Dung Beetle Ecology

Pscrrdo,mlor.irr grosra

Ecological Pnrarr~etolr

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6.0 5.2 5.5 3.3

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6.0 4.3

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R R

4.3 5.8

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T T

T T

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T T

4.8

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4.0 4.3 4.4 3.4 4.8 6.8 13.0

~ u r r sHU. : EL. MI. and CA indicate that the species prefers human. elephant. or mixellanenus dung UT crrrion. rcspcctivcly. D, diurnal: N. nocturnal: R, rollers; T, tunnelers.

.

..

. ... .

,

206

’

. African Tropical Forests

Chapter 11

to predation, Vadon (1947) reported that the diurnal A . goudori firmly wedges itself in the angle between two branches for the night. We have observed this behavior in Tay and Makokou in the small tunneler Onthophugus deplunurus and the large tunnelerpseudopedaria grossu, both of which are nocturnal. The latter species was found sleeping on low plants at day time, wedged between a leaf and a stem. Such ”rest perching” may occur at night in diurnal species, though we have not made any observations.

.

11.4. DUNGBEETLECOMMUNITIES Species Richness

.Table :I 1.4 compares the numbers of dung beetle species in five localities in the Ikry Coast and two in Gabon. In the localities with a rich mammalian fauna, and where elephants are still present, there is no significant impoverishment of the beetle fauna from the primary to the secondary forest (Table I I .4, localities b and c, both in Gabon; see also Nummelin and Hanski-1989). On the other hand, there is a clear decrease in species number when the forest becomes simplified in its structure and the mammalian fauna, either due to increasing altitude or decreasing area in the case of the “gallery” forest (Table 11.4, locqlities d-g). In the dry, deciduous forests in the northern Ivory Coast, there a& only a f e w v u e forest dung beetles. while savanna species penetrate to these forests (Cambefort 1984). The different dung beetle tribes are not equally affected by forest impoverishment. The Sisyphini and Onthophagini are always present, while the Dichotomiini (Heliocopris) and Oniticellini are more restricted to extensive forests with good mammalian fauna.

207

TnnLE I I.4 Thc expected numbcr of species in B sample of 300 individuals in seven localitics and four diffcrcnt typcs of forest in West Africa (riuefxlion, mean and standard deviation).

23.8 1( e ) 50.96

Size Diurnal dung beetles are significantly smaller than nocturnal ones (means 49 and 250 mg, respectively, t = 4.4, P.CO.001).In forest, the size difference between diurnal and nocturnal species cannot be explained by excessive elevation of body temperatures in large diurnal species (Chapter 3). Predation may play some role, though many of the insectivorous predators are themselves nocturnal. Omnivore dung specialisk are smaller than elephant dung specialists, but the difference is significant only in nocturnal species (Table 11.1). No large species is found in the canopy, nor feeding on camon, and only one was found perching on leaves. There is’no relationship between the individual size and abundance in Tai, with small and large species bcing, on average, equally abundant. There is consequently a good relationship between the biomass of the species and its fresh weight: the heaviest species are the most dominant in biomass and generally also in resource use.

.

N u m : The forest lypes ace: I, primary UT old secondary faren, 2. s e c o n d q forest in patchy andlur expluited stale; 3, iiiunlme ruurerl: 4 , riverine (gallcry) secondary furear. The localities we: a. Tar. Ivory Coast: b. Makokou. Gsbon: E . Nzoua-Meyang. Gabon: d. Sipilou. Ivory Coast: C. YfalC. Ivory Coisl: 1. Mounl Tonkoui (1.200 !IO, Ivory Const; p. Lomtu. Ivory Coust. See Appyndix A. t I 1or the ~ n a n m d i a nfaunas.

* Sasiplc of 247.

Dung Beetle Guild5 The four main types of dung beetles, the rollers, the tunnelers, the kleptoparasites, and the dwellers (Chapter 3 ) , are all present in Afrotropical forests. 1 The kleptoparasites are, however, verykare, and only one species of Pedaria has been collected in Makokou, where it probably exploits the brood balls of large Cuthursius species. Rollers. It is well known that the rollers as a group are more dominant in open habitats than in forests (Halffter and Matthews 1966). There are only five roller species in Tal and four in Makokou, and only one or two species are abundant. All the species are diurnal, and some of them can be found perching on leaves or occurring in the canopy (Section 11.3). Though the poor representation of rollen in forests is obvious in the Ivory Coast, it is difficult to explain. Rolling a ball across grass stems is more difficult than rolling balls on the almost bare forest floor. The efforts made in rolling may require high body temperature (Heinrich and Bartholomew 1979a,b), which.is easier to achieve in open savanna than in forest. Neosisyphus cui, which occurs exclusively in deep-forest shade, is always very slow in its ball-rolling movements. Sisyphus eburneus, another forest species, is very fastmoving,( both while rolling a ball and in flying away when disturbed from leaves where it was perching, in this case perhaps to increase its body temperature. Tunnelers. There are sixty-seven species of tunnelers in Tgi and sixty-two species in Makokou. Large tunnelers are more numerous in Makokou, pmbably because of the exceptionally rich manunalian fauna in this locality (Section 11.2). In Tay, the tunnelers include twenty-five diurnal and forty-two nocturnal species,.of which the former are more abundant but have a lower

208

'

Chapter I 1

average biomass per species than the nocturnal ones. Although the forest dung beetle fauna is impoverished in comparison with the savanna fauna, several pairs of seemingly very similar species occur in forest, especially in Ontho-: phagus (e.g., U . srrictestriatus-tenuisrriarus,fuscarus-fuscidorsis, hilaris-hilaridis). A pair of similar large tunnelers occurs in elephant dung, Copris ca-' merunus and Onitis nemorafis. The former species occurs under trees, the latter on tracks. This difference may be due to the washing of the shallow soils on the tracks, Unitis perhaps being restricted to the poorest sites, as in thc savannas (Chapter 9). Shallow soils undoubtedly explain why the nests of the tunnelers are noticeably shallow in African forests, even those of burrowers as skilled as Heliocopris and Onitis. Small tunnelers may be able to construct their small nests in the cracks between rocks and gravels, hut the large ones do not have this possibility. The brood halls of Copris andHeliocopris are always covered with a layer of soil, which may have a defensive function. The large Hefiocopris larvae m, aggressive and try to bite an intrudei, while the female in the nest stridulates energetically when disturbed. These features are more evident in the forest than in the savanna, perhaps due to a greater risk of predation in the forest. Dwellers. Must Aphodiinae, the archetypal dwellers, are small in size. Aphodius egregius and A . wittei, two African forest species, are two examples of exceptionally large species, both measuring 18-20 nun. These species in fact dig burrows and function as tunnelers. Tegumentary expansions, or horns, which are frequent in Scarabaeidae but rare in Aphodiidae, are present in A . renaudi males. It appears that the Afrotropical forest Aphodius are unusually similar to Scarabaeidae in their biology. i 1 S.FOREST-SAVANNA COMPARISON

Africa is the only continent with extensive tracts of both rain forest and savanna. In this section we compare the dung beetle faunas of these two biomes using data from two closely situated localities, Tay forest and Kakpin savanna (Chapter 9) in the Ivory Coast, Both study localities are situated within national parks with rich mammalian fauna. The results are summarized in Fig. 1 i .3 and Table 11.5. Species richness is clearly lower in forest than in savanna, both in traps baited with h ~ m a ndung- and in elephant dung pats, and regardless of whether calculated as.the number of species per trap or per three hundred individuals (Fig. 11.3). The number of individuals per species i s lower in forest (46) than in savanna (92), but the really striking difference is in beetle density: traps baited with human dung attract forty times more individuals in the savanna than in the forest, and elephant dung pats have six times more individuals.

African Tropical Forests HUMAN DUNG

300i

'

209

'ELEPHANT DUNG

T

T

'83

S SPECIES 300 IND.

SPECIES INDIVIDUALSSPECIE%

3M IND

Fig. .I I .3. Comparison of dung bcetles attracted to hum" and elephant dung in forest (Tal) and sawnnil (Kakpin) in the Ivory Coast. The columns give rhc numbers of species and individuals, and rhc cxpccted nuntbcr of specics ill a semplc of thmc hundrcd individuals. Dark columns are for forest. light columns for savanna (dara from Appen-

dixcsB.~andn.~I).

TAIJLE 11.5 Cmupttriscm of dung bccllc assembk~gesi n trupical forest (Tei) and in savm~ra(Kakpin) in Ivory Coaal. Savanrio

Furesl

Pcrccnlagc of diurnal

Pcrccntsge ofrollers

Pcrccnrvgc of large tunnelers*

Pcrccnugc of klcptoparasitcs

'

N

B

49

a7

I6

50 Y 10

45 55 31 I

S

N

B

S

42 7 22 0

62

25

8

2

8 0

62 0

24 10

N o m :S. N. and U dcnole species. individunh. and biomw, respeclivcly. See also Table 11. I mdFigs. I l . 2 a n d 11.3. * Longer than 13 mm.

(Fig. 11.3). The respective factors are six and three for the numberofspecies. A complicating filctor is that the radius of attraction of a trap or a pat may be somewhat greater in the open savanna than h t h e closed'forest, but this difference can hardly explain more than a small psrt of the observed difference in density. We d o not have seasonal data for Kakpin, but we can compare Tai' with another savanna locality,, Abokouamekro (Fig. 11.2). Although the forest dung beetle community appears to be as clearly seasonal as the savanna community, Ihc peak abundance of beetles OCCUE in the second half of the year in lhe forest, not in the lirst half as in the savanna. About half of the species are diurnal in both biomes, but in terms of individuals the diurnal ones dominate

210

’

Chapter I 1

the community especially in the savanna (Table 113). The savanna species are larger, on average, than the forest species, especially among the nocturnal ones (Table 11.1). Taxonomically, the forest and savanna beetle assemblages are rather similar. Scarabaeini and Canthonini are absent in our forest samples, but they are relatively scarce also in the savanna. The other rollers, Gymnopleurini and Sisyphini, are relatively more numerous in savanna, especially in numbers of individuals, while Oniticellini are relatively more abundant in forest, apparently benefiting from the relatively weak competition with large tunnelers. lo: both biomes, the Onthophagini is the dominant ttibe, but,even more so in the forest. Finally, there are two substantial differences between the two biomes in terms of the functional groups of beetles: the rollers are much more numerous in the savanna, especially in numbers of individuals; and the kleptoparasites are absent (Tail or nearly absent (Makokou) in forest but represent 10% of the dung beetle fauna in savannas (Table I 1 3). These comparisons clearly indicate that Afrotropical savanna and forest dung beetles belong to the same taxonomic pool and that their differences are quantitative rather than qualitative. Generally, the savannas have a richer assemblage of dung beetles than the foksts, and the density of beetles is much higher in the savannas. The oldest Scarabaeidae groups, Canthonini and Dichotomiini, have practically disappeared from both forests and savannas, hcing present only in the southernmost part of the continent (Chapter 4). The simplest explanation of the greater diversity and higher density of dung beetles in savannas is the greater availability of resources there than in forests. Some groups of species, especially the rollers Gymnopleurini and Sisyphini, have obviously diversified in savannas.and secondarily penetrated to forests, but it is difficult to draw any similar conclusion about the other tribes.

C H A P T E R I2

Dung Beetles in Tropical American Forests Bruce D . Gill

12: I , INTRODUCTION

Central and South America enclose the largest expanse of tropical forests in the world, with a long evolutionary history and a rich fauna of dung beetles. Nearly all tropical American dung beetles belong to the family Scarahaeidae, with only a few species representing the Aphodiidae, Hybosoridae, and Trogidae. Many groups of dung beetles in tropical America are stili poorly known taxonomically, especially the genera with predominantly small species, such as Aleuchus, Conthidiurn, and Uroxys. Lack of revisionary work and the presence of many undescribed taxa makes identification diftictllt and has led some workers to study only the larger and more easily recognized species (Wille 1973; Wille et al. 1974; Janzen 1983221, while others have resorted to arbitraly numbering systenis (Howden and Nealis 1975; Peck and Forsyth 1982). Although this latter approach has permitted the study of entire dung beetle assemblages, it has also made comparisons between different localities difficult if not impossible. To alleviate this problem and to facilitate ecological work, Howden and Young (1981) completed a taxonomic monograph on the Scarabaeidae of Panama. Much of this chapter is based on fieldwork conducted in Panama and Costa Rica. The term “dung beetle” is taxonomically ambiguous since the habit of coprophagy is shared by taxa within several different lineages of the3carabaeoidea (Chapter 2). On the other hand, many species of the true dung beetles (Scarabaeidae) do not feed on dung but use other resources such as camion or decomposing fruit. Such diversity of feeding habits is especially ch acteristic of neotropical dung beetle assemblages and undoubtedly contribu es to the high species richness in this region. Historical events such as the megafaunal extinctions of the Quaternary (Martin and Klein 1984) have probably favored dung beetles capable of exploiting altemati food resources. To better understand the modern dung beetle commnnitie .and the evolutionary history that has shaped the present fauna, it is important io consider all the species of Scarahaeidae regardless of their present feeding habits.

7

r

212

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Chapter12

12.2. BIOGEOGRAPWY

den an Nealis (1975) tor Colombia.

Physical Setting

Lowland tropical forests covered much of South America by the close of the Cretaceous (Raven and Axelrod 1975). Miocene and Pliocene orogenies (Harrington 1962) fragmented lowland forests while giving rise to montane habitats. Other types of forest as well as savannas probably developed in responsc to changing patterns of rainfall due to changes in topographic relief. Orogenic activity was also responsible for completing the Central American land bridge 3 million years ago (Marshall et al. 1979), providing the first direct forest connection between the North and South American faunas. Reduced rainfall resulting from lowered sea levels and lowzred temperatures during the Pleistocene is thought to have shrunk the tropical forests into isolated refugia (Haffer 1969, 1974; Prance 1973, 1985). Pollen analyses from sites in South America (summarized in Absy l9E5) indicate that savannas expanded several times, with forests presumably contracting to areas of higher rainfall. The existence of refugia has been used to explain speciation and distributional patterns in a variety of organisms, including birds (Haffer 1969). lizards (Vanzolini and Williams 1970) and butterflies (Brown 1982). Climatic changes may have also contributed to the extinction of many species of mammals (Patterson and Pascual 1968), giving rise to the current fauna, which is, in comparison with other continents, relatively poor in large mammals. Within historical times, tropical forests have extended from approximately central Mexico to northern Argentina. Spanning 50 degrees of latitude and a wide range of elevations, these forests encompass an exceptionally rich assemblage of plant species. Forest classifications are traditionally based on relief, seasonality, biomass, and the presence of specific plant forms or taxa. For many groups of animals, including dung beetles, floristic paramelers and plant biomass are perhaps less imponant th& topography and seasonality in determining suitable habitats. Therefore, while discussing habitat associations of dung beetles, I shall use the Holdridge Life Zone system (Holdridge 1967; Holdridge et al. 1971). The present status of tropical American forests is precarious. Most forested areas have been severely reduced in size during the past 50 rears, and the remaining areas continue to be lost at a catastrophic rate (Caufi~ld1984; Myers 1984). Amazonia had a forest mosaic that covered much Pf its nearly 6 million q u a $ kilometep as late as the 1970s (Pires and Prance 1977, 1985). but vast regions have been destroyed in the last few years. The situation in Central America is no better (D'Arcy 1977): Janzen (1986) estimates that less than 2% of the original tropical dry forest of western Mesoamerica remains. The wholesale disappearance of forests is likely to cause the extinction of most dung beetle species along with many other forest animals, as shown by How-

213

m g beetles in clearings of wet forest at eticia,

Biogeographical Trends among Dung Beetles

:

.

