenesis When feeding is impaired individuals never reach reproductive maturity Minimum temperature and nutrient reserves may regulate reproductive periodicity Gametogenesis commences when temperature and light are at their minima
Pearse (1970)
Pearse (1968a, 1974)
Tuason and Gomez (1979) Muthiga (2003)
Nunes and Jangoux (2004) Buchanan (1966) Pearse (1969b)
Muthiga and Jaccarini (2005)
225
(continued)
Appendix A9
(continued)
226
Species
Location
Methods
Control
Source
Echinometra mathaei
H, OSFD
Echinothrix calamaris
Rottnest Island (Western Australia) Fiji
Echinothrix diadema
Fiji
GI, gonad smears, H
Echinus affinis
Deep sea from NE Atlantic
Pearse and Phillips (1968) Coppard and Campbell (2005) Coppard and Campbell (2005) Campos-Creasey et al. (1994)
Eucidaris tribuloides
Florida (USA)
Analysis of digestive tract contents, OSFD GI, H, laboratory experiments
Eucidaris tribuloides
Plantation and Tavernier Keys (FL, USA) Marlborough Sounds (New Zealand)
GI, H, laboratory experiments
Gamete synthesis possibly under the influence of temperature Monthly reproductive rhythms attuned to lunar cycle Monthly reproductive rhythms attuned to lunar cycle Possible correlation between phytodetritus pulses and gonad growth Demonstrated role of photoperiod in control of gametogenesis; short days entrain gametogenic development High temperature inhibits spermatogenesis, but not oogenesis
Brewin et al. (2000)
Evechinus chloroticus
Doubtful Sound (New Zealand)
GI, H, OSFD
Hemicentrotus pulcherrimus
Oshoro Bay ( Japan)
GI, whole gonad maturation stage
Hemicentrotus pulcherrimus
Japan
H, laboratory experiments
Gametogenesis possibly cued by increasing day length and nutrient availability Differentiation and proliferation of gametes coincide with increase in temperature and day length Gonad maturation initiated by decrease in temperature to ca. 15 C Continuation of maturation occurs when temperature is <5 C Demonstrated the role of temperature (not photoperiod) in the control of gametogenesis
Evechinus chloroticus
GI, gonad smears, H
GI, H
McClintock and Watts (1990) Lares and McClintock (1991)
Lamare et al. (2002)
Agatsuma and Nakata (2004)
Yamamoto et al. (1988)
Hemicentrotus pulcherrimus
Japan
H, Laboratory experiments
Hemicentrotus pulcherrimus
Japan
Lovenia elongata
Gulf of Suez
Effectiveness of KCl injections, F, GI, laboratory experiments, Whole gonad maturation stage H, OSFD
Lytechinus variegatus
Gulf of Mexico (USA)
Paracentrotus lividus
Ireland
Effectiveness of KCl injections, GI GI, H, OSFD
Paracentrotus lividus
Red Sea (Israel)
Laboratory experiments
Paracentrotus lividus
Morocco
GI
Paracentrotus lividus
Brittany (France)
GI, H, MI
Gametogenesis normally occurs in fall and early winter when temperature <20 C; gamete growth suppressed when animals are held at 15 C. Gonad maturation can only be initiated by a change from high (ca. 25 C) to low (ca. 15 C) temperature and does not occur at constant temperature Role of temperature in control of gametogenesis
Nutrient accumulation may be linked to temperature and photoperiod and play a role in gametogenesis Potential role of temperature and photoperiod Maximal gonadal growth seems to correspond to period of decreasing temperature and day length <12 h Long days and temperature between 18 and 22 C enhance gametogenesis Increased GI with increased temperature and food consumption Possible influence of temperature and day length
Sakairi et al. (1989)
Ito et al. (1989)
Pearse (1969a)
Beddingfield and McClintock (2000) Byrne (1990)
Shpigel et al. (2004) Bayed et al. (2005) Spirlet et al. (1998)
227
(continued)
Appendix A9
(continued)
228
Species
Location
Methods
Control
Source
Prionocidaris baculosa
Gulf of Suez
H, OSFD
Pearse (1969a)
Psammechinus miliaris
Loch Fyne (UK)
H, laboratory experiments
Pseudechinus huttoni, Pseudechinus novaezealandiae
New Zealand
Effectiveness of KCl injections, GI, H
Pseudechinus magellanicus
Golfo Nuevo (Argentina)
GI, H, OSFD
Pseudocentrotus depressus
Japan
Pseudocentrotus depressus
Japan
H, laboratory experiments Effectiveness of KCl injections, GI, H
Sphaerechinus granularis
Brittany (France)
Sphaerechinus granularis
Glenan Archipelago (France)
Strongylocentrotus droebachiensis
British Columbia (Canada)
Nutrient accumulation may be linked to temperature and photoperiod and play a role in gametogenesis Reproductive cycle can be manipulated by adjusting photoperiod and temperature Lower temperature in second year of the study prolonged reproductive cycle. Extended reproductive season could be due to El Nin˜o Gametogenesis may be negatively correlated with photoperiod and temperature (results inconclusive) Controlled by temperature (not photoperiod) Maturation promoted at a constant temperature of 19–20 C, but not at 13 C. Rising temperature to 25 C from February to June, and then a constant temperature of 20 C after July stimulates maturation Temperature acts on time course of reproductive cycle, not fecundity rate Mature individuals in good nutritional condition allocate energy to gonad production and store reserves in body wall. Limiting food stops gonad growth without complete regression Gametogenesis seems to respond to photoperiod regime
GI, laboratory experiments Laboratory experiments
GI, H, laboratory experiments
Kelly (2001)
McClary and Barker (1998)
Marzinelli et al. (2006)
Yamamoto et al. (1988) Noguchi et al. (1995)
Guillou and Michel (1993) Guillou et al. (2000)
Dumont et al. (2006)
Strongylocentrotus droebachiensis
New Hampshire (USA)
GI, H
Strongylocentrotus droebachiensis
Maine (USA)
GI, H, laboratory experiments, ratio of nutritive phagocytes to gametes in gonad
Strongylocentrotus droebachiensis
Maine (USA)
GI, H, laboratory experiments, OSFD
Strongylocentrotus intermedius Strongylocentrotus intermedius Strongylocentrotus nudus