Three genera of Hybosoridae-Ailaides, Chaetodus, and Coilodes-are occasionally found in dung and carrion in lowland and montane forests. The lethargic behavior OF hybosorids (Young 1983) suggests that they are not successful competitors when Scarabaeidae are present. Among the Aphodiidae several species of Aphudius and Araenius are frequently recorded from lowland forests (Howden and Nealis 1975; Peck and Forsyth 19821, and Aphodiidae are abundant in pastures and clearings both in lowland and montane habitats in Panama and Costa Rica. In forests the importance of Aphodiidae is. however, eclipsed by the much richer and more active fauna of Scarabaeidae, with about twelve hundred recognized species in tropical America (see Table 4.1). The true species diversity may be much greater since the largest tribe. the Dichotomiini, is also one of the least studied. In lhc Onlhophagini, represented by Oiithoplragirs, species number decreases rapidly from Central,to South America:'Central American Oiirhophagus occupy a variety of forests from sea level to'over 2,000 m, and they use a wide range of food resources. The 0niticellini.h~no species extending into the forests of Cintnl America or South America, and of the nineteen species of Central American Cupris (Coprini), only C . iiicertus has a range that cxtcnds to South Anierica (Matthews 1962). The Central American Copris are.primarily dung feeders found in pastures and in low and middle elevation forcsts. The Phanaeini is a predominantly tropical group endemic to the New World (Edmonds 1972; Chapter 4). The approximately fifty species of Phanaeus are distributed from the eastern United States to Argentina, with about half of the species occumng in Mexico. Central and South American Phariaeus are diurnal dung keders found in dry, moist, and wet forests; the dry forest species often venture to open pastures. Coprophanaeas is found from Mexico to Argentina but is most numerous in South America. The thirty or so described species are crepuscular or nocturnal and feed mainly on vertebrate anion. The subgenus Megapharmeus includes the largest New World dung beetles with lengths exceeding 50 mm. Oxysrernon and Sulcophanaeus are diurnal dung feeders widely distributed in South American forests, with only a few species extending to Central America. The Dichotomiini has twenty-three genera and nearly half of the dung beetle species in tropical America. Dichotornius includes medium-sized to large nocturnal dung feeders, which are often very abundant in forests. About half of

F

214

Tropical American Forests

. Chapter12

the' twelve Central American species are found in low- and middle-elevation moist forests, while the remainder occur in dry forests and pastures. Ateuchus, Canthidturn, and Uroxys are ubiquitous members of the dung beetle assemblages in tropical America, with numerous species found over a wide range of forests and exhibiting a variety of feeding habits. Some of the larger species of Uroxys as well as some Pedaridium and Trichillum are phoretic upon sloths. Several species of Ontherus live in the nests of leaf-cutting ants. The Eurysternini is restricted to the New World, with twenty-six species oT Eurysternus (Jessop 1985; Martinez 1988). These species are mostly dung feeders and occur in a wide range of tropical forests from Mexico to Argentina. Another South American group is the Eucraniini, ,which is. restricted to the arid and semiarid regions of Argentina. The Sisyphini is represented by two Mexican species of Sisyphus (Howden 1 9 6 3 , one of which (S.mexicanus) can be found in tropical dry forests as far south as Costa Rica. Another exceptionally successful group of dung beetles in tropical Amcrica is the Canthonini, which is also relatively will studied with over three hundred described species. Of the twenty-eight currently recognized genera (Halffter and Edmonds 1982), about ten areponotypic and another ten have five or fewer species. The remaining genera include several that are predominantly West Indian (Canthochilum, Pseudocanrhon, and Canthonella). The fourteen species of Cryptocanthon are widely distributed over Central and South America. Cryptocanthon and Canthonella include very small species, less than 3 mm in length, which are abundant in the deep litter of wet habitats, especially cloud forests, Malagoniella (9 species) and Scybalocanfhorl (16 species) are widely distributed in lower-elevation dry and moist forests of Central and South America. Deltochilum and Canlhon are the largest genera of New World canthonines, with 76 and 148 species, respectively. Deltochilum is widely distributed over lowland and montane forests of tropical America, with large and small species feeding on can'ion and dung. Canthori contains small to medium-sized species that are predominantly dung feeders, although a few have become carrion specialists. Most species of Canlhon are restricted to forests below 500 or 1,000 m in elevation.

215

more even in space and time than the availability of fresh carrion, and the dung of smaller mammals is more evenly spaced than the dung of larger mammals. Beetles specializing in small mammal dung may be expected to show the lowest level of aggregation in space. Locating carrion and larger dung pats necessitates B greater reliance on flight than locating the pellets of small mammals and invertebrates (see Section 12.4 on foraging behavior). Dawn and dusk are the two periods when the defecation rate of mammals might be expected to peak due to a change in activity in both diurnal and nocturnal species. The activity patterns of many dung beetles seen] to be geared IO these periods (Section 12.5). Many types of dung are deposited in places that make it difficult for dung beetles to locate and use the resources. Tapirs and pacas show a strong tendency to defecate in water, while sloths descend to the ground to bury their dung. Unusually long periods of time between defecations in sloths impose problems that may have favored the development of phoresy in several species of U r o q s and Trichill~rruthat specialize in sloth dung (Ratcliffe 1980). The dung of many arboreal mammals is released high in the canopy, with the result that much of it is available only to beetles that forage in the canopy (Section 12.5). Fossorial mammals may defecate within burrow systems, making their dung unavailable to most beetles.

'

Allernalive Food Resources

.

Temporal and Spatial Avuilabiliv of Food

: '

.

Tropical American dung beetles utilize a variety of food resources other than mammalian dung. Among the records pertaining to the dung of nonniammalian vertebrates, Young (198 1) recorded Cantlion moniliatirs and Onthophagus sharpi in traps baited with iguana and boa constrictor feces, and 0. sharpi, Ateuchus candezei, Canrhon lamprimus, Uroxys gorgon, and U . micros at toad feces on Barro Colorado Island. Onthophagus nyctopus and Sulcoplianaeus nocris have been trapped with fresh Anteiva lizard dung in Costa Rica (Gill, unpubl.). Records of dung beetles using bird droppings and guano include Anontiopus wittmeri in northern Argentina (Martinez 1952), canthonines in Puerto Rico (Matthews 1 9 6 3 , Onthophagus hopfrieri in Guanacaste, Costa Rica (Janzen 1983b3, and Canthidium ardens pushing chicken droppings in western Panama (Gill, unpubi.). Zonocopris gibbicollis is the only known example of a tropic Amerlcan dung beetle that feeds exclusively on nonmammalian dung. Adults of this unusual canthonine are phoretic on large terrestrial snails (Arrow 1932) and presumably feed on the dung produced by their gastropod host (Martinez 1959). Larval habits of this species are still unknown. Snail excrements are also used by several canthonines in Puerto Rico (Matthews 1965), but none of these is restricted to this type of dung. The frass of large lepidopteran larvae is a potentially important resource for many of the smaller dung beetles, but this possibility bas been little studied. Only two species, U . gorgon and Dichorurn-

?

12:3. FOODSELECTION AMONG TRoPlCAL AMERICAN DUNGBEETLES

The conditions of high temperature and humidity that are responsible for the luxuriance of plant life in tropical forests also favor the rapid breakdown of dung, carrion, and fruit. Successful scavengers must be able to locate and secure these resources as quickly as possible. The availability of fresh dung is

'

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:

216

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Chapter 12

ius fernoralus, have been reported on caterpillar droppings (Howden and Young 1981). In addition to insect droppings, tropical forests produce a rain of plant debris that is exploited by some dung beetles. Mature and rotting fruits are particularly attractive to a variety of species (Table 12.1). Many of the species recorded at fruit are generalists and can also be found on dung and camon, but a few species, such as Onthophagus atriglabrus, 0. belorhinus, and 0. carpophilus, may feed predominantly or perhaps exclusively on fruits. The genus Bdelyrus is occasionally .collected in dung-baited pitfall traps, hut their peculiar flattened shape appears to be an adaptation for living in terrestrial and epiphytic bromeliads (Pereira et al. 1960; Huijbregts 1984). These beetles presumably feed on the plant material or insect frass that accumulates in these plants. Debris piles of leaf-cutting ants are also used by dung.beetles. Halffter and Matthews (1966) list fourteen.neotropica1 species of Scarabaeidae from Attini nests, one of which, Ontherus cephalofes, has also been found in the fungus gardens and may feed on fungi. Fungal' feeding is known for ocher species not associated with ants; for example, Canthidium bokermanni and C . kelleri were described by Martinez et al. (1964) from specimens taken from Hymenomycetes fungi inBrazil and Argentina, Other records of fungal t'eeding include generalist species such as Canthon v. leechi, Deltochilum fuscucupreurn, D . granulatum, Phanaeus daphnis,. and P. endymion (Halffter and Matthews 1966). A final but significant category of alternative food resources for dung beetles is canion. Coprophanaeus, Deltochilum, and Canthon have many species that are predominantly or exclusively: necrophagous, but carrion-Feeding has also been reported for Agamopus, Ateuchus, Canthidium. Cunrhonella (as lpsellisus), Copris, Dichotomius, Malagoniella, Onthophagus, Peduridiurn, and Phanaeus (Halffter and Matthews 1966). Necrophagy is not limited to vertebrate carcasses, as species of Cunfhon andDeltochilum are reponed from dead insects and millipedes (Luederwaldt 191 1; Pereira and Martinez 1956; Howden and Young 198 l ; Janzen 1983h); Several Brazilian species ofCunrhuri are reported to kill reproductive Atta ants and to use them as carrion (Halffter and Matthews 1966). Halffter and Matthews (1966) also mention that Deltochilum koibei may attack live millipedes. The broad range of genera involved indicates that canion feeding is of major importance in tropical American dung beetles.

12.4. POPULATION ECOLOGY Seusonality Tropical insects exhibit great variability in their seasonality and year-to-year abundance changes (Wolda 1978a, 1983). Differences occur between species but also within species depending on local conditions. Variability in rainfall

Tropical American Forests

'

2 17

12. I Tropical Anicrican dung bcctlcs (Scarabacidae) recorded from fruils. TABLE

Species

Localiry Panama W. lndies Panama Brazil Brazil Panama Brazil Brazil Panama Brazil Brwil Brazil Brazil

Pallalna

Brazil Brazil Brirzil ? Brazil

Brazil

Brazil Panilma Panama Costa Rica Costa Rica Guatemala Mexico Panama

Ecuador Ecuador Mexico Panama

Panam Panama Costa Rica Pannma Panama

Panama Ecuador

Ref

Type of Fruir

Palm

6

? Palm Butia palm Butia palm Ficus

Butia palm Butia palm Solancus Butia palm Butia palm Butia p a h i Butia palm ElltadJ Butia pcllm Butis palm Butia palm Banana, avocado Guava, pineapple Coffee Palm Gusruvia Virols cicrus Citrus, banana Cacao lackfruit Solancus Banana Banana Zapate Gustavia Avocado Palm

Banana, jackfruit Palm, banana Gusuvia. maguira Gustavia Banana

I

6 II

I1 6 I1 11 3 12

I2

I2 12 6 12 12

12 9 7 I1 8 6 6 13

13

2 4

3 IO 10 ''

'

I1 6 3 6 3 6 6 6 10

218

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Chapter12

appears to be the prime factor influencing seasonality in tropical organisms (Wolda 1978b, 1982), and this seems to hold true for many dung beetles. Janzen (1983a,b) found that most dung beetles were strongly seasonal in the tropical dry forest at Guanacaste, Costa Rica, The appearance of large species, such as Dichororniur and Phanaeus, coincided with the start of the rains in early May; fresh horse dung was rapidly degraded by these and many smaller species during the first month of the wet season. By the early dry season all of the larger beetles had disappeared leaving only the smallest species, such as Onthophagus hopfneri. The severity of the dry season in Guanacaste curtails the activity of most species (Janzen 1983a). In the Brazilian state of Parana, Stumpf and coworkers (Stumpf 1986a,b; Stumpf et al. 1986a,b) found seasonal abundance changes in most dung beetle species, The numbers of Ateuchus apicatus,A . mutilam, and Uroxys dilaticollis correlated with rainfall, the minimum numbers occurring in Febr u m , the driest month of the study. In Panama: the large sloth beetle Uroxys gorgon is present throughout the year in blacklight samples on Barro Colorado Island (Wolda and Estribi 1985). where it shows a bimodal abundance pattern with increased numbers in the beginning and at the end of the wet season, and the lowest numbers coinciding with the dry season: Similar fluctuations in abundance were seen in U . gorgon Populations at Fonuna, an area with high rainfall throughout the year (Wolda and Estribi 1985). Waage and Best (1985) found a similar pattern of seasonality for the sloth beetle Uroxys best; at Manaus, Brazil, where beetles were abundant on their Brudypus hosts in June and again in December. While the numbers of U . besti and the smaller sloth associate, Trichillum adisi, were not correlated with rainfall at Manaus, the numbers of T. adisi on sloths on a neighboring island showed a strong correlation with seasonal flooding (Waage and Best 1985). Beetles were rarely encountered on sloths during the period of inundation from May to August. Since sloths must defecate into water, beetles presumably underwent reproductive diapause or dispersed to areas of dry ground. In contrast to the seasonal abundance changes observed for dung beetles in tropical dry and moist forests, Peck and Forsyth (1982) did not observe any overt seasonality among dung beetles in a tropical wet forest. Excluding rare species, therank order of species’ abundances remained constant over the wetdry season transition at Rio Palenque in western Ecuador (the “dry” season at Rio Palenque being slightly drier than the wet season). Peck and Forsyth (1982) questidn the validity of any observations of seasonality based on pihall trapping data by suggesting that differences in rainfall may limit available flight time for beetles. However, perching beetles (see below) do not seem to be perturbed by rain, and flight interception and pitfall traps baited during rain storms continue to collect beetles. But heavy rainfall can flood traps washing away specimens or the bait, while baits may dry out very quickly in the dry season, reducing their apparency or perhaps suitability to foraging beetles.

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Apart from seasonality, beetle numbers vary from one year to another, though there is very little information on this topic. Howden and Nealis (1975) compared pitfall samples taken two years apart in a wet forest at Leticia, Colombia. Species composition and the relative abundances of the dominant species at carrion and dung were not greatly changed. Estimates of actual population densities are difficult to obtain since little is known about the distances traveled by beetles collected in traps. Wille et al. (1974) attempted to trap out the adult population of the large canthonine Megothoposoma candczei from a 3.8-hectare patch of isolated forest in Costa Rica. Fifty-six individuals were removed, giving a density of 15 beetles per hectare. Peck and Forsyth (1982) used a mark-recapture technique at Rio Palenque to estimate total population size for all dung beetle species in a forest of 80 hectares. Of 2,178 beetles marked and released over a 3-day period, only 41 were recovered in a recapture sample of 3,184 beetles, giving an estimate of over 2,000 beetles per hectare. Foruging Modes mid Dispersal

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Dung beetles have ’evolved specialized foraging techniques to rapidly locate and utilize suitable food resources. Prompt detection is especially important in tropical forests, where the combination of high temperatures and rainfall hastens the deterioration of perishable materials such as fresh dung. All dung beetles rely upon olfactory sensillae in the antennae to detect airborne food odors. Arrival at suitable resources is generally accomplished by flight, with the exception of a, few flightless species associated with montane habitats: Gypiocmirlmit species (Howden 1973, 1976) and Oirfliophuglrs rilicroplerus (Zunino and Halffter 198 I) among tropical American species. Fully winged dung beetles detect food odors during cruising flights or while perching on vegetation, and most species exhibit a strong preference for one of these two basic foraging techniques. Cruising species can be loosely divided into fast and slow Hiers. Fast fIiers, such as the Phanaeini, are easily detected by the loud buzzing sound they produce during flight. These.species may be tlying close to the maximum range velocity (Pennycuick 1982) to cover as much terrain as possible during flight. Oxysternon and Phanaeus are generalist dung feeders that have flight periods lasting many hours per day. Coprophanueus are carrion specialists that fly for a short time, usudlly less than 30 min, at dusk and dawn. It is tempting to speculate that carrion specialists have shorter flight periods because the temporal availability of fresh camion is much less predictable than the supply of fresh dung: powered flight is not an efficient method of passing time while waiting for the appearance of fresh,’carrion. A short high-speed flight may be sufficient to determine whether a carcass is locally available on a given day. Shon periods of rapid flight are also seen in species other than carrion spe-

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cialists. Onthophagus belorhinus and 0. mirabiiis have flight times of 2WO min at dusk in the lower montane wet forests of western Panama (Gill, unpuhl.). These species can be collected ai a wide variety of resources that include dung, canion, and f d t . The fact that the foraging periods of unrelated species (Coprophanaeus and Onthophagus) coincide at twilight may indicate that predation pressure on dung beetles is temporarily relaxed during these times. Slow flight is typical for nocturnal species of all sizes and for some diurnal species. Slow fliers may.be flying at the minimum power velocity (Pennycuick 1982) to reduce energy costs while maximizing the period of time they are airborne and searching for food. For many of the larger nocturnal species, for exampleD. satanas, slow flight also eliminates the production of buzzing sounds that might be picked up by foraging bats. Slow flight among diurnal species may be selected against by increased predation from aerial predators such as the asilid flies (Sectfon 12.4). On Ban0 Colorado Island, only Canthon e. s a k i and C. moniiiatus appear to flyat the minimum power velocity. These two species are brightly colored and vely conspicuous while they slowly meander over the ground at the height of 15-30 cm. Carzthori c. sollci is known to produce a secretion that repels blowflies from its food (Belles and Favila 1984). Beetles captured in flight have a distinctly unpleasant aroma (Gill, unpubl.), whicH may confer some form of protection from diurnal predators (Section 12.4). Canrhon moniliatus may ‘alsobe chemically protected, or it may be a Batesian mimic of C . c. sullei. Like the slowly flying species, beetles that perch on vegetation may increase their foraging time without excessive energy expenditure. Perching beetles can be readily divided into two groups. Selective height perchers are found over a narrow range of heights above the ground. The average perching height for these species is usually between 10 and 50 cm above the ground and is strongly correlated with body length (Howden and Nealis 1978; Gill, unpubl.). The nonselective height perchers are found over a broad range of heights, and they apparently perch for a variety of reasons. Selective height perchers are specialists on small, scattered resources, such as rodent droppings, which are potentially much more evenly dispersed in space and time than the dung of larger mammals. Certain dung beetles have adopted perching as a,“sZt and wait” tactic for locating these small resource patches. Since larger beetles require larger droppings, they presumably perch higher up tq.avoid being distracted by odors from resource units that are too small to be utilized. Field observations on Barro Colorado Island (BCI) suggest that beetles using this strategy may increase their chances of locating food by perching downwind of mammals. Canthidium aurifcx is active throughout the day on BCI (Fig. 12.1) with peak flight times in the beginning and at the end of the day. Between these two “rush hours,’’ beetles spend most of their time perching on leaves about

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HOURS OF THE DAY Fig. 12. I . D i d nctivity 01 sclccted specics of duiig bccllcs illustrating diflcrcnt pattcn1s. Top fcll: cx;unplcs of species showing curythcmiic ilighl activity (I, C
25 cm above the ground (Fig. 12.21, with occasional flights to new perches. Seeding a study plot with human dung results in a noticeable increase in the numbers of beetles perching downwind. Large concentrations of perching beetles were often found on vegetation, although no dung was apparent in the vicinity. On one occasion several dozen Carirhidiwn aurifex and C . haroidi were found on a bush immediately downwind from where an agouti l y d been sitting for 20 min. All of these beetles departed within some minutes of the agouti leaving. The absence of dung and urine indicated that the beetles were pcrching in response 10 the odor of the mammal, and were waiting for thc appcarance of food. Nonselective height perchers may also use perching as a means of increasing foraging tinie while reducing the cost of flight, but these species are not specialists on ground-based resources. In contrast, most of these species use resources, such as monkey dung, that are distributed over a range of heights

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were recovered at distances of 180 and 700 m after two days (Peck and Forsyth 1982).

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HEIGHT ABOVE G R O U N D (cm) Fig. 12.2. Perching height distributions in two spccics of dung bcetlca on Barro Culorad0 Island, Panama. (a) Canihidium rrur.$?z, B cclcclivc height pcrchcr (uppcr pmcl): and ( b )Canlhan angustofus, a nonselective height pcrchcr llower pancl).

above the ground. Canthon angustatus is a typical nonselective height percher that can be found on leaves up to several meters or more above the ground (Fig. 12.2). Since C. angustatus usually perches only in the vicinity of fresh howler monkey dung, perching beetles may he waiting fur fresh dung to fall or the opportunity to steal the dung ball of another C . angustatus. In addition to searching for food odors, some species of dung beetles use perching for thermoregulatory purposes. Young (1984) has reported that Carlrhon septemmaculatus preferentially perches on leaves that are located in sun flecks. Eurysrernusplebejus also shows this behavior on BCI (Gill, unpubl.). By elevating their body temperatures, beetles may be more successful in foraging or in avoiding predators. Differences in foraging behavior such as perching versus flying may affect the dispedal ability .of a species. Among the species that rely upon Right, some of the fast fliers (Phan&us and Oxysternun) are widely distributed over Central and northern South America. The slow-flying Canrhon cyanellus also has good dispersal ability (different subspecies range from the United States to Venezuela), perhaps because it has a long period of daily Right activity (Section 12.5). Individual beetles may cover large distances; for example, Ox‘.ysternonconspicillatus flew at least 1 km in two days, and some Onthophagus

Dung beetles fall prey to a wide variety of predators. Janzen (1983a, 1983c) describes graphically how Eulissus chalybaeus, a large staphylinid beetle, consumes sinall and medium-sized dung beetles (Dichotomias yrrcatanrrs, Onthuphogus chainpioni, and Canthidim centrule) in Guanacaste. The predatory beetles fly to fresh dung pats, where they await the arrival of their prey. In the lower montane wet forests in Costa Rica, another large staphylinid, Leistotrophus versicolor, is found on fresh dung where it feeds upon large blowRies (Gill, unpubl.) and probably also on small dung beetles. The tiger beetle Megucephula afjinis is reported to prey on Onhophagus landolti and 0. murginicollis from beneath cattle pats in a Panamanian pasture (Young 1980a). The assassin bug Apiomerus ochropterus is a conspicuous predator on leaf surfaces on BCI (Gill, unpubl.), where it must frequently encounter the common leaf-perching dung beetles, Corithidiuin ardens, C. aicrvex, and Canthoit angastorus. When disturbed while perching. the typical defensive reaction of the first two species is to retract their appendages and to “sit tighl.” Whcn confined in a jar with one A. ochroprcrus, such defense offered no protection, and the assassin hug readily consumed several beetles (Gill, unpubl.). In contrast, Canrhon aiigustarus is chemically defended, and when disturbed while perching it assumes an aposomat/c display stance with the head down, pygidium raised, and legs outstretched. When a single C. angustatus was confined in a jar with an A.’ ochroprerus, the hug approached the dung beetle with its ’ beak raised, ready to strike. Once the forelegs of the bug touched the beetle, the beetle instantly dropped into a display stance and released a strongly smelling odor that caused the normally staid bug to flip over backwards and to retreat to the far side of, the jar. The release of this odor was an effective delense, as the bug showed no further interest in repeating the experience. In a study of the prey captured by Argiope argentam spiders on BCI, Rohinsori and Robinson (1970) found that Scarabaeoidea constituted 1.3% of the total prey biomass Over a 12-month period. Most of these were proba y small dung beetles that are common in the area and likely to be caught in lyw-lying spider webs. Aerial-foraging robber flies prey on dung beetles. One example is Senobasis cursair, a common robber fly on BCI (Shelly 198s). T. Shelly (pers. comm.) recorded 178 captures of prey, 74% of which were beetles, and most of the latter were small metallic-colored dung beetles, including Areurhus aeneomicans, C . ardens. and C. aurqex (Gill, unpubl.). Insectivorous bats may prey heavily on nocturnal dung beetles. Howden and Young (1981) report a specimen of Onrhophagiis batesi taken from the stomach of a bat in

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Costa Rica. While data on stomach contents are difficult to obtain and destructive to bats, examination of feeding roosts (Dunkle and Belwood 1982) could yield quantitative estimates of bat predation on dung beetles. Beetle fragments from bat roosts on BCI (supplied by J. J. Belwwd) contained an assortment of elytra belonging to species of Copris and Dichorornius (Gill, unpubl.).

12.5. DUNGBEETLECOMMUNITY ON BARROCOLORADOISLAND,, PANAMA BColorado Island is a 1,570-hectare reserve situated within Gatun Lake about 35 km northeast of Panama City. The island was created in 1914 during the formation of the Panama Canal and is administered by the Smithsonian Tropical Research Institute. With an elevational range of 20-170 in above sea level, BCI lies within the Tropical Moist Forest life zone (Holdridge 1967). The island is covered with a mixture of second growth and niature semideciduous lowland forest (Foster and Brokaw 1982), and it experiences a moderate dry season from late December to April. Heavy rains at the end of April signal the start of a 7-month rainy season. Additional information on the physical setting and ecology of BCI can be found in Leigh et.al. (1982). As a result of.its isolation and protected status, BC1 has maintained a rich mammalian fauna. Diversity and biomass estimates for many of the forty-two nonvolant mammals (Appendix A.12) recorded on the island compare favorably with other Neotropical lowland forests (Eisenberg and Thorington 1973; Eisenberg 1980; Glanz 1982). The dung beetle fauna on BC1 was studied for a total of 13 weeks fmm April 27 to July 7, 1981; September 2 to 6 , 1982; June 3 to 14 and September 5 to' 12, 1983. These dates correspond to carly and middle rainy seasons. Beet@ were collected using Right interception traps, two sizes of dung-baited pitfall traps. and dungbaited soil traps. Fresh human dung was used in all baited traps. Details of trap design can be found in Bemon (1980), Peck and Davies (1980), and Peck and Howden (1984). Species Composition and Abundances Combined with data from Howden and Young (1981). a total of fifty-nine species of Scarabaeidae dung beetles are known to occur on BCI (Appendix B.12). Species composition and relative abundances during the 3-month field study v&d in the.results obtained by the different sampling methods used. In dung-baited traps, the size of the bait and the height of the trap clearly affected trap catches. The use of carrion or other type of dung would certainly have affected the species composition as well. To reduce some of the biases associated with baits, flight-interception traps were used to quantify relative abundances of species. Observations of beetles Rying into these traps, however, revealed differences in Right behavior that affected trapping efficiency.

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Small diurnal species (for example, Carirhidium) fell into the collecting trough after colliding with the flight interception screen, but larger and more powerful fliers (for example, Phaiiaeus) often bounced off the screen and escaped, though some were collected as they attempted to fly beneath fhe obstruction. Large nocturnal species (for example, Canfhon aequiirocfialis and Dichotomius satanas) fly much slower than similar-sized diurnal beetles, and often hovered in front of the screen before changing direction and Rying away. Contamination of the fluid in the collecting trough with dung from passing mammals or from a buildup of decomposing organic matter changed the flight interception trap to a large "baited" trap, in which C. aequinocrialis and C. angrurarus were collected in large numbers. Unusual behavior or feeding habits may explain the supposed rarity of many. species. Uroxys gorgon should be abundant since it is phoretic on the threetoed sloth, Bradypus infuscalus, the most abundant mammal on BCI (Appendix A. 1 2), but only two specimens were collected with dungbaited and flightinterception traps during three months. However, Wolda and Estrihi (1985) collected more than twenty-five hundred U. gorgorz on BCI with two hlacklight traps over a three-year period. In the case of Ontherus breuipe~aiis,only two of the thirty-one specimens seen by Howden and Young (1981) had been collected since 1912, but twenty-three teneral and newly sclerotized adults were removed from their pupal chambers in the refuse dump of an Atfa colombica nest on BCI. With such unusual nesting and, presumably, feeding habits, it is not surprising that 0 . brevibeiinis is rarely encountered. Twoother apparently rare species are Pedaridium bonimeri and P. breviserosurn. These beetles are probably phoretic on sloths or other arboreal mammals. Confhoii,juvencus, Crrirthon inutubilis, Carirlroir v. meridioiialis. Dichotomius agenor, and Uroxys inicrocularis are abundant in the drier forests on some of the smaller islands in Gatun Lake and at Gamboa. on the neighboring mainland. On BCI such environmental conditions are restricted to some small clearings, which may limit the population sizes of these species. The two species of Copris recorded from BCI may be limited to the drier pans of the island.

Diel Activiry . The dung beetle community on BCI is composed of thirty-three< diurnal, twenty-four nocturnal, and two possibly aurorallcrepuscular species. The preponderance of diurnal species contradicts the view of Halffter and Matthews (1966) that nocturnal species predominate in tropical American forests. Noctumal species appear to be more abundant due to the great abundance of Canthon aequinocrialis (Appendix B.12), but it is difficult to say to what extent this result reflects the greater proclivity of nocturnal species to be caught in , i traps rather than their large population sizes.

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Diurnal species display several distinctive patterns of flight activity. Constant levels of activity throughout the day are exhibited by Conthon c . sollei, Canthun morsei, Onrhophagus c . panamensis, and 0 . sharpi (Fig. 12.1). These eurythermic species seem unaffected by diurnal temperature changes. Most species are more selective and show a peak of flight activity either in early morning, in late afternoon, or at midday. Speaies that remain inactive during the hottest hours of the day include Canthidium aurifcx, C. haroldi, Onthophagus acuminatus, 0. panamensis, C . moniliarus, and Oiizhuphagus’ stockwelli (Fig. 12.1). Canthidium ardens has a long flight period but does not show peak activity until 2 hours hefore dusk (Fig. 12. I). In contrast to the previous species, Canrhon lamprimus, C . septemmaculatus, E. plebejrrs, Onrhophagus coscineus, and 0 . lebasi have shoner flight periods coinciding with the hottest hours of the day (Fig. 12. I). With the exception of 0. lebasi, these species are commonly found in the drier forests and presumably have relatively high thermal preferences. Nocturnal species on BCI concentrate their Bight activity to the first few hours of darkness. Over a five-day period, flight interception traps caught thirty-four, seventeen, and three specimens of C . aequinoctialis during the first, second, and third hour of darkness. Additional specimens were seen flying in the hour hefore dawn.

Food Relocation

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Chapter I2

Dung beetles employ several techniques to sequester dung from droppings (Chapter 3). The most common.one is the excavation of burrows beside or beneath droppings, which are then packed with dung. Beetles using this technique are the tunnelers (Chapter 3), represented by Onthophagus and many of the Coprini on BCI. Because they tunnel into the soil directly adjacent to their food, tunnelers are limited to resources that are located on substrates suitable for burrowing and nest construction. Several other relocation strategies appear to have deveIoped from the basic tunneler technique. Mexican species of Phanaeus are known to push fragments of dung overland before burying them (Halffter and Matthews 1966; Halffter and Lopez 1972; HaIffter et al. 1974). On BC1 three diurnal species, Phanaeus howderii, P. pyrois, and Sulcophanaeus cupricullis exhibit similar behavior, often constructing burrows 5-20 cm away from the dropping. These beetles work in bisexual $airs, and while one beetle excavates the burrow, the other individual pushes fragments of dung to the burrow entrance. Such “head butting’’ is an above-ground extension of the behavior used by beetlcs to move dung through their underground tunnels. Halffter et al. (1974) point out that dung pushing reduces potential competition for nesting space among tunnelers. It also allows beetles to utilize dung that is located on unsuitable substrates, such as

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rocks, and may also be an effective defense against another group of dung beetles, the kleptoparasites (also called cleptocoprids; see Brussaard 1987). Kleptoparasitism is a modified tunneler strategy, in which beetles remove dung from tbe subterranean supplies provisioned by other species, most often by large tunnelers. On BCI, Onrhophagus acuminatus is a facultative kleptoparasite that provisions burrows like a typical tunneler at small droppings, but becomes a kleptoparasite at larger resource patches. Excavation of soil beneath dung pats of 200 cm3 revealed numerous 0. acuminorus at 20-30 cm depth, stealing food from the large dung-filled burrows of Dichotornius satunas. Exclusion experiments were used to determine whether 0. acuininarus was brought down in the dung by D . satonas. Placing coarse-mesh screen over fresh dung prevented colonization by D . soranas but had little effect on 0. ocrrniinotus, which tunneled deep into the soil aiid were found waiting in empty burrows. Pedaridium pilosum and .$carimus osarus are two other kleptoparasites on BCI that rarely provision ~ u r r o w sby the tunneler method. Another method of overland transport that does not require ball formation has developed in the coprine genus Canthidium. On BC1 at least three species, C.-arde&, C. ouriJkx, and C. haroldi, are accomplished pellet rollers that can rapidly’disperse rodent droppings. The elongate shape and dry texture of rodent dung allows these beetles to run away from a pile of fresll dung with a single pellet rolling along on the front edge of the clypeus. The frontal tubercles and carinae that characterize these species probably assist in maintaining contact with and providing directional stability to the pellet during rolling. On rare occasions, beetles will attempt to roll fragments of human and howler monkey dung, hut the immorphous shape and sticky texture of these types of dung prevent bcetles rrom moving quickly. Species using pellet rolling utilize dung that is ”packaged” for moving. This method of food relocation probably occurs in other groups of dung beetles that have specialized on rodent droppings. The final strategy for transporting dung is the roller technique. Conthun and Deltochihrrn are the only dung beetles on BCI that exhibit typical hall-making and ball-rolling behaviors. Like head butters and pellet rollers, the :rue rollers avoid possible competition for nest sites by moving dung away from the site where it was deposited (Chapter 3). Resource Utilization