Armur Bay (Russia) Northern Primor’e Coast (Russia) East Russia
Strongylocentrotus purpuratus Strongylocentrotus purpuratus
West coast (USA)
Strongylocentrotus purpuratus
Oregon (USA)
Baja California (Mexico)
Walker and Lesser (1998)
GI
Change in photoperiod influences gonad size and onset of gonial cell mitosis; decrease in temperature may stimulate vitellogenesis Food availability regulates energy storage and relative size of gonad. Temperature affects growth rate and maturation of primary oocytes. When gametogenesis is initiated, mature gametes are produced, even at low food availability Maintenance at constant photoperiod yields gonads that do not initiate gametogenesis, although some new sperm are produced. Gonads of both sexes attain large size as a result of growth of nutritive phagocytes Modulated by temperature
GI, H
Regulated by temperature
Gamete volume, gonad morphology Field and laboratory work GI, H, OSFD, laboratory experiments H
Deep red light (wavelength 720 nm) activates gonad development Gonad synthesis influenced by light regime Gametogenesis is under photoperiodic control
Viktorovskaya and Matveev (2000) Evdokimov et al. (2001) Boolootian (1963, 1966) Pearse et al. (1986b)
Temperature may influence filling of nutritive phagocytes
Garrido and Barber (2001)
Bo¨ttger et al. (2006)
Vaschenko et al. (2001)
Chatlynne (1969)
229
(continued)
Appendix A9
(continued)
230
Species
Location
Methods
Control
Source
Strongylocentrotus purpuratus Strongylocentrotus purpuratus
Oregon (USA)
GI, H
Gonor (1973c)
California (USA)
Laboratory experiments
Strongylocentrtus purpuratus Stylocidaris affinis
Pigeon Point (CA, USA) Gulf of Naples (Italy)
Laboratory experiments
Stylocidaris lineata
Deep water (Northern Bahamas)
Tripneustes gratilla
Philippines
Possible correlation between decreasing day length and onset of gametogenesis Annual reproductive cycle correlates with ocean temperature: rise >17 C ( June) coincides with cessation of gamete synthesis. Individuals maintained at ca. 13 C do not spawn Demonstrated role of photoperiod in the control of gametogenesis Food availability may be responsible for gonad development; photoperiod may play a role (no clear correlation) Gametogenesis appears to depend on food availabilityIndividuals may aggregate for reproduction Temperature and food abundance may modulate reproductive activity
H, OSFD
Effectiveness of KCl injections, field observations, H GI, OSFD
Cochran and Engelmann (1975)
Bay-Schmith and Pearse (1987) Holland (1967)
Young et al. (1992)
Tuason and Gomez (1979)
Appendix A10 Summary of correlations suggested for the exogenous control of spawning in echinoids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species
Location
Methods
Control
Source
Allocentrotus fragilis
GI
When upwelling of deeper water occurs
Boolootian et al. (1959)
Anthocidaris crassispina Anthocidaris crassispina Anthocidaris crassispina
Monterey Bay canyon (deep west coast USA) Mera Bay ( Japan) Hong Kong (China) Japan
GI, H GI, H GI
Horii (1997) Chiu (1988) Tsuji et al. (1989)
Anthocidaris crassispina
Seto ( Japan)
At full moon Apparently correlated with temperature In July–August when temperature increases Semi-lunar spawning rhythm
Centrostephanus rodgersii
New South Wales (Australia)
Byrne et al. (1998)
Centrostephanus rodgersii
New South Wales (Australia) Northern Gulf of Mexico (USA) Coast of Panama
Effectiveness of KCl injections, GI, H GI, H
Diadema antillarum
United States Virgin Islands
Diadema antillarum
Coast of panama
Diadema savignyi
Eastern South Africa
In situ spawning observations using KCl injections Effectiveness of KCl injections GI, H, OSFD
During short days and lunar conditions that coincide with the days preceding winter solstice When temperature and day length are at their minima May be correlated with increasing day length Non-random distribution of spawning around the lunar cycle, but apparently no lunar periodicity More likely to occur during the new moon (however, observed outside this period) Lunar rhythm, each spawning during a different lunar phase Could be linked with lunar cycle (new moon)
Clypeaster ravenelii Clypeaster rosaceus
Gonad smears, gonad volume divided by test volume Gonad retrieval rate, H
Effectiveness of KCl injections
Kobayashi (1969)
King et al. (1994) Vernon et al. (1993) Lessios (1991)
Levitan (1988)
Lessios (1991) Drummond (1995)
231
(continued)
Appendix A10 (continued) 232
Species
Location
Methods
Control
Source
Diadema savignyi
Fiji
GI, gonad smears, H
At full moon
Diadema setosum
H, OSFD
Diadema setosum
Various locations Indo-Pacific Red Sea (Egypt)
Diadema setosum
Seto ( Japan)
Diadema setosum
Gulf of Thailand and Andaman Sea
Diadema setosum
Fiji
GI, gonad smears, H
Reproductively active when temperature is above ca. 25 C At full moon. A spawning male stimulates nearby ripe individuals of both sexes Semi-lunar periodicity with gamete release around full and new moons Correlation with lunar cycle (semi-lunar rhythm) with peak around full and new moons At new moon
Coppard and Campbell (2005) Pearse (1968a)
Echinocardium cordatum
Northern France
GI, H, MI
Echinocardium cordatum Echinocardium cordatum Echinocardium cordatum
Vostok Bay (Russia) Seto ( Japan) Oresund (Denmark)
GI, H GI Larvae from the field
Echinometra mathaei
Coast of Kenya
GI, H
Echinometra mathaei
Various locations Indo-Pacific Coast of Panama
H, OSFD
Echinometra viridis
Laboratory experiments
GI, MI (from gonad smears) Gonad morphology
Effectiveness of KCl injections
Temperature may induce or inhibit spawning Temperature variation Temperature variation May coincide with summer peak of primary productivity Commences when temperature and light reach their maxima; peak activity coincides with peak in phytoplankton abundance Reproductively active when temperature >18–20 C At random during lunar cycle
Fox (1924a)
Kobayashi and Nakamura (1967) Kobayashi (1994)
Coppard and Campbell (2005) Nunes and Jangoux (2004) Yakovlev (1987) Nakamura (2001) Thorson (1946) Muthiga and Jaccarini (2005)
Pearse (1968a) Lessios (1991)
Echinothrix calamaris
Fiji
GI, gonad smears, H
At new moon
Echinothrix diadema
Fiji
GI, gonad smears, H
At full moon
Echinus esculentus
Port Erin (UK)
When temperature is increasing from 7 to 9 C
Eucidaris tribuloides
Coast of Panama
Evechinus chloroticus
Marlborough Sounds (New Zealand) Doubtful Sound (New Zealand) Doubtful Sound (New Zealand) Oshoro Bay ( Japan)
Gonad weight, laboratory spawning induction Effectiveness of KCl injections GI, H
Evechinus chloroticus Evechinus chloroticus Hemicentrotus pulcherrimus
GI, H, OSFD Field observations, GI, plankton sampling GI, whole gonad maturation stages
Hemicentrotus pulcherrimus Hemicentrotus pulcherrimus Heterocentrotus mammillatus
Hokkaido ( Japan)
GI
Seto ( Japan)
Leodia sexiesperforata
Coast of Panama
Lytechinus variegatus
Florida (USA) and Bermuda
GI, gonad morphology, gonad smears Effectiveness of KCl injections, GI, gonad smears, H, OSFD Effectiveness of KCl injections Gonad volume, spawning observations
Northern Red Sea
Lunar rhythm, each spawning event during a different lunar phase When surface temperature reaches ca. 15 C After summer solstice but before the peak summer temperature At full moon, during spring tides and decrease in temperature Temperature <5 C prevents spawning; temperature rising from 6 to 9 C favours gamete release With low winter temperature
Coppard and Campbell (2005) Coppard and Campbell (2005) Stott (1931)
Lessios (1991) Brewin et al. (2000) Lamare et al. (2002) Lamare and Stewart (1998) Agatsuma and Nakata (2004) Agatsuma (1992)
Seems consistent with semi-lunar rhythms Weak correlation with semi-lunar or lunar cycle
Kobayashi (1992)
Randomly during lunar cycle
Lessios (1991)
Possible correlation with a lunar cycle in Bermuda but less apparent in Florida
Moore et al. (1963a)
Dotan (1990)
233
(continued)
234
Appendix A10 (continued) Species
Location
Methods
Control
Source
Lytechinus variegatus
GI, field observations
Lytechinus variegatus
Eastern coast of Florida (USA) Coast of Panama
Appearance of young sea urchins in a year with low rainfall Every new and full moon
Moore and Lopez (1972) Lessios (1991)
Lytechinus williamsis
Coast of Panama
Lessios (1991)
Mespilia globosus
Seto ( Japan)
Paracentrotus lividus
West coast of Ireland
Effectiveness of KCl injections, GI, H, MI GI, H, OSFD
Paracentrotus lividus
North Adriatic Sea
In situ experiments
Paracentrotus lividus
Algeria
GI, RI
Paracentrotus lividus
Brittany (France)
GI, H, MI
Paracentrotus lividus
Coast of Spain
Presence of larvae
Paracentrotus lividus
Ligurian Sea (W Mediterranean) Villefranche-sur-Mer (France) Morocco
Presence of larvae
Non-random distribution of spawning around the lunar cycle, but no clear lunar periodicity Spawning apparently follows a semilunar rhythm during breeding season ( July–September) Increasing temperature (13–15 C) is a possible proximate cue Sperm may induce spawning in congeners of both sexes Successive episodes seem to be correlated with temperature cycle Events appear to be triggered by day length May be correlated with rising temperature Coincides with end of spring phytoplankton bloom Possible influence of temperature
Paracentrotus lividus Paracentrotus lividus
Effectiveness of KCl injections Effectiveness of KCl injections
GI, larvae from plankton, MI GI
With phytoplankton bloom induced by upwelling
Kobayashi (1967)
Byrne (1990) Keckes (1966) Semroud and Kada (1987) Spirlet et al. (1998) Lopez et al. (1998) Pedrotti (1993) Fenaux (1968) Bayed et al. (2005)
Paracentrotus lividus
Portugal
Laboratory work
Paracentrotus lividus
Coast of Algeria
GI
Phyllacanthus imperialis
Lizard Island (Australia)
In situ observations
Sphaerechinus granularis
West Brittany (France)
GI, H, OSFD
Throughout the year using special diets with controlled environmental conditions equivalent to field conditions during late spring (14 h of light and 18 C) Hydrographic conditions suggested as determining factors Single male observed 4 days after full moon spawning with corals May be modulated by temperature
Stomopneustes variolaris Strongylocentrotus droebachiensis Strongylocentrotus droebachiensis
Madras Harbour (India) Puget Sound (BC, Canada) West coast of Vancouver Island (BC, Canada) Vancouver Island (BC, Canada)
GI Field observations, GI
Decrease in salinity Spring phytoplankton bloom
Field in August 1987
High tide, 1 day after full moon. A single individual
Pearse et al. (1988)
Field in March 1998
Levitan (2002b)
Strongylocentrotus droebachiensis
Maine (USA)
Fertilization assays, field experiments, GI
Strongylocentrotus droebachiensis Strongylocentrotus droebachiensis
Maine (USA)
GI
St. Lawrence Estuary (eastern Canada)
Controlled laboratory experiments
Strongylocentrotus droebachiensis
Kodiak (AK, USA)
GI
Long sunny period, phytoplankton bloom. Simultaneously with S. purpuratus and S. franciscanus At a larger scale spawning appears related to lunar cycle. At a smaller scale early phytoplankton bloom seems to be the cue May be influenced by several factors including temperature Induced by presence of high concentration of phytoplankton. Sperm induces females to spawn Possible correlation with spring phytoplankton bloom
Strongylocentrotus droebachiensis
Luis et al. (2005)
Guettaf et al. (2000) Olson et al. (1993) Guillou and Lumingas (1998) Giese et al. (1964) Himmelman (1976)
Gaudette et al. (2006)
Seward (2002) Starr et al. (1990, 1992, 1993) Munk (1992)
235
(continued)
Appendix A10 (continued) 236
Species
Location
Methods
Control
Source
Strongylocentrotus droebachiensis Strongylocentrotus franciscanus
Gulf of St. Lawrence (QC, Canada) Vancouver Island (BC, Canada)
Field observations, GI