{

Different types of dung are not evenly utilized by the different sorts of dung beetles on BCI. The howler monkey, Aluuuttapalliatu, is the largest producer of mammalian dung on BC1 (Appendix A. 12). These diurnal primates are often found in fig trees, where they Iransform fruits into an aromatic yellowishgreen dung, which is typically released high in the canopy, with the result that

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much of it lands on the lower vegetation as it cascades toward the ground. Defecation in the early morning by a troop of howlers atwacts many species of dung beetles. Canfhonnngusratus is always the most abundant species. On one occasion, several thousand C . angustatus formed a dense cloud of beetles that hovered under a tree in which nionkeys were defecating. Howler dung that lands on vegetation is located by C. angustatus and transformed into balls. These balls are rolled off the vegetation. and they fall to the ground with the beetle riding on top. Rolling continues on the ground, where pair formation also takes place and intraspecific combat is common. Ball construction seems to be restricted to the canopy, however, as very few beetles were observed making halls of dung that had fallen directly to the ground. The only other species on BC1 that regularly removes dung from the surface of vegetation is Canthon subkyalinus. Though less abundant than C . anyustutus, it is likewise found on leaves with fresh howler dung. Both species prefer dung that is located above ground level. A trap at 8 m above ground also collected several C. uequinoctialis, a species that feeds on human dung placed on branches and leaves hut has not been seen to make balls above the ground level. Howler dung that reaches the ground is quickly colonized by P. howdeni, P. pyrois, S. cupricollis, and many smaller species, including Ateuchus aeneomicans, 0. acuminafus, 0: c . punumensis, 0. sharpi, and 0.stockwelli. Numerous C. lamprimus, C. aurifex, and C. haroldi perch on vegetation surrounding howler dung, yet are rarely found on the ground in the dung. Howler dung that is defecated late in the afternoon is usually colonized by Cunthn aequinoctialis and Wrogs micros after dark. Capuchin monkeys, Cebus capucinus, also defecate in the canopy but their fecal masses are much smaller than those of the howlers and attract fewer beetles. Agouti, Dasyprocta punctata, are diurnal caviomotph rodents that produce elongate dung pellets. A pile of agouti pellets discovercd in the late afternoon was in the process of being rapidly dispersed by eight Confhidium uurifex and six C. haroldi. The'Canthidim species had no difficulty in rolling the pellets away. The large amount of agouti dung that is produced each year (Appendix A.12) may account for the abundance of Canthidium uurifex and C . haroldi on BCI (Appendix B.12). 12.6. SUMMARY

Tropical American forests support a rich and varied fauna of dung beetles that exhibit great diversity in feeding habits, including carrion- fruit, and detritus feeding. While many species are capable of utilizing a wide range of different types of dung, differences in the spatial and temporal availability of the dung types have led to feeding specializations among forest dung beetles. A case in point is the species that have evolved panicular foraging behaviors to cxploit

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monkey dung located high in the canopy. Other species have specialized in widely scattered ground-based resources, such as rodent pellets. Baited pitfall traps remove many of the extrinsic characteristics of different dung types and may give a rather distorted picture of local dung beetle assemblages. The dung beetle community on Barro Colorado Island has more diurnal than nocturnal species, although nocturnal species may be more readily collected by baited pitfall traps. A large number of questions remain concerning the taxonomy and ecology of tropical American dung beetles. We can only hope that enough forest will be saved to help answer some of these questions.

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CHAPTER 13

Dung Beetles of the Sahel Region Daniel Rougon and Chnstiane Rougon

13.1. INTRODUCTION

Sahel, “the edge of the desert” in Arabic, comprises a band of land in Africa running from the Atlantic Ocean to the Red Sea (Fig. 13.1). The Sahelian climate is distinguished by a long dry season from October to May, and by a short rainy season from June to September, during which pluvial agriculture is possible but risky. For the past twenty .years, the Sahelian region has had exceptionally low rainfall, which, when combined with intensive use of the vulnerable soils by man, has given rise to extensive desertilication. Two groups of dung beetles have adapted to the contrasting seasons of the Sahel. Dung beetles of the dry season are represented by a small number of species, all of which are tunnelers. Dung beetles or the rainy season are marc numerous in species and individuals, and they include rollers as well as tunnelers. Under the extreme environmental conditions of the Sahel, rainfall is the limiting factor, as clearly shown by a prominent increase in the numbers of dung beetles in the beginning of the rainy season. In this chapter we focus on the,dung beetles of the dry season, because, by their nesting behavior, they are actively involved in the fertilization of the Sabelian soils in regions where millet grass is cultivatcd. During the dry season, the Sahelian dung has a short,“life” of nine days due to very rapid desiccation. The Sahelian dung beetles have evolved short life cycles, and they feature exceptional flexibilify in their nesting behavior, which undoubtedly helps them survive the extreme conditions they face. This chapter is based mostly on our own studies conducted in Niger for ten years. No similar study has been carried out in any other arid environment. OF THE S A H E U A N t3.2. BIOGEOGRAPHY

REGION

Characteristics of the Study Area In Niger, the Sabelian region can be divided into two p m s along the isohyet of 350 mm (Peyre de Fabr&gues 1980); the northern “nomadic zone” with a primarily pastoral livelihood, and the southern ”sedentary zone,’’ where agriculture is practiced in the rainy season and cattle breeding during the rest of

<

Fig. 13. I . The Sahelian rcgiun (dotrcd a r i l : according to the African chorologic mnp 01‘ Whilc 1965. 1916, simplilicd hy Rougon). 1 . Mcdilctrancarr endcmism ccnlcr; 2 , Sub-Mcdilwrmcm trmsiciun LUIIC; 3, Sah;lro-Sindiim cndcmism ccntcr; 4, Sal~aruSudanian trilnsilion z m c (Snhel); 5. Sudanian endemism cenler; 6, Sudano-GuineoCongolese transition zonc.

thc year. Dung beetles have been studied in the southern area, at the univcrsity campus of Niamey. The outstanding feature of the south Sahelian climate is dryness, atuibutable to low rainfall during one short rainy season from June to September, and to high temperatures, the annual average reaching 28-29OC. At the study site in Niamey, the average annual rainfall is 592 mm (SD 127 mm), and the ratio of the maximum over the minimum value is 21 for the years 1941-70. The Niamey climate is very warm with an average annual temperature of 29.1”C. The south Sahelian area has tropical ferruginous soils, which are not at all or only a little washed, and are formed on sand or sandstone. The sandy texture of the soils is suitable only for the less demanding pluvial crops, such as millet grass and peanuts. The soil is very poor in organic carbon((C<0.2%). organic matter (M.0.<0.3%), and total nitrogen (N<0.01 Yo), and it is slightly acidic (5.6
232

'

The Sahcl Rcgion

Chapter 13

season, stockbreeders leave the south and proceed to north, giving up the land to pluvial cultures. After the rainy season, herds of cattle are brought back to the south, where cattle are now fed with the straw of the millet grass, left in the fields to dry after the harvest. Dung in the Sahelian Region Because of the extreme climate, two microclimatic parameters are crucial for the Sahelian dung beetles: (1) the microclimate prevailing around droppings in April (dry and warm season) and io July (rainy season); and (2) changes in the temperature in the dung and soil over 24 hours. During the dry and warm season, air temperature reaches 44°C at 2 P.M.; relative humidity remains less than 25% from 11 A . M . 10 8 P.M., and drops down to 10% ur less fTOm I P . M . to 6 P.M. Temperature in the dung and the underlying soil is highest in April, when it reaches 26°C at 8 A.M. and 48.5"C at 3 P . M . in droppings. In the soil, the thermal amplitude has a maximum df 32.3"C at the surface (between 7 A . M . and 2 P.M.), reduces to 16.4% at adepth of 5.7cm (between 7 A . M . and 4 P.M.), but is only 3.I"C at a depth of 45 cm (Fig. 13.2). Considering the average temperature (36.6 -C 5.9"C) and its amplitude (22.5aCj in droppings, zebu dung is relatively well buffered against ambient temperatures. The main physico-chemical characteristics of Sahelian dung are the following: Appearance. The dung consists of dissimilar, mugh, and very fibrous com-

.

233

ponents and has a less pasty consistency than in biomes with a less extreme climate, for example, in the Ivory Coast (Cambefort 1984). Rote ofproduction. A zebu weighing 250 kg consumes 6 kg of dry matter (straw of millet grass) per day and defecates 3 kg of dry fecal matter, or 10 kg of dung in fresh weight. A zebu defecates about ten times a day, giving an average weight of 1 kg per dung pat (Rougon 1987). Humidify of dung. The average water content is 71 2 5 % (n = 88), which is much lower than in temperate (more than 82%; Frison 1967; During and Weeda 1973; Matthiessen and Hayles 1983) and in wet uopical regions (80%; CanibefoK 1984). In the Sahel, dung loses all its water in nine days during the warm season in April; and after ten days, if not buried. the dung pa: is like a stone. In the beginning and at the end of the rainy season in lune and September, when it rains during the night, dung pats retain 45% of water after ten days. Cheniicul composition, The Sahelian zebu dung is poor in nitrogen (about 1% of dry matter) and mineral elements, especially in calcium (0.05%). Two amino acids normally found in natural organic matters, b-alanine and Ornithine, are missing in zebu dung. Availabili~yof zebu dung ID dung + d e s . Following the harvest of niillet grass, the most common crop in Niger (90% of arable land), an estimated 2.56 tons per hectare of straw remain in the fields and are available to zebu during the dry season. Digestibility of the straw is SO%, thus the potential quantity of dung is 1.26 tons per hectare per year (dry weight), or 4,400 droppings per hectare per year.

The Sahelian Dung Beerie Fauna

30

0

6

12

18

24

HOURS hours on Ihc surface and al diflcrcnl depths in the soil (Boudouresque and Rougon, unpubl.. April 15, 1082).

Fig. 13.2. Fluctuations of temperature during 24

During the years 1978-79, 17,175 beetles were extracted from 240 zebu droppings (Table 13.1). Twenty families of beetles accounted for 93% of the total dung insect fauna. Among the beetles, Staphylinidae predominate (42% of individuals), followed by Histeridae (39%), Aphodiidae ( I I%), and Scarabaeidae (3%). Staphylinidae are represented by three subfamilies in the Sahel-Oxyfelinae, Staphylininae, and Aleocharinae--oT which the first has coprophagous species while the others are predators (Hanski and Koskela 1979). Two other beetle families, Lathridiidae and Anthicidae, e unusually well represented, while Hydrophilidae are relatively scarce (T&e 13.1). A complete list of the dung beetles (Scarabaeidae and Aphodiidae), with ecological data, is given in Appendix 8.13. The activities of humans have affected dung beetles in two major ways in the Sahel. Since the frightful drought of 1968, the Sahelian governments have, for varied reasons, tried to settle the nomadic stockbreeders into specific areas. When the ancient practice of seminomadism disappears, large areas will remain ungrazed and the dung beetles will disappear. In addition, the increasing

..~,,

,

234

, .

.

.

,

.

The Sahcl R C ~ L O ~ 235

Chapter 13

TABLE13.1 Numbers of beetles collected from 240 zebu droppings in Niamey, Niger. in 1978-7'3. Number of

Funlily

Carabidae Dyliscidae Slaphylinidae Sc ydmaenidae Hydrophilidae Histeridae Scarabaeidae Aegialidae Aphvdiidae

Hybusuridae Dynastidae Cetonid;re

Species 4 1 11 1

4 8 20 I 20 I

1

I

Elaleridae

L

Cucujidae Lathridiidae

1 I 1

Coccinellidac Anthicidde

Tenebrionidae Chrysomelidae Curculionidae Total

I 7 I 1 87 . .

APHODIID E

RAB EIDAE

Number of

lridividuulv

30 2 7,186 I

205 6,771 4s7 IO

1,953 13

I

I 2 46 262

LIT

00

cz

32 z

HISTERIDAE 500

500t 1oof

iU

SONDJFMAMJJA

MONTH

I

Fig. 13.3. Monthly changes in Ihc numbcrs vfindividuals in four bcctlc f;lmilics (from Scptembcr I978 la Augur1 1979).

22 I 9 3 I

A p h o d d a e show the same seasonal pattern, but have only a small decrease in the numbers dunng the dry season.

17.175

use of airplane-dispersed insecticides in the fight against locusts and owlet moths and the use of nematicides against cattle parasites undoubtedly have harmful effects on dung beetles.

13.3. THEDUNGBEETLECOMMUNITY Beetles were collected by depositing, once per month, 125 kg of fresh zebu dung in heaps of 1 kg. The 125 dung pats were placed in a line at one-meter intervals. Five pats and the underlying soil were removed after 1, 3, 5 , and 10 days, and beetles were extracted by water Rotation.

Seasonality The numbers;of predatory beetles, the Staphylinidae and Histeridae, peak in October. In November the numbers of insects in dung pats generally begin to decrease; thiy reach a minimum in the dry season, and begin to increase again in the beginning of the rainy'season in June (Fig. 13.3). Scarabaeidae and

Food Web Relations in ?hi,Dung Insect Community In July, freshly deposited dung pats attract many species of flies, mainly Sepsidae and Muscidae, seeking a place to deposit their eggs and larvae. Droppings attract flies for only two or three hours, however, because the rapidly developing hard cmsl prevents oviposition. Ovipositing flies are followed by coprophagous beetles, the Aphodiidae and Scarabaeidae, and by the,first predators, the Staphylinidae and especially the Histeridae. Dung beetles reach their maximum numbers on the second (Aphoodiidae) and third days (Scarabaeidae; Fig. 13.4). Scarabaeidae are entirely absent by the seventh day while the numbers of Aphodiidae decrease more slowly. Dung beetles car& phoretic mites, which prey on the eggs and larvae of flies (Seymour 1980). Predatory beetles, the Staphylinidae and Histeridae, are the dominant beetles between the third and sixth days, reaching their peak abundance on the fourth day. Their main prey, fly larvae, reach their maximum numbers on the fifth and sixth days. Beginning on the fifth day, a third wave of arthropods invades the droppings, which have, by then, lost their specific characteristics as a result of

The Suhel Rcgion

300

January

............ April ....._

v)

<E

237

N. lividus

- September

w

m

E. intermedius

'

200

0. gazella

DAYS Fig. 13.4. Chilngcs in the numbers of individuals o1'dung bcctlca IScxabecid Aphodiidac) according lo the season and lo thc agc of thc dung pat.

desiccation and chemical changes. This third wave is comprised of' species from the surface of the soil and from the soil'itself: Entomobryidae, Isotomidae (Collembola), and Tenebrionidae, all of which are thought to be saprophagous; Formicidae. represented by the three genera Pheidole (granivorous and predaceous), Monomorium (cmnivorous), and Messor (granivorous); and Carabidae and Araneidae, which are.generalist predators. In April, during the warm and dry season, the dung microhabitat features extreme climatic conditions, and. the temporal sequence of colonization described above is greatly accelerated; the maximum numbers of dung beetles (four species of Scarabaeidae and Nialus lividus, Aphodiidae) are already reached during the first day (Fig, 13.4). The predatory Staphylinidae are doniinant on the third day, w h i b Histeridae are abundant from the third lo the eighth days. From the third day onward, soil arthropods start to colonize the. dung, which is rapidly drying out. Unlike in July, termites colonize droppings in great numbers in April, and they are by far the most abundant taxon beginning on the third day. Microorganisms do not appear to play an important role in the pmcess of dung decomposition during the dry season, undoubtedly bccause of the rapid desiccation and hnrdening of the dung (see Merritt and Anderson: 1977 for California). 13.4. POPULATION ECOLOGY OF DUNGBEETLES

Among the twenty species of Scarahaeidae collected in 1978-79 in Niamey, only five species accounted for more than 5% of the total number. Fig. 13.5

MONTH ,Fig. 13.5. Monthly chnngcr in llic numbers of liiur dominant spccier of dung bccllcs (from Scplctnbcr 1978 to Augusl 1979).

sbows the monthly abundance changes in the two dominant species, Euoniticellus intermedius and Digironthoplragus gazella, which occur at different times of the year. Of the 1,953 individuals of Aphodiidae collected in 197879, only six out of twenty species were coinmon, each representing more than 2% of the total number. Fig. 13.5 gives the monthly abundance changes in two species. Nidus lividus is the only Aphodiidae present in large numbers throughout the year, while Orudaluspnrv~lu~ is a common species during the rainy season only.