Himmelman et al. (2008) Levitan (2002b)
Strongylocentrotus nudus
Japan
GI
Strongylocentrotus nudus
Hokkaido ( Japan)
Strongylocentrotus nudus
Hokkaido ( Japan)
GI, H, larvae from the plankton GI, H
Strongylocentrotus purpuratus
Vancouver Island (BC, Canada)
Field observations in March 1998
Toxopneustes variegatus
Beaufort (NC, USA)
Tripneustes esculentus
Barbados
Tripneustes esculentus
Miami (FL, USA) and Bermuda
Tripneustes gratilla
Kenya coast
Tripneustes ventricosus
Coast of Panama
Gonad status (macroscopically) Laboratory observations Gonad volume, spawning observations Effectiveness of KCl injections, GI, H Effectiveness of KCl injections
Massive events coincide with large increase in temperature in summer Long sunny period, phytoplankton bloom. Simultaneously with S. droebachiensis and S. purpuratus in 1998 September–October when temperature drops September–October when temperature drops from 20 to 15 C When temperature drops from 20 to 15 C Long sunny period, phytoplankton bloom. Simultaneously with S. droebachiensis and S. franciscanus Empty gonad after night of full moon
Field in April 1995 and March 1998
Tsuji et al. (1989) Agatsuma et al. (1988, 2000) Sugimoto et al. (1982) Levitan (2002b)
Tennent (1910)
Both sexes induced to spawn by sperm suspension in seawater Seems to be induced to spawn by increase in temperature
Lewis (1958)
Possible correlation with some phase of the lunar cycle At random during lunar cycle
Muthiga (2005)
Moore et al. (1963b)
Lessios (1991)
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TAXONOMIC INDEX
A Acanthaster planci, 6, 62, 85, 92, 114, 120, 126, 135–6, 139, 165, 190 Achlyonice violaecuspidata, 61 Acrocnida brachiata, 38, 140 Actinopyga echinites, 19, 145, 158–9 Actinopyga lecanora, 78, 90 Actinopyga mauritiana, 146–7 Aeudocentrotus depressus, 167 Allocentrotus fragilis, 48, 120 Allostichaster capensis, 45 Amperima rosea, 41–2 Amphiodia occidentalis, 18, 102 Amphiodia pulchella, 192 Amphioplus abditus, 89, 130 Amphipholis gracillima, 192 Amphipholis kochii, 16, 66, 95, 159 Amphipholis squamata, 77, 123, 142 Amphiura chiajei, 16, 95, 140 Amphiura filiformis, 16–17, 38, 77, 94, 129, 133, 142 Antedon bifida, 16, 37, 133 Antedon mediterranea, 66 Antedon rosacea, 89 Anthocidaris crassispina, 26, 32, 99, 114, 117, 167, 187 Apostichopus japonicus, 66, 96, 143, 159–61 Arbacia punctulata, 153 Archaeopneustes histrix, 64 Archaster angulatus, 135 Archaster typicus, 62, 126, 131, 135 Aslia lefevrei, 18, 41, 78, 91, 96, 130 Aspidodiadema jacobyi, 64, 128 Asterias amnurensis, 166 Asterias amurensis, 23, 67–8, 85, 165, 167 Asterias forbesi, 69, 85, 97, 135, 162, 165, 184 Asterias rubens, 6, 15, 21, 23, 67–8, 85, 92, 126, 139, 147, 173, 180 Asterias vulgaris, 173 Asterina gibbosa, 6 Asterina minor, 126 Asterina pectinifera, 68, 164–7, 180 Asterina stellifera, 173 Asteroporpa annulata, 94 Astrobrachion constrictum, 18, 95, 98 Astropecten irregularis, 6, 174 Astropecten irregularis pentacanthus, 67
B Bathybiaster vexillifer, 47 Bathyplotes natans, 42 Benthogone rosea, 42 Bohadschia argus, 78, 90, 110, 112, 124, 130, 134, 138, 190 Bohadschia graeffei, 190 Brissopsis lyrifera, 148, 192 C Capillaster multiradiatus, 89 Caudina chilensis, 96 Centrostephanus coronatus, 35, 116, 118 Centrostephanus rodgersii, 32, 55, 152, 171, 187 Cidaris blakei, 64, 128 Clypeaster japonicus, 167 Clypeaster ravenelii, 54 Coelopleurus floridanus, 64 Comanthus japonica, 9 Comanthus parvicirra, 37 Comatella nigra, 37 Conolampas sigsbei, 64 Coscinasterias muricata, 24, 45, 88, 98, 165 Cosmasterias lurida, 21, 45, 104 Crossaster papposus, 92, 102, 191 Ctenodiscus crispatus, 6, 46–7 Cucumaria frondosa, 19, 40–1, 58–60, 62, 66, 78, 85–6, 88, 92, 96, 103, 119, 130, 143–4, 157, 172, 175–8, 188–9, 191–2 Cucumaria lubrica, 78 Cucumaria miniata, 78, 135, 138 Cucumaria pseudocurata, 103, 124 D Deima validum, 42 Dendraster excentricus, 167 Dermasterias imbricata, 85 Diadema antillarum, 35, 55, 115, 127, 137, 187 Diadema savignyi, 109, 116 Diadema setosum, 25, 101, 114, 149, 187, 189 Dytaster grandis, 105 E Echinocardium cordatum, 26, 48, 54, 101, 155, 187 Echinometra, 184 Echinometra lucunter, 121, 152
293
294
Taxonomic Index
Echinometra mathaei, 25, 32, 101, 109, 114, 178, 186 Echinometra vanbrunti, 109 Echinostrephus aciculatus, 114 Echinothrix diadema, 116 Echinus affinis, 13, 56–7 Echinus esculentus, 54, 98, 127, 148, 192 Echinus miliaris, 63 Elpidia glacialis, 61 Euapta godeffroyi, 78, 90, 110, 112, 124, 138, 190 Eucidaris tribuloides, 15, 28, 31, 117, 187 Eupentacta chronhjelmi, 41, 91, 135 Eupentacta quinquesernita, 92 Evechinus chloroticus, 55–6, 87, 99, 117, 127, 149–150 F Florometra serratissima, 9, 37 Fucus vesiculosus, 105 G Gorgonocephalus caput-medusae, 89 Gorgonocephalus caryi, 89, 142, 193 Gorgonocephalus chilensis, 123 Gorgonocephalus eucnemis, 38, 89, 142 H Heliocidaris erythrogramma, 127 Hemicentrotus pulcherrimus, 26–7, 32, 71, 99, 114, 117, 155, 167, 185–6 Hemipholis elongata, 16, 120 Hemipholis elongate, 89 Henricia abyssicola, 48, 178 Henricia lisa, 4, 64, 98, 126, 137, 148, 174, 192 Henricia sanguinolenta, 92 Heterocentrotus mammillatus, 117, 178 Heterometra savignyi, 89 Holothuria atra, 66, 78, 90, 144, 157 Holothuria coluber, 138, 190 Holothuria fuscogilva, 96, 104, 145, 157 Holothuria fuscopunctata, 19, 78, 90 Holothuria leucospilota, 20, 78, 91, 134, 145, 158–63 Holothuria moebi, 160 Holothuria nobilis, 78, 157 Holothuria pardalis, 158–60 Holothuria pervicax, 160 Holothuria scabra, 19, 34–5, 40, 61, 78, 96, 112, 120, 124, 145, 156–7, 159, 189 Holothuria scabra versicolor, 19 Holothuria tubulosa, 40, 66, 96, 135 Holothuria whitmaei, 146 Hothuria leucospilota, 190 Hymenaster membranaceus, 13 Hyocrinus foelli, 37 Hyphalaster inermis, 48