Adupfive Nesting Behavior in Saheliarr Dung Beetles Studies on the nesting behavior of the most abundant species of Scarabaeidae, conducted both in situ and in the laboratoty, have led to three main conclusions: { / t i the dry seasun on srrrrdy soils. rlie galleries of drrng beetles ore sliurerl up. In the Sahel, tunnelers shore up their shafts and the galleries leading to the nest with a stercorous matter, thus preventing them from caving in. Depending on the species, the thickness of the film of excrement used for this purpose varies from I , I mm in Onitis alexis to 1.5 mm in Euoniricellus intermedius and Digitorithophagus, gazella (D.Rougon and C. Rougon 1980, 1982a,b; Rougon 1987). Nests are stratiJed at diferenr levels in the soil. The Sahelian dung beetles

.

. 238

’

Thc Sahcl Rcgion

Chapter 13

have evolved a stratified nesting behavior, which should dccreasc interspecilic competition during the warm and dry season. The nests are tiered down to a depth of 50 cm beneath the soil surface. Onificellusformosus is a dweller active in the dry season. It makes spherical brood balls inside two or three cavities (5 or 6 cm in diameter), burrowed in large two-or three-day-old dung pats. Each cavity contains an average of nine cells (1.2-cO.1 cm in diameter and weighing 9 8 0 2 1 2 0 nig, Fig. 13.6; Rougon and Rougon 1982b). The same type of nesting behavior has been described for this species in South Africa (Davis 1977; Bemon 1981). In the Sahel, the life cycle of Oniticelfurformosus is 3 8 1 2 days. Three other common species-Onitis alexis, Euoniticcffus intermedius, and Digitonrhophagus gazellu-build their nests at varying depths in the soil below the dropping. These three species bury a large arnuunt of dung in a very short period of time; the dung will then be used to prepare the brood balls. Euoniticeffusintermedius builds its nest only 3-8 cm beneath the soil surface. In the warm season the structure of the nest is of the “onitidian type,” that is, access to the nest is by a shaft that penetrates the soil vertically for 3 cm, then branches off into two galleries parallel to the ground (Fig. 13.7). Along these galleries, six mounds of stercomus matter, each 3crn wide, are deposited at a depth of 3-8 cm. Each mound is a miniature version of an Onitis a h i s nest and is formed of four to six brood sausages, with a diameter of 7.5-8 mm, placed side by side (Rougon and Rougon 1982a). This compact structure protects the progeny from drought more effectively than would a nest in the shape of isolated ovoid cells. The life cycle of Euoniricellus intermedius is 28 days in the Sahel. Digitonrhophagus gazella constmcts its nest at a slightly greater depth, 2035 cm beneath the soil surface, Thenest consists of a network of galleries with 1325 brood balls, each 2.620.4 cm in’length and 1.4t0.3 cm in diameter (C. Rougon and D. Rougon 1980). The life cycle of this species is 41 days in the Sahel.

c93

Dung

0Sandy soil

0 Cavity Pedotrophic cell

Fig. 13.6. Nest of Oniticpllw~onnosusC h e v d d t .

’

239

LB Dung 0 Sandysoil

NesllnQmass 0 Sand carried up

0 Gallery

Pig. 13.7.,Ncsl of Ewnhicdus irrrcrrwdit,.r (lleichc) during thc dry and warn, scasu~~ (“Ooitidian type,” OLI thc Icfl) and in the beginning or Ihe rainy s c w m (”Onthuphagian lypc,” on the right).

Oniris ulexis, the largest dryseason dung beetle, builds a large nest at a depth between 28 and 46 cm. Oniris alexis always colonizes 1-48-hour-old dun2 at dusk. Its nest is reached via a perpendicular shaft, 1.6 cm in diameter and 30 cm in depth, which is shored up with a stercorous substance 1. I nim thick. The nest has 204 k 84 g of stercorous matter (after 4 days), comprising 7 2 3 brood sausages parallel to each other or ramified and packed tightly together. Each roll contains two or three chambers with a single egg in each one (Rougon and Rougon 1982a). The life cycle of Onitis alexis is completed in 112 days on average, a very short period of time compared with the 2-year life cycle of Oniris caffer in South Africa (Oberhulzer 1958). Oniris alexis plays a crucial role in dung burial in the Sahel: it buries, on average, a quarter of a dung pat weighing 1 kg. The rypc of nest corurrtrcted depends on the season. Eiioniticclhis inrerntediirs constructs two types of nest depending on the water content in the soil adjacent to the dung pat. In the warm and dry season, when the water content in the soil is less than I%, E. intermedius builds a nest of the “onvdian type” (Fig. 13.7). In the rainy season, in contrast, the nest is of the “onthophagian type” (Fig. 13.7): access is by a shaft that opens to highly ramified galleries with one or several, brood balls measuring 1.520.2 cm by 0.8+-0.1 cm. During this season the higher water content in the soil (2-20%) prevents the balls from desiccating. Dung beetle nesting behavior is not fixed or unchanging; in semiarid regions it;is flexible and adapted to the prevailing environmental conditions. The remarkably flexible nesting behavior of Euoiriticellus intermedius al-

... l i

240

.

Chapter 13

lows it to thrive all over Africa and may explain why this;species has been so easy to introduce into other parts of the globe, for example, to Australia (Bornemissza 1976) and New Caledonia (Gutierrez et al. 1988; Chapter 16).

Kleptoparasitism in Aphodiidae

'

Four species of Aphodiidae4iulus bayeri, N . nigritrr, N . lividus, and M e sontoplatys rougoni-dl apparently unable to survive the thermal and moisture conditions prevailing in droppings in the dry season, have become kleptoparasites of 0.alexis, E . intermedius, and D.gazella. These Aphodiidae take advantage of the rapid (less than 48 hours) burial of dung by the larger beetles, and they ensure the development of their own progeny by using the subterranean dung reserves of the host species (D.Rougon and C. Rougon 1980, 1982% 1983; Rougon 1987). Either the Scarabaeidae are passive carriers of the Aphodiidae adults when they descend to construct their nests, or the Aphodiidae actively seek out the dung buried by Scarabaeidae. Both processes probably occur. The behavior of kleptoparasitic Aphodiidae has several distinctive features. The larvae move about actively within the nests and transport grains of sand, which obstruct the chambers where the larvae ofD. gazella, 0. ulexis, and E. inrermedius lodge. These grains of sand can damage the thin integuments of the host larvae, causing their death. The latter are often found desiccated in their chambers, reduced in size, and filled with grains of sand. The larvae of Aphodiidae develop up to the third larval instar inside the host nest, but the pupal stage is spent outside the nest. Nidus larvae migratc in the third larval instar to the periphery of the nest of 0.alexis ur to the surrounding sand. The larvae construct small pupal-cocoons composed~ofa mixture of sand grains and fragments of their excrement. The third instar larva of M. rougoni leaves the bmod hall of D.guzella and burrows directly into the sand to form a small chamber 4 mm long and 2.5 mm wide, in which it pupates.

13.5. CONCLUSION

' '

Ecological studies of the Sahelian dung beetles demonstrate that Scarabaeidae and Aphodiidae, though not represented by many species, have a relatively large biomass. To survive the extreme microclimate in zebu dung pats during the warm asd dry season, dung beetles have evolved particular nesting behaviors: shoring up the gdleries, stratification of the nests in the soil, flexible nest architecture, and kleptoparasitism. By building shafts and subterranean galleries, dung beetles contributc to aeration of the soil and improve its structure and water circulation. Dung beetles in the Sahel play the role of earthworms in.humid temperate and tropical biomes; the Sahelian soil, by its highly sandy texture and desiccation-prone

The Sahel Region

.

241

structure, rules out the presence of earthworms. In the warm season, the abundant dung beetles play an essential role in dispersing organic matter over a wide area, thus preventing the Sahelian soil from becoming sterile. Field experiments (Rougon 1987) show that the nesting activity of dung beetles leads to a notable increase in the content of organic carbon ( X 2 ) , nitrogen ( X 3), interchangeable bases [ X 2), and humic acids in the soil. Without dung beetlcs, zebu dung becomes rapidly desiccated, and the potential organic enrichment to the soil is lost. Rougon (1987) showed that dung beetles are essential to the stability of the Sahelian ecosystem; hence it is necessary topreserve the association between agriculture and cattle rearing in the Sahel, and to enable the Peul cattle breeders to continue their seminomadic way of life.

Moovtnc Dung becllcs

.

243

distributions of dung beetles (Section 14.2) and describe the papulation ecology of high-altitude dung beetles, mostly AphOdiKS, in the Alps (Section 14.3 'and 14.4). The rest of the chapter deals with montane dung beetle communities, species richncss, and abundance distributions (Section 14.5). The focus ofour discussion is the dung beetle community in the Swiss and French Alps, where recent quantitative studies have been carried out (Lumaret and Stiernet 1990).

C H A P T E R 14

Montane Dung Beetles Jean-Pierre Lwnarer and Nicole Stiernet

14.2. DISTRIBUTION OF MONTANE DUNGBEETLES: AN OVERVIEW 14.1. I N T R O D U C ~ O N Montane habitats have special ecological interest because of the predictable, systematic change in envimnmental conditions within sbon distances. The tree line comprises a natural ecological boundary between the lowlands and high altitudes, but its position depends on the montane system and the latitudc. i n the Alps, the tree line is located between 2,000 and 2.100 m on the southcrn and between 1,800 and 1,900 m on the north,em slopes, while in the Himalayas it is at about 3,600 m (Mani 1968). Gams (1935) recognized four biotic zones above the tree line on the Central European mountains: the lower alpine zone, the upper alpine or grassy meadow zone, the subnival zone up to the closed meadows, and the nival zone. The three biotic zones below the tree line are the subalpine, the upper montane, and the lower montane zones. The elevational limits of the high montane habitats are not fixed, however, but they fluctuate in time, and the organisms have to respond to these variations. In the Alps, the snow line was located some 1,200 m below its present elevation at about 3,000 m during the Wiirm glaciation (20,000 BP). In the Himalayas, the snow line is at ahout 5,200 m. Many dung beetles have been collected on high mountains all over the world, but ecological studies on them are scarce. Biogeographical data on montane dung beetles, inclilding their elevational distributions, have been compiled and discussed by Horion (1950) for the Alps and the Carpathians. and by Reinig (1931), Mani and Singh (1961), Mittal (1981a), and Stehnicka (1986) for the Pamir, the Himalayas, and northwest India. Dung beetle distributions on mountains in Mongolia have been described by Nikolajev and Puntsagdulam (1984) and Grebenscikov (1985), and in Afghanistan and Iran by Petrovlu (1959, .1961, 1965, 1967) and Bortesi and Zunino (1974). Some ecological data on dung beetles on the Mediterranean mountains are included in Lumaret (1978), Martin-Piera (1982), Avila- and Pascual (1981, 1986, 1987), Galante (1983) and Mesa (1985). Veqhlittle is known about dung beetles on tropical mountains (Hanski 1983; Mor6n and Terr6n 1984; Halffter 1987). In this chapter, we present an overview of the geographical and elevational

E

The geographical distribution of montane dung beetles depends, like that of an insular fauna, on the present structure and the history of their discontinuous environment (Halffter 1987). Several examples of dung beetle distributions from various pans of the world demonstrate that mountain systems constitute both centers of differentiation and refuges for dung beetles. A case in point is Agolius and Ncagolius, two alpine subgenera of Aphodius, which occur along the entire alpine arc and are distributed, respectively, from Spain to the Himalayas and from Spain to Central Asia. Most species and subspccies are endemics, patchily distributed and restricted to high altitudes, rarely collected below 1,800 m. Sexual dimorphism is often striking, and some females were first described as distinct species (Dellacasa 1983). An examination of morphological characters leads to the conclusion that Agolius and Ncagolius are relicts with few affinities with other Aphodius (Banud 1977). The geographical isolation between the Pyrenees and the Alps, and between the different massifs of the Alps, has led to subspecific differentiation in many taxa. For example, A . (Agoliusj abdominalis ( = A . nzirtus), a species widely distributed from Spain to Italy, is differentiated into four distinct subspecies. Aphodius (Neagolius) schlumbergeri is also divided into four subspecies. but numerous transitional forms occur in the Pyrenees between A . schlumbergeri s. str. and A . schlumbergeri ssp. remperei, including a c h e in paramere shape (Baraud 1977). Apparently, A . schlumbergeri is in the active process of differentiation in the Pyrenees, both horizontally and vertically, while the two other subspecies in the Alps are more distinct because of their isolation. Endemics may also differentiate from species with orophilors tendencks. In the westem Alps, Aphodius gemiandi represents an a p ~ n evlcar~ant closely related to A . obscurus, a species widely distributed from Spain to Poland, Asia Minor, and the Caucasus. Onrhophogus baraudi is the montane sister species of 0. joannae, with a lowland to midaltitude distribution in western Europe. Another characteristic set of species in the Alps consists of species with boreo-alpine distribution. Most of them belong to the Agoliinus and AgriLinus subgenera of Aphodius, for example, A . piceus, A . ater (with sevepl subspecies), A . nemoralis, A . borealis, and A . fenellus.

244

'

Chapter 14

Halffter (1962, 1974, 1976, 1987) and Mor6n and Zaragoza (1976) have described distributional patterns in the montane dung beetles in Mexico. The mountains of western Nonh America continue through the United States, Mexico, and Central America to merge with the northernmost spurs of the Andes. Mexico constitutes a crossing point where both Nearctic and Neotropical dung beetles may be found (Chapter 7). The occurrence of Nearctic species on the highest Mexican mountains is explicable by the reccnt transformation of a large part of the Mexican Altiplano to a desert; examples are Ceratotrupes, Georrupes, Copris, Onrhophagus, and Aphodius. A mixed, Nearctic-Paleo-American fauna dominates between 2,000 and 3,000 m, while all the dung beetles above 3,000 m are exclusively Nearctic (Halffter 1987). Species present in the alpine meadows between 2,980 and 3,050 m include Geotrupes viridiobscura, G . sobrina, Copris ormarus, Onlhophagus chevrolati, and 0 . hippopotamus. Turning to the altitudes at which dung beetles occur on mountains, the mdximum upper limit generally depends on the duration of snow cover and the length of the period when the average temperature exceeds 5°C. The maximum altitudes reached by dung beetles v a r j with latitude (Table 14.1). In the western Alps, Aphodius species are dominant and reach the permanent snow, whereas Onthophagini and Geotrupini do not exceed 2,400 rn. In the high plateau of Iran and Afghanistan with its higher summer temperatures, Scarabaeidae are more numerous at high altitudes despite winter frost. In the Himalayas, several Onthophagus reach 5,000 m (Table 14.1).