I Isostichopus fuscus, 4, 8, 78, 91, 113, 146, 189, 192 K Kolga hyalina, 125 L Labidoplax buskii, 78, 96, 130 Laetmogone violacea, 42 Lamprometra klunzingeri, 89, 132 Leptasterias hexactis, 44 Leptasterias littoralis, 85, 97 Leptasterias ochotensis similispinus, 125 Leptasterias polaris, 44, 62, 97, 131, 165, 174, 180 Leptasterias pusilla, 20, 44, 136 Leptasterias sp., 21, 85 Leptasterias tenera, 47 Leptopentacta elongata, 91 Leptosynapta inhaerens, 40, 158, 160 Leptosynapta tenuis, 78, 96 Linckia multifora, 6 Loxechinus albus, 152, 189 Luidia clathrata, 6, 20, 44 Lytechinus variegatus, 6, 49, 70, 116, 121, 127–28, 138, 148, 181 M Marthasterias glacialis, 85, 92, 97, 126, 165 Mediaster aequalis, 165 Mespilia globulus, 114, 117 Microphiopholis atra, 16, 120 N Nemaster rubiginosa, 16 Neosmilaster georgianus, 63, 126, 135 O Odontaster sericeum, 16 Odontaster validus, 16, 23, 47, 87 Oneirophanta mutabilis, 42 Ophiacantha bidentata, 39 Ophiactis resiliens, 90, 133 Ophiarthrum pretum, 90 Ophiarthum pictum, 77 Ophidiaster granifer, 87, 92, 114 Ophiocantha bidentata, 94 Ophiocoma aethiops, 140 Ophiocoma dentata, 133 Ophiocoma echinata, 38, 89, 95, 129–30, 140, 142 Ophiocoma pica, 89–90 Ophiocoma pumila, 90 Ophiocoma wendtii, 140, 142 Ophiocten gracilis, 39 Ophiocten hastatum, 39
295
Taxonomic Index Ophiocten sericeum, 16, 140 Ophiodaphne formata, 123 Ophiodaphne materna, 123 Ophioderma brevispinum, 16, 129, 184 Ophioderma cinereum, 90, 140 Ophioderma echinata, 133 Ophioderma longicauda, 94 Ophioderma nubicundum, 123 Ophioderma rubicundum, 77, 89, 111, 129, 140 Ophioderma squamosissimum, 129 Ophiomusium lymani, 39, 103 Ophionephthys limicola, 142 Ophionereis fasciata, 133 Ophionereis olivacea, 94 Ophionereis schayeri, 90, 133 Ophionotus victoriae, 17, 38, 143 Ophiopholis aculeata, 34, 77, 89–90, 94–5, 123, 129–30, 139–42, 142–3, 159, 190 Ophiopteris papillosa, 18, 38 Ophioten sericeum, 77 Ophiothrix caespitosa, 133 Ophiothrix fragilis, 17–18, 34, 38, 77, 88, 94, 119, 133, 140 Ophiothrix longipeda, 94 Ophiothrix oerstedi, 129, 140 Ophiothrix orstedii, 90 Ophiothrix propinqua, 90 Ophiothrix spiculata, 18, 102 Ophiothrix spongicola, 90, 133 Ophiothrix suensoni, 193 Ophiothrix texturata, 77 Ophiura albida, 16, 38, 94–5, 102 Ophiura brevispina, 89 Ophiura hastatum, 39 Ophiura ljungmani, 39, 103, 143 Ophiura ophiura, 38, 129, 142 Ophiura robusta, 34, 77, 90, 95, 123, 139, 190 Orthasterias koehleri, 85, 135 Oxycomanthus bennetti, 77, 89 Oxycomanthus japonicus, 9, 15, 34, 66, 77, 89, 93, 110–11, 129, 132 P Palaeopneustes cristatus, 64 Paracentrotus lividus, 33–4, 49–51, 70–1, 98, 128, 137, 148, 153–4, 180, 184, 186, 188 Parastichopus californicus, 78, 88, 104, 124, 159–61 Paroriza pallens, 42 Paroriza prouhoi, 42 Patinapta ooplax, 112 Patiria miniata, 21, 44, 160, 165 Patiriella gunnii, 44, 98 Patiriella parvivipara, 87, 97 Patiriella pseudoexigua, 44 Patiriella regularis, 46, 85, 92, 165 Pearsonothuria graeffei, 78, 90, 139, 190 Peniagone azorica, 178 Peniagone diaphana, 178
Peniagone vignoni, 43 Peronella japonica, 167 Phaeodactylum tricornutum, 105, 158 Phyllacanthus imperialis, 87, 92, 117 Pisaster brevispinus, 85, 165 Pisaster giganteus, 165 Pisaster ochraceus, 15, 20–2, 43–4, 67, 87, 160, 165, 174, 183 Plutonaster bifrons, 47 Polycheira rufescens, 112 Porania antarctica, 87 Posidonia oceanica, 127 Prionocidaris baculosa, 49 Promachocrinus kerguelensis, 9, 37 Protelpidia murrayi, 42 Protoreaster nodosus, 87, 139 Psammechinus miliaris, 33, 148, 176, 186 Pseudocentrotus depressus, 26, 32, 55, 71, 117, 185, 186 Pseudocnus lubricus, 78, 119, 124, 130 Pseudostichopus villosus, 42 Psolus chitonoides, 135 Psolus dubiosus, 78 Psolus fabricii, 19, 41, 104, 191 Psychropotes longicauda, 42 Pteraster militaris, 46, 87, 92, 131, 165, 191 Pycnopodia helianthoides, 165 S Salenia goesiana, 64, 128 Schizochytrium sp., 157 Sclerasterias mollis, 22, 46, 67–8, 180 Scotoplanes globosa, 61 Skeletonema costatum, 105 Smilasterias multipara, 87, 165 Solaster endeca, 92, 102, 191 Sphaerechinus granularis, 53, 100, 128, 171 Sphaerechinus granularis granularis, 138 Sterechinus neumareyi, 156 Stichopus californicus, 159–60 Stichopus chloronotus, 78, 90, 104, 110, 112, 138, 146, 157, 190 Stichopus herrmanni, 114, 124 Stichopus japonicus, 160 Stichopus mollis, 18, 143, 147 Stichopus variegatus, 19, 110, 112 Stomopneutes variolaris, 121 Strongylocentrotus droebachiensis, 28–31, 49, 52–3, 92, 100, 105–7, 117, 139, 153, 158, 171, 174–6, 185–6, 189–91 Strongylocentrotus franciscanus, 70, 109, 127, 132, 153, 185–6 Strongylocentrotus intermedius, 26, 49, 54, 72, 153, 155, 173, 180, 186, 189 Strongylocentrotus nudus, 29, 71, 99 Strongylocentrotus purpuratus, 15, 24, 26–7, 28, 49–50, 70, 99, 121, 148, 155, 167, 184–6, 192
296
Taxonomic Index
Stylasterias forreri, 85 Stylocidaris affinis, 29 Stylocidaris lineata, 57, 63, 128, 138 Styracaster chuni, 48 Styracaster horridus, 48
Thyone briareus, 90, 96, 157 Toxopneustes variegatus, 116 Tripneustes esculentus, 6, 127 Tripneustes gratilla, 54, 114, 155 X
T Thelenota ananas, 19, 78, 91, 96, 157
Xyloplax, 3
SUBJECT INDEX
A Aggregation, 122 associated with reproductive cycle, 61 Asteroidea, 97, 125–6 breeding aggregations, of deep-sea echinoderms, 64 in brittle stars, 133 in deep sea, 63–4 dense aggregations of elasipods, 61 Echinoidea, 63, 127–9 feeding aggregations, 63 and gamete synthesis, 192 Holothuroidea, 123–5 Ophiuroidea, 123 pre-spawning aggregations, 131, 136, 213 small-scale aggregations, 76 of urchins, 109 Algal blooms, 102 Aperiodic reproductive cycles, 4–5, 15, 47, 78, 125, 148, 170 Apodida, 6, 84 Aquaculture, 1–3, 76, 161 Aspidochirotida, 6, 79 Asteroidea, 2, 6, 11, 20-4, 43, 61, 67, 85, 88, 92, 97, 104, 114, 120, 125, 131, 135, 147, 162, 217, 220, 221 evidence of chemical exchanges, 61 gonad-stimulating substance (GSS), role of, 67–9 inter-individual interactions during gametogenesis, 62 photoperiod and reproduction, 11 photoperiod cycle, role in, 21 pre-spawning sex recognition, 63 pyloric caecum and gonad indices, 24 regulation of oogenesis, 22 reproductive cycles, 11 reproductive system, 6 role of food and/or nutritional status, 11 role of sinking phytodetritus, 11 time of gametogenic and gonad development in, 147–8 Asteroids. See also Asteroidea; Sea stars aggregation in, 125 chemical signalling in, 61 cyclic changes in lipid content of, 46 developing gonads in, 47 disruption of steroid metabolism in, 180
final oocyte maturation, 67 gametogenesis in, 13 influence of detritic food pulses on, 109 maturation of oocytes in, 167 1-methyladenine (1-MA) in, 159–60 radial nerve factor, 137 reproductive cycles, 37 reproductive modes, 6 RNF from, 160-1 spontaneous spawning in, 85 Asterosaponins, 68–9 Asynchrony, of spawning between sexes Asteroidea, 131–2 Crinoidea, 129 Echinoidea, 132 Holothuroidea, 130–1 Ophiuroidea, 129–30 B Biocides, 180 Bioluminescence, 61 Breeding aggregations, 122. See also Aggregation Breeding periods, 1, 10, 14, 76, 95, 101, 126, 140, 144–5, 172, 182, 189, 192 Breeding success, 2 Brittle stars, 5, 39, 94, 102, 111, 133, 139, 159. See also Ophiuroidea; Ophiuroids Brooding species, 6, 44, 78, 94, 97, 119, 125, 135, 142 C Carotenoids, effect on reproduction, 37 Chemical communication, 2, 58, 74, 190 demonstrations during gametogenesis, 175 evidence in Asteroidea, 135–7 Crinoidea, 132–3 Echinoidea, 137–8 Holothuroidea, 134–5 Ophiuroidea, 133–4 Chemical signalling, related to reproduction, 122. See also Chemical communication Concentricyloidea, 2 Crinoidea. See also Crinoids; Feather stars gametogenesis, 2 endogenous regulation, 65–6 food availability and assimilation, 37 lunar periodicity, 34
297
298
Subject Index
Crinoidea (cont.) photoperiod and temperature, 15–16 reproductive cycles, 9 reproductive features, 5 spawning, 76–7 chemical communication, 132 day/night cycle, 89 endogenous mediation, 158 lunar cycle, 110 plankton levels, 102 sex asynchronization, 129 temperature, 93 endogenous regulation, gamete synthesis in crinoids, 65 gametogenesis, 15–16 reproductive cycles, 9 Crinoids. See also Crinoidea; Feather stars contractions of gonadal musculature in, 158 factors influencing spawning in, 76 larvae, 100 regulation of gamete synthesis in, 65 reproductive cycles in, 9, 169 spawning in, 102 stalked and stalkless, 5 steroid levels in, 66 synthesizing sex steroids, 65 Cyclic AMP, and oocyte maturation, 66 Cyproterone acetate (CPA), 180 D Day length annual temperature and, 98 gametogenesis in Oxycomanthus japonicus and, 15 and increased seawater temperature, 16, 121 influencing, sea surface temperatures, 14 and lunar phases, 192 Paracentrotus lividus gonadal growth coinciding with, 33 and reproductive cycles in asteroids, 11 gametogenesis, controlled by short, 28 and temperature in holothuroid gametogenesis, 19 and light cue, on brittle star reproduction, 88 Day/night cycle, 89 Deep-sea asteroids Henricia lisa, 5, 98, 132 Hyphalaster inermis, Styracaster chuni, and Styracaster horridus, 48 brittle star Ophiomusium lymani, 39 crinoid Hyocrinus foelli, 37 deposit feeders, 42 echinoderms, 12–3, 37, 64, 76, 139, 178, 182 echinoid Echinus affinis, 56 ecology of benthic organisms in, 182 environment, 104 floor, 182–3
habitats, 181 holothuroids, 42, 78, 125, 179 invertebrates, 63, 181 occurrence of seasonal pulse into, 36 organic matter to, 43 pulses of organic food to, 47 species, 3, 6, 39, 178 Dendrochirotida, 5, 83 Diel dark–light cycles, 88 Dithiothreitol (DTT), 158 E Echinoid gonad, 6 Echinoidea, 2, 12, 24, 35, 48–57, 70–72, 87–9, 92, 98–102, 105–9, 114–8, 120–1, 127–9, 132, 137–8, 158, 166–7. See also Echinoids; Sea urchins development of gametes, 26 endocrine control, of reproduction, 69, 71 gametogenic synchronization, 26 gonad growth, 11 latitudinal gradients, gonad maturation, 25 photoperiodic control, gametogenesis, 27–32 pre-spawning clustering in, 63, 131, 136, 213 seawater temperature, 11, 25, 27, 29, 32-3, 99–101, 117 and gonad development, 24 and gonad maturation, 26 temporal and spatial factors in reproduction of, 148–56 breeding of red sea urchin, 153 latitudinal variability, 151 reproductive cycle, of Paracentrotus lividus, 153 seasonal variations in gonad index and, 155 spatial and temporal disparities, 149 Echinoids, 1, 11, 14–5, 26, 27, 29, 32–3, 36–7, 49, 55–58, 64–5, 70–1, 76, 87, 98, 105, 114, 120–2, 127–8, 134, 137, 148, 167, 171, 176, 178, 180, 183–6, 189, 191–2. See also Echinoidea; Sea urchins determination of spawning periodicity in, 175 endocrine control in, 69 exhibiting GI values of unequal magnitude, 172 food supply on reproductive cycle of, 49 gametes and brooding, 6 gametogenesis in, 12 gonad, 6 influence of detritic food pulses on, 109 light intensity in, 184 lunar reproductive patterns in, 118 nutritive phagocyte utilization, 24 pre-spawning clustering in, 63 reproductive development in, 51 sensitivity to food limitation, 50 somatic and gonadal growth in, 48
299
Subject Index
Endocrine system, 64. See also Neuro-hormonal system endogenous mediation climatic impact, 179, 180 in Crinoidea, 66, 111 in Echinoidea, 69, 71 in Holothuroidea, 160 Endogenous mediation of reproduction, 64 Asteroidea, 67–9 Crinoidea, 64–6 Echinoidea, 69–2 Holothuroidea, 66 Ophiuroidea, 66 Environmental factors, 2, 4, 8–11, 13–5, 18–9, 23, 37, 42, 45, 52, 58, 67, 76–7, 85, 93, 102–3, 117, 118, 157, 174, 179, 190, 194 F Feather stars, 5. See also Crinoidea; Crinoids Fenarimol (FEN), 179 Fertilization success, 76 Food availability, and assimilation, 35 Asteroidea, 40–3 direct relationship, with feeding, 46–7 indirect evidence, from shifts in nutrient storage, 43–6 pulses of organic food, to deep sea, 47–8 Crinoidea, 37 Echinoidea, 48–55 deep sea, 56–7 proposed mechanisms, 55 Holothuroidea, 40–3 Ophiuroidea, 38–40 Food supply, effect on gametogenesis, 35–6 G G-protein-coupled receptors (GPCRs), 184 Gamete maturation, 4, 10, 39, 62, 126, 176, 185. See also Gametogenesis Gamete release, 102. See also Spawning in Asterias amurensis, 85 in Cucumaria miniata, 104 in Cucumaria frondosa, 157 and environmental factors, 102 heterospecific cueing of, 139 induction by potassium chloride (KCl), 166 in situ, 75 lunar periodicity, 110 monitoring, 89, 146 in Parastichopus californicus, 78 periods of, temperature maxima/seasonal increases in temperature, 94 regulation, 71 stimulus required to induce, 75 stress-induced, 174 in Strongylocentrotus droebachiensis, 92