TAKE 14. I

High-altitudc observoiions or dung beetles. IrnrrersJ

3,200

Swiss Alps, Gnbons (46-30")

3,000

Frcnch Alp,. Vanothc (45"30'Nl

3.000 2,800

Sierra Ncvsdd, Spain (37"N)

,

2,400 2,600 2.500

2,200 Alai Valley. Pamir (37"NI

3,200

Iran and Afghunisian (32"N)

3.200

3,000

2,700 2,450

14.3. BIOGEOGRAPHY OF THE' ALPS

Lumaret and Stiemet (1984, unpubl.) have studied the ecology of dung beetles in the European Alps, in the French National Park of Vanoise, and in the Swiss National Park of Grisons. The Vanoise National Park (528 km') lies at altitudes between 1,250 and 3,852 m. The relief is broken, with 107 peaks exceeding 3,000 m. Forty-five percent of the surface area belongs to the zone of vegetation mats and meadows, extending from the lowest limit of snow patches in July to the upper limit of animal life. Forests are very scarce (0.8%), while meadows and pastures account for 17% of the area. Human influence is negligible, except during summer, when sheep and cattle from adjacent valleys are grazed in the subalpine and alpine meadows up to 3,000 m. Ti% park hat a rich fauna of wild mammals, including wild goats (Caprn ibex), chamois, marmots, and hares (Appendix A.14). The Grisons National Park is smaller (170 km2) and stretches between 1,700 and 3,164 m in altitude. The abundance of wild mammals is high: 2,130 red deer, 1,230 chamois, 238 wild goats, and 57 roe deers were counted in the park in 1985. In addition, cattle, sheep, and a.few horses (all outside the park limits) increase the abundance and diversity of dung in this area (Appendix A.14). '

Alrilude

Lucoliiv (Lurirdel

Sikkim. Tibct (30"N)

Wcstcrn Hininlayn (29-N)

2,200 2.100 00B-5,200 (Ma4,200

2oo-~,o~o

6004,200

NW Himalaya (28"NI

Punjab (28"N) Kashmir (26"Ni

3.IW3.600 2.400-3.I00 3,660 3.0W3.450 3,050 3,800 3,000 2,500-2.800

Colorado Mountains (38"N) Mexiam Altiplrino (1Y-N)

4.000 3.000

Species

246

'

Montane Dung Beetles

Chapter 14

The environmental conditions vary from the westem to the eastern Alps. In the Vanoise, annual precipitation ranges between 860 mm (Bozel) and 1,100 mm (Pralognan) (Balseinte 1955). In winter, snow may lie 9 m thick on glaciers. Temperature decreases by about 5.5"C for an increase of 1,000 m in elevation. July and August are the warmest months, with maximum air temperatures ranging from 18°C (2,500 m) to 26°C (1,900 m) (Gensac 1978). Temperature fluctuations are great, and night frosts occur frequently, even in summer. In contrast, the soil temperature at a depth of 10 cm is more constant. In winter, the minimal soil temperatures scarcely decrease helow 0°C. while in summer average temperatures are always 3°C higher in the soil than in the air, and exceed 20°C. The vegetative period (soil temperature exceeding 5°C) lasts for 5 months in the subalpine zone and for 3.5 months in the alpine zone (Gensac 1978). In the Palearctic region, most of the alpine dung beetles belong to Aphodiidae, whereas on tropical mountains Geotmpidae and Scarabaeidae constitute a larger part of the fauna. This difference reflicts the generally increasing dominance of Aphodiidae with increasing latitude (Chapter 4). For example, anlong the thirty-seven species recorded in the Vanoise National Park and its surroundings, Scarabaeidae account for only 18% of.the species (six Onrhophagus and one Euoniticellus) and GeotNpidae for 8% (Ceorrupes, Anuplotrupes, and Trypocopris), while Aphodiidae include the remaining 73% (twenty-four Aphodius, two Heptaulacus, and one Oxyomus) (Lumaret and Stiemet, unpubl.). The results are very similar for the Grisons National Park, with thirty-six species (Handschin, 1963; Besuchet 1983; Dethier 1985; Stiernet,.unpubl.). Species richness in the.Alps is much increased by the network of deep valleys, which make it easier for nonmontane, Medio-European species to penetrate the region. Many such species can be found on exposed slopes, for example, Euoniricellus fulvus and Onthuphagus joannae in Vanoise up to 2,200 m, and 0. lemur up to 1,900 m (Lumaret and Stiemet 1990). OF HIGH-ALTITUDE 14.4. POPULATION ECOLOGY DUNGBEETLES

This section is largely based on the results from the Vanoise National Park. Taking into account the relative abundances and seasonal dynamics of the twenty-'four dung beetle species at the Vanoise study sites, three groups ol species can'be'distinguished: (1) lower and upper montane dung beetles (two Geotrupidae, six Aphodiidae), which only exceptionally reach the subnival level; (2) midaltitude dung beetles (two Onthophagus, one Hepraulucus, and two Aphodius), all of which reach the subnival level (in this group 0.buraudi is an endemic species); and (3) true high-altitude dung beetles, all Aphodius, with the elevational distribution often beginning in the lower montane or subalpine zone. Two subgroups of the high-altitude species may be distinguished: species that occtu up to the upper alpine level (six species), and the ones that

'

247

reach the subnival and nival levels (five species). Among these eleven typical high-altitude dung beetles, A . (Neagulius) amblyodon is an endemic and A . (Agolius) abdominalis is represented by its subspecies, A . a. abdominalis. Aphudius yermandi is the high montane vicariant of A . obscurus, a polymorphic and dominant species widely distributed on exposed mountain pastures in central and southern Europe as far as the Caucasus.

Phenoluy)' of High-Altitude Dung Beetla Many high montane species overwinter as adults, their emergence primarily depending'on air and soil temperatures. Emergence typically begins when soil temperatures exceed YC, though a few adults often emerge earlier and can be seen walking on the still-frozen soil and snow (A.fmeturius,A . obscurus, A. germandi, A . amblyodon, and A . abdominalis). These species constitute the core of the spring community (Section 14.5). Aphodius depressus is a characteristic spring species, which may represent more than 60% of subalpine dung beetles at sites below 2,000 in. At even lower altitudes, A . erraticits, a species more resistant to high temperatures (Landin 1961), shows a similar phenology. Aphodius fimerarius is another characteristic species, with two generations per year, both males and females occurring from spring to the end of autumn in all types o f dung. Under alpine conditions, only adults of this speries hibernate, regardless of the altitude. Other species spend winter as third instar larvae. On emergence the adults appear to he immature, with yellow or brownish appendices and tegument, as observed, for example, in Aphodiirs haemorrhoidalis, A . rufipes, and A . satyrus. Aphodius haemorrhoidah is a typical summer species, which emerges in the beginning of June. It may be dominant at the lowest sites, and is always present in montane dung beetle communities. Aphodius rufrpes emerges about one week later than A . haernurrhoidalis. It plays a significant role in the subalpine and lower alpine beetle communities because of its abundance and relatively large body size. Aphodius satyrus, an upper alpine and subnival species, may account for up to 40% of individuals in some summer dung beetle communities (e.g., Pont du Montet, 2,410 m). In the Vanoise National Park, A . satyrus occurs mostly at open sites that are not too dry, but in Grisons National Park, a more xeric region. this species is found mostly in forests. Finnlly, some montane dung beetles emerge only in the autumn, for example, A . tcnellus, which may be dominant at the most humid and cold upper alpine sites.

Aphudius ob.rcurus Aphodius obscurus is a polymolphic species that reaches an altitude corresponding tothe 0°C January isotherm (Lumaret 1978). It is often the dominant species, present in all montane dung beetle communities. In the upper alpine

248

'

Montane Dung Beetles

Chapter 14

and subnival zones it may constitute more than 50% of all dung beetles; in Balcon du Montet, at 2,760 m, it comprised 96% of beetles in the autumn. Aphodius obscurus is a spring and summer species at the lowest sites but it becomes a summer and autumn species at the upper ones. During the congregation period, A . obscurus oviposits under or in all types of dung, including manure at the resting places of cattle. Larvae may live inside large droppings, but they dig tunnels under small ones, which dry out quickly. Some other Aphodius species have similar habits under Mediterranean clinlatic conditions (Chapter 6). Pupation always takes place in the soil ( 2 4 cm depth). At subalpine and lower alpine sites, A . obscurus has two generations per year, but above the upper alpine level, up to the subnival and nival levels, there is only one generation per year. The sex ratio is typically close to 5 0 5 0 , but males are always in the majority in the beginning and at the end of the emergence period, with females dominant in July and August. Whatever the site, some individuals overwinter as adults (mostly males), while the rest overwinter as third instar larvae. The flexible phenotogy of A . obscurus may contribute to its dominance in montane dung beetle communities.

TAHI.E 14.2 Elcvnlionel dislributiun of dung bcellcs in the Alps (Vasmise National Park). Sire

Species

2 I I42 1,001 30 155 24 282 249 1.183 439 367 638 269

Scarabaeidae Few Onhophagus species reach high altitudes in the Alps, where the short summer does not permit them to complete their life cycle. Nonethcless, 0.

1

I 97 2 3 45 73 829 17 1,092 1.074 229 201 156

8 1

1 19

I a7 I60

I I 4 111

10

377 20

1 I 9 22 61 4 120 2 7 30

40 5 6 I 873

119

lndividurla Number of spccics Shannoa-Wcaver indcn Equiiabilily

9,962 22 3.08 0.69

6,426 21 2.95 0.67

3,924 15 2.91 0.75

3,583 16 2.33 0.58

7.465

0.54

20.911 17 0.98 0.24

Allitudc

1.750

1,960

2,OM)

2,230

2,410

2.440

17

(in)

\I

S

7

6

5

4

31 615 30 I 60 488 57 I 702 2 2 5 891

3,174 464

',

3

2

J

Aphodius amblyodon and A . abdominalis Many species in the subgenus Agolills are saprophagous and breed in old dung pats and in decaying vegetable matter in the soil, though adult beetles can be found feeding in fresh cattle pats. Aphodius amblyodon and A . abdominalis are two examples, sometimes found together in the Vanoise (Table 14.2). Males are often observed walking on snow patches, perhaps attracted by reflected sunlight. Aphodius amblyodon is a spring species, restricted to a few sites in the study region, though it may be abundant locally. The flight activity of inales begins when large snow patches still cover the ground (lune). Males are attracted to cattle pats in which they feed. Females, which are always short-winged, are never attracted to dung but remain'in the soil. The ecology of A . abdominalis is similar. The densityof this species may reach very high levels in the wettest places-for example, 19.925.3 (SD) males per square meter at an altitude of 2,490 m in July 1987 (Lumaret and Stiemet, unpubl.). Like in A . amblyodon, very fe,w females are attracted to dung, although they can Ry. Most females remain in the soil, where they lay eggs in mold and decaying vegetable matter. Larvae devel+ in the soil and hibernate in the third instar. Larvae have been found in July under large stones deeply sunk into the soil and under old dung pats dropped in the previous autumn (Lumaret and Stiemet 1984).

249

'

147 85 28 118 54 45

23 82 230 61 146 861 379 .3 17 1.644

85

1

3

10

67 2

95 971 2,718 20 71 3.081

867 838 1,061 I45 17.674

168 11 141 I54 537 6,117 8 0.54 0.18

3 0.79

2,760

2,960

12 1.95

2

I 23 92 116

0.49

Nore: sms: I . Besfam; 2. Bonnevui; 3,.Lu Ramasse: 4, Grand Plan: 5 , Pant du Monlrt: 6, Les Roches; 7, Balcun du Monal; 8. Col de Gonli?re.

<

baraudi and 0 .fracricornis occur in the Vanoise above the tree line. The former species emerges in spring, then disappears until the next year. Ontlwphagus baroudi probably hibernates in the adult stage, as very few immature individuals have been observed in spring. This species reaches the lower alpine zone (2,000 m), where it may represent 20% of the spring dung beetle community. On
k 7.50

'

Chapter

Montane Dung Beetles

14

tivity, the first one corresponding to the spring emergence of overwintered adults, the other one being that of the new generation. 14.5. THEALPINE DUNGBEETLECOMMUNITIES

The Dung Insect Communiry On the European mountains, insects constitute an important f w d source for many predators. Large flying dung beetles, such as Geotrupidae, are taken by foxes around cattle pats, and moles dig tunnels below the pats to get to the insects. Ravens and choughs often scatter cattle dung and sheep droppings while searching for insects. Spiders catch small Aphodius that land on droppings. Many types of droppings are present in the Alps. The colonization of cattle pats and red-deer droppings by dung insects has been studied in the Grisons (Stiernet, unpubl.). A large number of fresh qattle pats and red-deer droppings were placed simultaneously in the field and were subsequently sampled for thirty consecutive days. Staphylinidae were numerically dominant in deer droppings, while the species composition was more diverse in the larger cattle pats, with Aphodius, Hydrophilidae and Staphylinidae all well represented (Fig. 14.1). Flies were not scarce but the sampling method is not well suited for collecting them. When cattle pats and red-deer droppings become older, their attractiveness to insects decreases and most adult insects leave the droppings. At this stage Aphodius larvae are the dominant inhabitants of dung. On average, some 500 and 2,500 insects were attracted per kg (dry wt) of cattle dung and red-deer droppings, respectively, during the first nine days.

CATTLE DUNG

.

251

DEER FEWMETS

100

80

60 40 20

" n

1 2 3 4 5 7 913162230

1U I

w

Diptera Staphylinidae Aphodiidae (farvae) Aohodiidae ladultsi kiydrophifidae

DAYS

I

Fig. 14.I , Cumposition o f t h c dung insect fauna ing h agc.

2o

it?

caltle pats and deer droppings valy-

1

Species Richness of Dung Beetles Eight sites ranging in altitude from 1,750 to 2,960 m were sampled in the Vanoise in 1985-87. At each site, ten dung-baited pitfall traps were set up. each consisting of a collecting pot covered with a screen supporting the hait, 200-250 g of fresh dung from the dominant livestock at the site (sheep droppings in subnival and nival zones, cattle pats at lower altitudes). Species number varied from site to site but it remained high, around fifteen to tyenty species, along the entire elevational gradient, excepting the highest sites, where species number was eight (2,760 m) and three (2,960 m; Table 14.2). The-Ikge number of species (seventeen) at site 6 (Leu Roches) at.2,440 m, was more unexpected (Table 14.2), but this result is partly explained by the exceptional situation of this site, above site 2 (Bonneval). Most species at site 6 appeared to be immigrants, helped in their flight from the valley by air currents dong the slopes of the mountain. Density of dung beetles remained high at all altitudes, suggesting density compensation, with the species at the highest sites being more abundant, on

LOG ABUNDANCE Fig. 14.2. Abundmcc disrribution in the pooled material from the sevcn silcs. Thc horizontal :!xis is logarithinic (thc rbunduncc cIasscs arc I-?. 3 4 , 5-8. etc.).

.."

a r r i l m ~ ~ m - = m r n m 252

'

Chaprer 14

Montane Dung Hecllcs

average, than species at lower altitudes. Hanski (1983) found'a similar phenonienon on a tropical mountain in Borneo. A contributing factor may be decre.asing competition between Aphodius and other coprophagous insects, llies, and Staphylinidde beetles becoming increasingly scarce with altitude. Only Hydrophilidae remain abundant along the entire gradient, occurring mainly i n cattle pals. The marked decrease in the value of the equitability index with altitude (Table 14.2) indicates high degree of dominance by a fen, species at high altitudes, especially at the subnival and nival zones. Abundance Distribution Figure 14.2 shows the abundance distribution for the pooled inaterial linin sites 1 to 7. The abundance values are the numbers of beetles triipped at cacli site during one week per month from June to September (Table 14.2). The distribution is log-normal, apart from the peak of very rare species. Such bimodality suggests a natural dichotomy of species into the ones that have a breeding population at the site versus the others, the rare species, which are likely to be represented by immigrants from elsewhere. Coinparison benveen Cummrmifies ut Dgfqreiir E l o d o n s Siibalp,iile comnncniries. Four successive waves of species replace each other from spring to autumn at the Bessans site, where eleven coinnion species of the twenty-two local species form the core of thc assemblage (Tablc 14.3). The percentage similarity of the species composition in wccessi\'e months is only about 30%, indicating extensive seasonal turnover in species. Typically, each core group is comprised of species of different size. For example, in Augusl the five core species have the following dry weights (~ng):1.3. 4.0, 4.6, 5.9, and 19.8. The first wave of species in June consists mainly of three species-Ap/lodius depressur, A . crroricus, and A. obscui-tis-which reprcsent 8 I%of the numbers and 85% of the biomass of beetles. The second wave i n July also'lias three core species, of which only one was abundant in June ( A . crrotirus). This group accounts for 73% of beetles caught i n July. Their numbers rapidly decline while the third wase of species emerges in August (Table 14.3). w-ith twenty species and five core species, A . rujipes, Hepluducus cariirarlrs, A . obscurus, A . hueinorrhoidalis, and A . rufus (79% of individuals and 80% of biomass). As most of tlie species active in August were ~~lready Qrcscnt in early spring, the summer community is stable in species composition in spitc of great changes in dominance. The autumn community appears suddenly (Table 14.3). Some of the autumn species were present at low density in summer, but rlicir numbcrs rapidly

Othcr spccics Nunibcc ulspccics

10.8 8. I 3.0 Y.3 0.2 2.4 0.8 I1 8

30.3 16.8 6.0 3.6 0.5 0.4 0.3 0.8 0.3

4.0 16

5.2 1.3 10.6 12.8 24.0 22.')