synchronization with tides, 118 Gamete-shedding substance, See GSS Gametogenesis, 7–72 accumulation of reserves for, 41 accumulation of triterpene glycosides in, 66 chemical communication related to, 58, 61 controllers of, 13 in crinoids, 9 defined annual cycles of, 148 delayed, 32, 181 dietary administration of progesterone, testosterone and, 71 diet/nutritional factors, 48 elongated gonads/branched sacs during, 6 factors influencing, 12 food supply on, 35 gametes formation through, 8 and gonad growth, 8, 18, 21 gonad index and, 71, 174 in Hemicentrotus pulcherrimus, 26–7 at high temperatures, 27 of Holothuria leucospilota in the Cook Islands, 20 in holothuroids, 10 hormone levels during, 65 influence of photoperiod on, 20, 188 influence of temperature on, 15, 26 initiation in Strongylocentrotus droebachiensis, 29 in Jamaican population of Nemaster rubiginosa, 16 in Japanese echinoid species, 32 levels of sex steroids during, 68 lunar cycle, influence of, 115 and lunar periodicity in gamete release, 110 metabolic processes and, 21 nutrients used in, 36 and nutritive phagocyte utilization in, 24 in ophiuroids, 10 out-of-season in echinoids, 26 in Paracentrotus lividus, 51 patterns of, 23 pheromones and, 137 photoperiodic control of, 23, 31, 34, 175 in phytoplankton-feeding species Psolus fabricii, 19 in Pseudocentrotus depressus, 26 rate of, 32 role of, neural and chemical mechanisms in controlling, 69 role of single/multiple factors in control of, 10 of sea cucumber Cucumaria frondosa, 193 seasonality of, 12 in sea stars, 23, 68 of sea urchin, 27, 57 and short day lengths, 28 and specific environmental cue, 33 in Strongylocentrotus purpuratus, 27 suppressed/delayed, 23 in temperate species of echinoids, 11
300
Subject Index
Gametogenesis (cont.) and thickening of tubule wall, 41 winter sedimentation of primary production and, 55 Gametogenic cycle, 3–4, 8, 176. See also Gametogenesis gonadal cells, transformation during, 170 Germ cells, 46, 172, 179 Germinal vesicle breakdown (GVBD), 160–162, 165 Global warming, impact on reproductive processes, 179 Gonad growth, 8, 11, 51, 173, 179 Gonad index (GI) correlation with body size, 170 definition of, 171–2 drawback of, 172 for estimating reproductive activity, 170 histological determinations of, 172–3 of sea urchins, 171 variations of, 171 Gonad maturity, 8, 10, 18, 36, 50, 117, 156, 173, 181 Gonad production, and nutritional status, 12 Gonad-stimulating substance, See GSS Gonadosomatic index (GSI), 170. See also Gonad index (GI) Gregariousness, See Aggregation GSS, 67, 159, 162, 164–7
Lunar cycle, 34 and gametogenesis, in Diadema antillarum, 115 gametogenic synchrony, of Holothuria scabra, 34 influence on, holothuroid reproduction, 112–4 lunar periodicities in asteroid reproduction, 114 in brittle stars, 111 lunar reproductive rhythm, Diadema antillarum, 35 spawning Echinoids, 114–8 Crinoidea, 110–1 of Ophiothrix fragilis, 34 spawning periodicity, in Oxycomanthus japonicus, 34 Lunar periodicity, 34, 110, 114, 118, 156 Lunar reproductive rhythm, 35
H
M
Hermaphroditism, 5–6 Holothuroids. See also Holothuroidea; Sea cucumbers distinctive breeding seasons of, 103 epidemic events, 191 gametogenic development, 60 histology spawning of, 175 in situ study of spawning in, 85 relative frequencies of gametogenic stages, 177 spawning periods, 144 Holothuroidea, 2, 5, 34, 156–8, 159–62. See also Holothuroids; Sea cucumbers active phase, of gametogenesis in, 19 annual reproductive cycles, and factors controlling, 10 chemical communication in, 61 dense aggregations of elasipods, 61 field caging experiments, 59 influence of temperature, on oogenesis of, 20 inter-individual communication in, 58 reproductive habits, and geographical location in, 143 inter-annual variability, 147 spatial variability, 143–7 roles played by photoperiod, 20
Major yolk protein (MYP), 180 Maturation-inducing substance (MIS), 67, 130, 158, 160–2 1-Methyladenine (1-MA), 67, 137, 156, 158–61, 165–7 Methyltestosterone (MET), 180 Migrations, 8, 183 Mycosporine-like amino acids (MAAs), 66
temperature influence, on gonad maturation of, 18 I Inter-individual communication, 57–8, 63, 85, 121–2. See also Chemical communication L
N Neuro-hormonal system, 8 neuro-endocrine system, 64, 74 neuro-secretion/secretor, 136, 158–9, 164 O Oocyte maturation, final. See also Gametogenesis; Oogenesis extra-follicular mediation of, 165 schematic representation of, in holothuroid, 163 Oocyte size frequency distributions, 39, 75, 125, 171, 176 Oogenesis, 20–2, 33, 40, 45, 48, 67–8, 71–2, 179 Ophiuroidea, 2, 5, 34, 38–40, 66, 77, 88–90, 93–5, 102–3, 111, 119–20, 123, 129–30,
301
Subject Index