2.0 4.5

4.2 0.3 2.4 I .8 2.8 0.8 31.7 21.7 20. I

12.4

3.1

6.0

17

20

17

25.8

9. I I.?

'

253

increase. in Septeniber with the emergence of a new generation. Seventeen speries were observed in September, but only three of them contributed to the core group: Onrlio~~ltujius frncriconiis. Aphodiirs con,iiius, and A. fiiiieturi~is (80% of beetles). Gcoti-ripl,rs .rtercoriiriii& constitutes an imporrant functional species in Septetnber. with 55% of total hioinass in spite of its low frequency (2.5%). Lower- olpirie coritinuiiities. Only three seasonal waves of species were recorded at the Bonneval site. Thiiieen species are involved in the first wave with thrcc core species. lo .luly the core group consists of Oirthopliogus borc r i r d i (l5%), 0 . fracticorizis (16%), A . el-r-aticris (24?6), and A. obscarrcs (24%). The autumn wave of species is relatively distinct as at lower altitudes, with elcven satellite and three core species: 0.f,-acticoriiis, A . obsc!iriis, and A . /iinretnrii~s. Upper alpine, srrbilivul, mid riival cmiiitiiiiiilies. At mid- and high altitudes, dung beetles are scarce in spring (June) due to the late melting of s ow, and 4 the species number does not peak before late July. Species diversity then remains high until September, particularly in the nival communities. Two types of community organization c m bc distinguished in these CoIiiIiiunities: (1) specics emerge i n a rapid succession, but with little overlap between tlie peaks of cmcrgcnce; the species tend to differ io size (upper alpine communities at La Ramasse and Grand Plan sites); (2) species emerge synchronously in summer, with prolonged activity in autunin (subnival and nival conimunilies). The species coinposition of the upper alpine communities does not change

..

...

254

.

Chapter 14

much from spring to early autumn, though the species composition may vary from one site to another. In La Ramasse, the early wave of dung beetles includes two dominant species, A . amblpdon and A . obscurus. These species are rapidly replaced in July and August by a stable community of eleven species, the three numerically dominant species representing 85% of the total. In September, this community collapses suddenly and the last wave of beetles emerges, dominated by A. tenellus and A. fimerarius (82% o f total). The organization of the Grand Plan community at 2,230 m is similar to the previous one, in spite of the higher altitude, which delays the spring emergence of the earliest species. As soon as the snow has thawed, the summer wave suddenly emerges, with A. obscurus and A. alpinus being the two constantly dominant species, while a third one, A . depressus, is progressively replaced by the smaller A . satyrus with increasing altitude. The summer community disappears suddenly and is replaced by a new wave of dung beetles, among which A . tenellus is dominant. Three main sites were studied in the subnival and nival zones. The tliickncss of the snow cover delays insect activity until the middle of June, sometimes later. The first dung beetles to emerge at the Pant du Montet site (2,4 10 m) are A . obscurus and A. fmefurius, represented by small numbers of individuals flying between large patches of.snow. When the snow has complefely disappeared, an explosive emergence of thousands of beetles can be observed within a few days (Appendix B. 14). In early July, an average of 324 beetles was collected per pitfall trap in six days. Throughout the favorable period of activity, A . obscurus and A. alpinus (or A. satyrus depending on the site), form the core group. At the highest sites-for example, Balcon du Montet (2,760 m)-a community of six or seven species is dominated by A . obscurus, representing from 92% to 96%.of individuals active at any time.

.; '

14.6. SUMMARY At high altitudes, climatic constraints, in particular low temperatures and long-lasting snow cover, restrict the favorable season for dung beetles to a few months. High-montane dung beetles exhibit several adaptations to enable them to complete their life cycle in ihe short period of time available. One .such adaptation is to be ready to rapidly exploit the resources when they become available in early summer. In many dung beetles this is achieved by '. overwintering in.the adult stage. Species have typically very short breeding seasons, possibly because of competition with other common specics. Short breeding seasons allow successive core species to develop during the favorable period, with those occumng at the same time being generally of different size. In spite of the harsh environment, the montane dung beetle communities appear to be highly structured, which may contribute tu high species richness even at high altitudes, up to 2,200 m in the Alps.

CHAPTER I S

Native and Introduced Dung Beetles in Australia D . rM. Doube, A. Mucyueen,

T J. Ridsdill-Smith, and T A . Weir 15.1. INTRODUCTION

The Australasian land mass drifted apart from the rest of the Gondwana at the time when the dinosaurs were the dominant dung producers, 100 million years BP. During the past 25 million years, but excluding the last 200 years, the dominant herbivores and dung producers in Australia have been marsupial macropods with about fifty extant species (Tyndale-Biscoc 197 I), togcthcr with the wombats in eastern Australia. The culmination point fur dung beetles was the year 1788, when the arrival of Europeans and their livestock altered the herbivore complex dramatically and created an entirely new situation for dung beetles. The current dung beetle fauna in Australia consists of two elements: the indigenous species, most of which are adapted to use marsupial dung (Matthews 1972, 1974, 1976), and a suite of species that have been introduced over the past two decades for the biological control of bovine dung and dungbreeding Ries (Waterhouse 1974; Bomemissza 1976). The distribution of most indigenous species is given by Matthews (1972, 1974, 19761, but their biology .' and ecology are poorly known; they are of limited economic importance and are largely restricted to forest and woodland habitats. A few indigenous species are common in the open grasslands of southern Australia, where they use the dung of cattle, sheep, and horses. These beetles are probably now more abundant than'they were prior to European settlement due to the increased supply of dung. In contrast, many of the introduced species are ugely abundant in open pastures, and some of these species have spread to most of Australia. Today, at least one introduced dung beetle occurs in practically every pasture in Australia. In this chapter we review first the geographical distribution and habitat associations of the indigenous species (Section 15.2), then examine the attempt to establish an integrated complex of exotic dung beetles in Australian grasslands (Section 15.31, both in tropical and subtropical regions (Section 15.4) as well-as in temperate regions (Section 15.5). The roles of biotic interactions

2

256

'

Australian Dung Beetles

Chapter 15

and abiotic factors in determining the relative abundances of the species will be considered in Section 15.6. The invasion of dung beetle communities by new species is discussed in Section 15.7 in the light of the Australian expen" ence. 15.2. THEINDIGENOUS FAUNA There are 315 described species of indigenous dung beetles belonging to twenty genera in the family Scarabaeidae in Australia (Table 15.1). The indigenous fauna also includes 127 species of Aphodiidae and 40 species of Hy-

Family Trrbe Genus

Trtbe

N,,

Geotrupidae Geouupini

Georrupes

Bolboceratini

Elephaslomus

Scarabaeidae

Onthophagini Onthophagus Onirini Onitis Cheironiris Bubas Oniticellini

Liaungus Euoniricellus

Coprini

Copris Coprodactyla Thyregis Dichohini Dernorziella

species described by Storey and Weir (1989).

Genus

Sisyphini

Neosisyphus

Gymnopleurini

Allogymnoplcurus Canthonini Canrhon Aulacopris Cepholodesmius Conrhonusoma Amphisromus Labroma

N,,,J

N.,,,

-

5 (3)

-

I(-) -

3

3 3'

in

3

-

2

8

-

Boleroscaprer Aprenocanlhon pseudignainbia Leponus sauvagesinella Monoplisles Diorygopyx Tmnoolectrofl

2 3

-

ressedon

2

21 3 6

n

10

251

hosoridae, many of which are thought to be copropbages, as well as one coprophagous Geotrupidae (Came 1965). Most species occur in the higher rainfall coastal regions, but a few species are present in the dry interior of the continent. Some of the islands adjacent to the Australian mainland have simple dung beetle assemblages. Eight species of Onthophagus occur in Tasmania, which has been periodically isolated from the mainland, but only one of them is endemic (Matthews 1972). New Zealand has 14 species of Canthonini in two endemic genera as well as one introduced Copris (Matthews 1974). New Caledonia supports 20 species of Canthonini in eight endemic genera (Paulian 1986, 1987b), with one accidentally introduced Onfhophagus and 3 other introduced species (Gutierrez et al. 1988). Vanuatu has 3 deliberately introduced species and one accidentally introduced Copris (Gutierrez et al. 1988). Norfolk Island has no endemic dung beetles but now supports an introduced fauna consisting of 3 species of Onthophagus, one species of Euoniticellus, and one species of Onitis. In contrast to these impoverished faunas on small islands, New Guinea and the offshore islands have 103 described species in nine genera in the tribes Onthophagini, Canthonini, and Coprini (Balthasar 1970; Psulian 1985; Krikken 1977; Weir, unpubl.). Seven of the yenem and at least 7 species are shared with Australia, while a further 3 species have been introduced for the control of cattle dung.

Geographical DisrriOurior~s

Menrophilus Coproecu.

1

'

-

-

-

The major geographical constraint on beetle dispersal in Australia has been the central desert, which has isolated southwestern from eastem Australia. The different tribes of dung beetles differ markedly in their patterns of distribution over the Australian mainland. Onthophagini is represented by only one genus, Onrhophagus, with 191 species (Table 15.1; Matthews 1972; Storey 1977; Storey and Weir 1989). most of which are restricted to the northern and eastern regions of Australia (see Fig. 12 in Matthews 1972). Eight of the 9 species in southwestem Australia are endemic. The tribe Coprini includes two genera and 15 species, while Dichotomini has 14 species (Table 15.1; Matthews 1976; Matthews and Stebnicka 1986). Demarziella (14 species) and Coptodacryla (1 1 species) occur largely within several hundred kilometers of the northern and eastern seaboards of Australia. The genus Thyregis is represented by 3 species in southeastern Australia and one on the western coast. The tribe Canthonini has sixteen indigenous genera with 96 species (Table 15.1; Matthews 1974; Storey 1984, 1986). Four genera (Labrorna, Coproecus, Mentophilus and Sauvagesinella) are restricted to western Australia (WA), while most of the species in Tesserodon and Mo~loplistesoccur in the summer rainfall regions of northern Australia. Three species of Aulacopris

"

* 258

.

.

Chapter 15

Australian Dung Bectlcs

and Lepanus occur in Victoria with distributions extcnding to New South Wales (NSW). No indigenous Canthoninj have been recorded in South Australia (SA). Most of the species in the remaining genera fall into one of four broad distribution patterns: (1) coastal NSW and southern Queensland (Diot-ygopyx. Cephalodesrnius, Aulacopris, and Aptenocanrhon), with relict distributions in Aulacopris and Aptenocanrhon in high-rainfall montane regions in north Queensland (Storey 1984, 1986); ( 2 ) Queensland (Pseudignambia, Cunlhonosorna, and Boktoscapfer); ( 3 ) coastal Queensland and Northern Territory (NT) (Ternnoplectron); and (4) widespread along the coast from NSW to NT (Lepanus and Amphistornus). The Australian fauna shows a high level of endemicity at both generic and specific levels, which, together with the presence of archaic groups in the Coprini and Canthonini, gives the fauna a strongly insular aspect, unlike that of other regions of comparable size but reminiscent of the endemicity on some continental islands (Matthews 1976).'One of the two genera of Coprini and eleven of the sixteen genera of Canthonini are restricted to Australia (Matthews 1974, 1976). Most of the Australian species of the cosmopolilan genus Onthophagus are endemic. Matthews (1972) considcrs that OnrhOphrrgus may have originated in Africa, where there are uver 800 species, and to have entered Australia from the north (Chapter 4 ) .

Habitat Selection, .Food Preferences, and SeasonalActivily . : , . ,

The majority of the Australian indigenous dung beetles are associated with woodland or forest (Matthews 1972, 1974, 1976; Donovan 1979). In north Queensland, Fenar (1975) found that indigenous species were rare in cattle dung in open pastures, though there are some Onthophagus that occur in pastures and open savannas in northern (e.g., 0 . capella, 0. consenlu~~cus, and 0. rubrimaculatus) andkentral Australia (e.g., 0 . slounci: Matthiessen ct al. 1986). In southern Australia, a few species (e.g., 0. ferox, O.cupcflu, 0. mniszechi, 0. granularus, and 0. australis) are common in open pastures as well as in woodlands, and in some years they become seasonally abundant and cause substantial disruption of cattle dung pats (Hughes 1975; Donovan 1979; Tyndale-Biscoe et al. 1981; Ridsdill-Smith and Hall 1984a). In contrast to Sdahaeidae, .many indigenous species of Aphodiidae appear to he scarce in dense forest. For example, Williams (1979) and Williams and Williams (1982, 1983a, 1983h, 1983c, 1984) extensively surveyed the small wet Forests of coastal NSW and found numerous species of Onthophagini and Canthonini but caught only small numbers of a few species of Aphodiidae and Hybosoridae. Ridsdill-Smith et al. (1983) found twenty to forty times more Aphodiidae in open forest (jarrah) and heath than in tall open forest (kani). In southwest-

.

25Y

ern Australia, six species ( iphodins occur in pastures though only [be accidentally introduced A . p ~ c [ ~ l ~ d o lisi ~abundant i d ~ ~ (Ridsdill-Smith and Hall 1984a). The food preferences of the indigenous species have received little systematic attention. except for the work of Donovan (19791, who trapped six Onrhophagus species using five different types of hait. He found that traps baited with human dung caught by far the largest numbers of beetles, while the other baits were less attractive, the order of decreasing preference being horse, ,sheep, cattle, and kangaroo dung. Matthews (1972, 1974, 1976) concluded that mammalian entrails are the most effective bait, human dung is less attractive, and herbivore dung is relatively ineffective. The large majority of species appear to be coprophagous, but other types of food are also consumed, and a small number of Onrhophagus species are copro-necrophagous. Fourteen species of Onthophagus appear to be restricted to mushrooms, and one species feeds on fallen fruits (Matthews 1972; Storey 1977; Storey and Weir 1988). Ridsdill-Smith et al. (1983) noted that in southwestern Australia, species of Onrhuphojiss and Apliodirrs prefer dung over carrion. while Canthonini arc cqually atlmcted to botlitypes of bait. Sonic Onrhophugus species have nioiphnlogicel and behavioral adaptations that Facilitate their access to fresh macropod dung. These beetles have prehensile tarsal claws by which they hold on to the fur of macropods, especially in the cloacal region. As a fresh dung pellet i s extruded, the female beetle seizes it and falls to the ground with it. The pellet is then buried and provides food for one larva (Matthews 1972). Seasonal changes in adult activity have been documented for a number of indigenous species (Tyndale-Biscoe et al. 198I ; Ridsdill-Smith and Hall 1984a,b). These results conform to the usual pattern, with activity restricted to the moist seasons and being minimal during dry periods. Weir (unpubl.) found similar patterns among the Coprini in the forest regions around Cooktown in north Queensland, hut there were some Ontliophagus species that were most abundant during the dry season. Abundances can vary enormously from one year to another. For example, at Uriarra near Canberra, 0. grariulairis numbered from three hundred to three thousand beetles per trap in 1 9 7 6 77, hut during the next two years the catches rarely exceeded hundred individuals per trap. Such abundance fluctuations were explained by dhught and associated poor-quality dung in critical times o f the year (Tyndale-Biscoe et al. 1981).

The EIfecr ofHrrman Colonizafiort Aboriginal colonization of Australia dates hack at least 50,000 years, and it is apparent that the early colonists wrought substantial changes on the Australian landscape, primarily through the use of fire, hunting and the introduction of

260

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Chapter 15

the dingo (Singh and Geissler 1985; Singh et al. 1981). Fire altered the patterns of vegetation distribution. The extinction of the large grazing and browsing herbivores (e.g., dipmtodons and giant macropods) about 10,000 BP (Tyndale-Biscoe 1971; Owen-Smith 1987) reduced the types of dung available. These changes may have had severe consequences to indigenous dung beetles with narrow habitat and dung-type preferences. The European colonization of Australia over the past two hundred years has caused equally or more dramatic changes to the landscape through the clcaring of bushland for pasture, agriculture, and settlement, and through the introduction of exotic pasture plants and domestic mammals. The total area of 'many habitat types has severely contracted, thus restricting the distributions of their occupants, including the dung beetles. Large tracts of grazing land are now populated with cattle, horses, and sheep, but only a few species of indigenous dung beetles occupy this habitat. The CSIR0,Dung Beetle Program is attempting to redress this ecological imbalance by importing exotic dung beetles that are adapted to use the dung of domestic cattle in open pastures.