133–4, 158–9. See also Ophiuroids; Brittle stars annual shifts, in spawning seasons of, 142–3 breeding seasons of, and ambient seawater temperature, 16 duration and seasonality, of phases of gametogenesis in, 139 gametogenesis and spawning in, 16 gonadal growth in, 16–17 oocyte growth in, 16 oocyte size and temperature, 17 reproductive patterns, and gametogenic activity, 9–10 temperature and food supply, 17 temperature-related gonad development, 18 variations, in population reproductive cycle, 140, 142 Ophiuroids. See also Ophiuroidea; Brittle stars breeding aggregations, 122 breeding periods in, 172 cyclic variations in downward flux of particles, influence of, 103 gametogenic activity in, 9 oocyte maturation and spawning in, 159 photosensory organs in, 184 reproduction in, 158 reproductive cycle in, 16, 38 reproductive periodicity of, 119 seasonal reproductive patterns, 18 spawning in, 93–4 Ornithine decarboxylase (ODC), 68 P Pheromones, 57, 185 Photoperiod, 11, 14–15, 18, 21, 24, 26, 28–54, 52, 70, 76, 85, 87, 93, 98, 104, 144, 175, 184, 188, 191. See also Day length Phytodetritus, 11, 13, 37, 39, 42, 47–8, 57, 102, 104, 182. See also Phytoplankton Phytoplankton, 2, 19, 36, 38, 42, 47, 76, 85, 88, 103–5, 107, 109, 137–8, 156, 158, 175, 183–4, 188–9, 191 as spawning cue, 102 Planktonic food and food sources, 102 for Asteroidea, 104–5 for Crinoidea, 102 for Echinoidea, 105–6, 109 for Holothuroidea, 103–4 for Ophiuroidea, 102–3 and spawning periods of the green sea urchin, 107–8 Polychlorinated biphenyls (PCB), 180 Prey–predator interactions, 184 Proximate exogenous control, on reproduction, 14 Proximate factors, in control of reproduction, 4 Pseudo-copulation, 122 Pyloric caecum index, 23
R Radial nerve factor (RNF), 160–162, 165, 167 Reproductive activity, 2, 9, 15, 21, 25, 37, 54, 71, 101, 118, 151, 170, 175, 189, 192 Reproductive cycles, 2–4, 8–15, 19, 21, 23, 25, 29, 32, 35, 37–9, 41, 45-7– 50, 61-2, 65, 68, 70, 72, 75, 88, 94, 102, 104, 109, 114, 116, 119, 139–40, 143-5, 148-9, 152–3, 155, 169, 172-3, 176, 181, 185, 189, 191-2. See also Gametogenesis of Asterias rubens, 147 of asteroids, 67 of crinoids, 9, 171 in deep-sea echinoderms, 178 food supply on, 49 impact of global climate change on, 179 influence of intra-site variability on, 178 inter-annual variations in, 193 latitudinal variability in, 151 of ophiuroids, 16, 38 and photoperiod/temperature regimes, 33 of sea stars, 11 and seawater temperature, 26 timing of, 93 S Salinity, as spawning cue,120 in Echinoidea, 121 in Holothuroidea, 120–1 in Ophiuroidea, 120 Saponins, role in reproduction, 66 Sea cucumbers, 5, 58, 66, 103, 110, 119, 134, 160, 162, 176, 191. See also Holothuroidea Sea lilies, 5. See also Crinoidea Sea stars, 8. See also Asteroidea; Asteroids direct inducer of spawning in, 164 gonad and pyloric caecum indices, 45 inshore migration of, 125 Leptasterias polaris chemical communication, 62 spawning of, 97, 131, 174 Pisaster ochraceus gametogenic cycle in, 183 pyloric caeca of, 44, 67 radial nerve factor (RNF) in, 160 reproductive cycles of, 11 reproductive events in male and female, 44 sexual communication in, 135 steroids on gametogenesis in, 68 Sea urchins. See also Echinoidea; Echinoids breeding in, 153 chemical communication between individuals, 175 initiation of gametogenesis in, 29 phytoplankton as spawning inducer, 175 pollution-induced disturbance in, 181
302 Sea urchins (cont.) relationship, of temperature and spawning in, 100 sperm motility and exposure to phenols, 180 Strongylocentrotus droebachiensis artifical induction, 158 breeding, 153 chemical communication, 137 exogenous factors, 91, 100 gamete shedding, 174 gonad growth and gamete production, 52–3 gonad index, 176 heterospecific spawning, 138 lunar cycle, 117 methodological consideration, 171 photoperiodic control 28–31 phytoplankton, 105 variability in changes in GI in, 176 Seawater temperature, 11, 15–16, 18, 23, 25, 27, 33, 76, 85, 91, 94, 97, 101, 140, 146, 171 Sex ratio, 5–6, 59, 63, 128, 148 Simultaneous heterospecific spawning, 138–9 Spawning, 73–167 cues, 74–6, 89, 114, 117, 122, 125, 128, 133–4, 146, 156 in the early spring, Holothuroidea, 88 in echinoids, 87 embryonic development and duration of larval phase, 175 evidence of, 75 external signals and transduction into, 3 factors, influence in crinoids, 76–7 heterospecific simultaneous, 190–1 inducers, 105, 123, 129, 156, 158, 164, 166 in situ observations in holothuroids, 79–4 in laboratory, 75, 77–8, 85, 87, 89, 91–3, 96, 109, 119, 126, 129–30, 132–3, 135–7, 139, 142, 157–8, 170, 172, 174–5, 190–1 at low tide, 118 inter-annual differences, 179 in marine invertebrates, 74–5 mechanisms of final oocyte maturation, 162 of Ophidiaster granifer, 92 in ophiuroids, 77 in Parastichopus californicus, 88 periodicities in class Asteroidea, 85, 87 periodicities in holothuroids, 77–8, 85 periods of (Cucumaria frondosa), 144 periods of, in sea urchin Echinometra mathaei, 151 Evechinus chloroticus, 149
Subject Index
in population of Paracentrotus lividus, 89 role of 1-MA in inducing, 165 of sea cucumber (Cucumaria frondosa), 92, 144 in sea star (Marthasterias glacialis), 92 in sea urchin, 88 of sea urchin (Paracentrotus lividus), 154 seasons, 77 thermal shock, inducing spawning, 156 Sperm, 13, 55, 85, 87, 115, 122, 125, 129–38, 157–8, 160, 165, 180, 193. See also Spermatozoa Spermatogenesis, 28, 33, 40–1, 67, 71, 180. See also Gametogenesis Spermatozoa, 27-30, 42, 48, 55, 60, 74, 130, 173. See also Sperm Spontaneous spawning, 75 Steroid levels, and variations in gonad size in asteroids, 67 Storage/translocation, of nutrients, 8 Stress-induced gamete release, 175 T Temperature. See also Seawater temperature in regulation of spawning, 93 Asteroidea, 97–8 Crinoidea, 93 Echinoidea, 98–102 Holothuroidea, 95–7 Ophiuroidea, 93–5 and reproduction in echinoderms, 14–15 as spawning cue, 93 Tidal cycle, 118 Tides and currents influencing spawning of asteroids, 120 and reproduction of intertidal holothuroids, 119 and reproductive periodicity of ophiuroids, 119 water movements and reproduction of echinoids, 120 Time of day, influence on spawning, 89–92 in Asteroidea, 92 in Crinoidea, 89 dendrochirotids, light as potential spawning cue, 91 in Echinoidea, 92 in Holothuroidea, 90–2 in Ophiuroidea, 89–90 Tributyltin (TBT), 180 Triphenyltin (TPT), 179 Triterpene glycosides, in sea cucumbers, 66