Badaiar

Rochhamptm

15.3. THEAUSTRALIAN EXOTIC DUNGBEeTLE FAUNA Domestic animals were brought to Australia by the early European settlers. As animal numbers increased, a major problem arose with the accumulation of dung. Currently cattle are estimated to produce 35WOO million pats per day (Waterhouse 1974): In the absence of dung beetles, cattle pats foul valuable pasture for prolonged periods of time in the more intensively grazed areas, and the fiber and nutrients locked up in dung pats are not rapidly incorporated into the soil to maintain its fertility. Furthermore, two important fly pests in Australia breed almost exclusively in cattle dung: in tropical areas the blood-feeding buffalo fly, Hoematobia irritons exiguu, which infests cattle in large numbers; and in inland. and southern areas the ubiquitous bush fly, Musca vetustissima, which pesters man and beast alike. The aim of the CSlRO Dung Beetle Program has been to establish in the Australian pastures a dung beetle fauna that would rapidly bury the dung of the domestic stock (mainly cattle), and thereby benefit pasture production and reduce the numbers of pest flies. The selection procedure to secure the dung beetles has involved two phases. First, the"c1imates of the Australian target areas were matched with those of the prospective donor regions overseas. The climatic maps of Walter and Lieth (1964) were used to identify regions with similar temperature and rainfall patterns (Fig. 15.1). Further considerations of the diversity of foreign dung beetle Faunas led to the selection of parts of Africa and Europe as donor regions (Bornemissza 1979; Ridsdill-Smith and Kirk 1985; Kirk and Ridsdill-Smith 1986; Doube 1986). Tropical southern Africa was the chief source of species

Fig. I S . I. The study siics in iiurlhcrii and soutliwcstciii Australia and thcir climaiic diagrams. Ovcncas silcs with hurnolugous climales are shown fur comparison. The climatic diugrmu (aflcr Walter and Lieth 1964) show mean monthly temperature (thick linc) and rainfall on a coiiiiiion scalc; dry periods (precipitariun < evaporation) arc sh"wn as dullcd itrcas and ~lioistpcriwls (precipitalion > cvnpnruion) arc shnwn by vcrtici~Iincc. l31mk m u 6 ~ C I I O ~ Cwcl months rcccivilig cainl'all i n CXCCSB of 100 trim, on rciluccd scalc ( 1 - 10).

. 262

.

Chnptcr 15

for northern Australia, while the Cape Province (South Africa) and southern Europe provided species for southern Australia. The initial criteria used to select particular species were listed by Bornemissza (1976), and these criteria were progressively refined as a greater understanding of dung beetle biology was acquired. Between 1968 and 1982, surface-sterilized eggs of fifty-two species of dung beetles were received at the CSlRO quarantine laboratories in Canberra. The eggs were placed into cavities in specially prepared dung balls, in which the beetles developed to the adult stage (Bomemissza 1976). Either the reared adults or their adult progeny were released in the field. The releases were usually conducted in such a way that possible interspecific competition was minimized. Where possible, individuals of the introduced species were confined in crude field cages and supplied with fresh dung for up to a week following their release to encourage breeding at one site. Most of the early releases in northern Australia involved multivoltine, high-fecundity specids, of which 300-500 insectary-reared beetles were yeleased at each of several sites in areas with a favorable climate. These species often built up large populations within a few years of release; their progeny were collected lor redistrihution to other areas to assist natural dispersal. A total of forty-one species was released and, to date, twenty-two species have established breeding populations in the field (Table 15.1). The reasons for the failure of establishment of some species are discussed in Section 15.7 (some imported species were not released at all because it proved impossible to rear them satisfactorily in the laboratory). The early successful establishment of beetles has been summarized by Bornernissza (1976, 1979), and the piokressive establishment and spread of species have been referred to by other CSIKO workers (papers by Wallace, Macqueen, Tyndale-Biscoe, Hughes, Doube, Ridsdill-Smith) and detailed in CSIRO annual reports. However, no comprehensive ecological analysis of the introductions has been published, so far. Currently at least one exotic dung beetle occurs in almost every Australian pasture, and up to seven species occur together in a few localities. Some species occur over much of the continent. while others are restricted to the northern or southern regions. Tropical and subtropical study sites at which dung beetle populations have been monitored include Townsville, Rockhampton, and Brisbane in Queensland (Fig. 15.11, while temperate communities have been examined in NSW, near Canberra (cool tempefate), and near Perth, southwestern Australia (winter rainfall). The next two sections examine the situations in Queensland and southwcstcrn Australia in more detail.

15.4. BEETLESOF SUMMERRAINFALLREGIONS The first species to be introduced to Australia were released in 1968 at several sites in coastal Queensland (Fig. 15.1). where the dung-breeding buffalo fly

Australian Dung Bectlcs

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263

is a serious pest of cattle. Populations of these beetles became established in numerous localities, and they were monitored with pitfall trapping over anumher of years at three of the original release sites near Townsville, Rockhampton, and Brisbane. Indigenous Australian species were scarce in open pastures, and relatively few were caught in the pitfalls. At Kockhampton in coasral central Queensland, seven introduced species have so far established brceding populations, of which sixspecies were present in 1986 at the end of the monitoring period (Table 15.2): Seusonnl Abiindunce and Acriviry

The same broad pattern of seasonal activity has been apparent at each of the three monitoring localities, of which data are given for Rockhampton in Fig. 15.2. Adults of all species are relatively common during the wanner months of the year, and they are scarce during the.cool, dry winter period, in July and August (Fig. 15.2). Two species, Sisyphus (Neosisyphus)spinipes and Oniris viriddirs, emerge in large numbers earlier in the season than the others. 011thop/~ugz~.s ( ~ i ~ i c r ~ ~ l c h r ~ ~ ~ /glm r ~c j/ /i [l ir,sElronifice/his ) ;l?lcrrnediii,s, and S. .spinipes show typically one or more periods of exceptional abundance each season, when up to several thousand beetles may be caught per trap in twentyfour h o u r s Such mass occurrences, following the emergence of new adults, s o m h n e s persist for several weeks. The patterns of seasonal change in these species have seldom been synchronous at the three localities, probably because of some differences in local rainfall patterns. In coastal central Queensland, breeding by the tunnelers was studied by counting the number of broods excavated from beneath dung pats in the field. Breeding occurred primarily in spring, summer, and early autumn. but the species showed some differences in timing within breeding seasons (Fig. 15.2). Eiiorriticclliis irirerniedius can breed throughout the year, albeit sporadically during the cooler months. The other species terminate breeding in autumn but the adults may survive for many weeks, depending on the severity of the winter. In mild .winters some adults survive to breed in the fdlowing spring. Larvae develop slowly to fully fed third instars during the winter and early spring, but they do not pupate until they receive an environmental s imulus t , ' Some species (S. S J J ~ I ~ ~and ~ C ES . inrermedius) respond largely to increasing temperatures in the spring, since pupation and adult emergence can occur in the absence o f rain in others (c.g., 0. gazella), the first cnicrgence of new adults in the spring does not occur until there is adequate soil moisture (Macqueen, unpubl.). Seasonal changes in beetle activity lead to corresponding changes in the level of dung dispersal, which has two components: a part of a pat is actually removed by beetles, while another part or all of the remainder is shredded into fragments but not removed (Fig. 15.3). Broad agreement was found between

,,I

..~..

Australian Dung Beetles

-

Adult beetles

v)

..--.,

'

265

Broods

S. spinipes

L; rnjlilaris

W

m

0

o

sagrttarrus

E. mtermedius

0 vindulus I

MONTH Fig. 15,.3.Scironal changes in the level of dispersal of dung pats at Rockhampton. This lipurc is bescd on rcsults for eight years (1975-85).

266

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Australian Dung Beetles

Chapter15

contrast, up to twelve thousand beetles were collected per pitfall trap in twenty-four hours in other years with high rainfall and/or low stocking rate, when the pastures grew tall and dense. In some years, S. spinipes has been scarce on overstocked, denuded pastures but abundant in adjacent, wellgrassed pastures. At Rockhanlpton, 0. sagirtorius decreased in abundance following the establishment of additianal species (Table 15.2). Tyndale-Biscoe (pers. comm.) observed a similar decline in the numbers of E. inrermedius at Nmabri (NSW) following the establishment of 0.gazella, and of Oniris alexis in the Araluen Valley (NSW) following the establishment of a number of species, including Onthophagus binodis. The explanation of these trends is not clear, but tbe declines of 0. sugirturius at Rockhampton and of E . intermedius at Narrabri have been attributed to increased interspecific competition, especially with 0. gazella.

the level of reproductive activity (numbers of brood balls produced) and the amount of dung dispersed, but there was no clear relationship between the numbers of beetles collected in baited traps and the level of dung burial or shredding (Doube, Giller, and Moola 1988). The proportion of the pat removed by beetles after seven days was independent of pat volume in the range from 0.5 to 3.0 liters, so that larger pats had a greater mass of dung remaining (Macqueen, unpubl.). This has important implications for the other members of the dung insect community.

Community Structure The Australian experiment provides a unique opportunity to study the development of dung beetle assemblages by serial introduction of species. The observed abundance changes in the introduced species in three localities in coastal Queensland are shown in Table 15.2. The most comprehensive data set, coveribg fourteen years, is availablc for Rockhampton. Onthophagus guzellu, Onthophagus ( D i ~ i l a ~ ~ J l ~ o p h usuggl[s) itrurius, and Liutangus militaris were first released in 196&69; Euonilicellus intermedius arrived by natural spread, S. spinipes was released in 1972, and 0.viridulus in 1977. The first year of exceptional overall abundance occurred in 1978-79, following substanti&rain in winter and spring of 1978. Beetles were also very abundant during the years 1983-86. However, the performance of different species has varied markedly, and there is no one pattern common to all species. Some species, €or example, 0. guzellu and L. militaris, show no obvious trend over the study period, while 0. sugittarius has declined markedly since 1978-79; other species, for example, E. intermedius and S. spinipes, have increased dramatically during the latter part of the study period. The rank order and absolute abundances of the species have varied widely over the seven-year period for which data are available for the three study sites (Table 15.2). Two conclusions can be drawn from these data. First, some species have been consistently more abundant (e.g., S. spinipes, E. inrermedius, and 0. gazellu) than others (e.g., 0. sagittarius and Onitis viridulus), though no one species has been consistently dominant at all three localities during the years examined, despite substantial climatic and biological similarities among the sites (open grassland grazed by cattle on loam or clay soil with stocking rate ranging from 0.1 to 0.8 beasts per hectare). Second, there have been substantial year-to-year difkrences in the mean abundance of individual spccics as well as in tbe overall numbers of beetles. Some years were highly favorable for breeding while others were relatively unfavorable, and different years favored different species. For example, S. spinipes, which places its broods in grass tussocks, was scarce in drought years, when grass tussocks werc grazcd short and the broods were exposed to tbesun and often trampled by cattle. In

267

'

Beetle A6rindance in Africa Orid Australia Because the nature of the habitat is a major determinant of dung beetle abundance (Nealis 1977; Doube 19831, comparisons of abundances between continents require that beetles are sampled in similar habitats. The data in Table 15.3 are based on beetles trapped during the active season over three years, in

,',

TAHLE 15.3 The abundance of live species of African dung beetles in grassland graed by largc buvids (pastor8l4attle: game kserve-Cape buffalo) in the Hluhluwe district of Natal, Sourh Africa. and n c i r Ruckhampion. Australia. Africa

Atuwa1ju

Hluhluwe Pustorul

Hh,hl,,we Game Reserve

Spccicu

0.guvllo L . militoris E . irirerrnediius S. spiniper 0 . viridulss

I982 5

7 13 1

1983

1984

3

I 3

I3 14 S

1

1982

1983

I 7 18 1

2 . 9 28 3

- -

Rockhampton Postural 1984

1982

I

81 5

7 4

121

,

'.

1983

1984

99 96 689 792

98 46 497 1,208 5

-

-

* *

26

38

6

27

42

I4

213

1,682

1,854

Pcrccntagc of 811 bcctlcs lrappcd

44

11

12

43

20

25

100

100

100

Numbcroftraps

108

81

42

108

81

42

78

78

12

Turd

I

6

*

- q

p.!

!>

'

.

. 268

.

, .

Australian Dung Bccllcs

Chapter 15

three localities with similar climates and extensive tracts of clay-loam grassland grazed by large ruminants. The main result is that the introduced beetles at Rockhamptonin Australia have been many times more abundant than populations of the same species near Hluhluwe, South Africa: 0 . guzellu X 70, Liutongus miliraris x 10, E . intermedius X 50, S. spinipcs X 400, and 0. viridulus x 390. The densities of these species in Hluhluwe were of the silnlc order of magnitude than in other years and in other, Comparable localities i n South Africa (Doube, unpuhl.). Even more striking than the differences in the abundances of these species is that the total biomass of all dung beetles was ten to one hundred times greater in Rockhampton than in Hluhluwe. Since the .'same type of' bait and traps were used in both localities, we conclude that the introduced species breed much more successfully in coastal regions of northeastern Australia than they do in homologous areas of South Africa. These differences are also reRected in the level of dung dispersal observed in the two localities. Doube, Giller, and Moola (1988) found that there was almost complete dispersal of dung i t Kockhampton in the summer of 198182, whereas in parallel studies conducted in the Hluhluwe Game Reserve the level of dung dispersal was found to be 53% in grassveld and only 32% in bushveld. Additional unpublished data collected from 1980 to 1986 in Al'rica indicate that the level of dung dispersal observed in clay-loem soils insidc and outside the game reserve is consistently lower than that observed in the northem Australian regions where exotic dung beetles are abundant. In contrast, the level of dung dispersal during summer is extremely high on deep sandy soils ,in the summer rainfall regions of South Africa (Doube, Giller, and Moola 1988). The reasons for the.relatively low biomass ofdung beetles in the Aliican clay-loam systems are'not known but may he related to predation on buried dung by termites (Chapter 8).

15.5. BEETLES OF WINTERRAINFALL REGIONS One of the main aims'of- dung beetle introductions to southwestern Australia was to reduce the abundance of the pestilent bush Ay. This Hy shows a short period of rapid population increase in the spring (Matthiessen 1983), when few beetles are active at present (Ridsdill-Smith and Hall 1984a). The introduction of exotic dung beetles has increased the level of dung dispersal and has extended the time over whichthat dispersal occurs, particularly in summer and autumn, thus shortening the bush Ry season substantially (Kidsdill-Smith and MatthiesBen 1988). Nine of the fourteen species introduced from southern Africa and Europe have become established so far. The first beetles were released in southwestern Australia in 1972. Three African species, Onitis alexis, Euotiificellus infermedius, and Onthophagus binodis, were present in substantial numbers by 1978, and the other species now established are Oniris ayglrlus and Onifis

265

cofler from South Africa; Onthophagus fourus from Greece, Spain, Italy, ant Turkey; Euptilficelluspallipes from Iran and Turkey; Euoniticellusfulvus froin France; and Bubas bison from France and Spain. The distribution and basic biology of these species are described by Kidsdill-Smith et al. (1989). Of the nine established species, all except B . bison are also established in southeaste m Australia. Introduced dung beetles now occur in niost of the areas wherc cattle are present, though the distribution of some species is still very restrictet (Ridsdill-Smith et al. 1989). The dung beetle fauna of this region has beer increased substantially from eighteen to twenty-seven species, but Ridsdill. Smith and Matthiessen (1984) and Ridsdill-Smith and Kirk (1985) argue fo the introduction of further species that would have their main period of activit: in spring, to coincide with the critical fly-breeding season. Seasonul Abundance and Activiiy The seasonal occurrences of the native species and most of the introduce species ase markedly different. The native species show a bimodal pattern I seasonal activity in the cooler regions but a unimodal pattern in the w m n regions. At Busselton, 200 kill south of Perth, the endemic 0ittliopIuigii.sfen shows a bimodal pattern with substantial adult activity in spring and autuiii when the soil is moist and the temperatures are sufficiently high; hut ifs se sonal occurrence becomes unimodal in the warmer regions north of Busselto where beetles are active throughout late autumn and winter (Table 15.4). In contrast to thc bimodal pattern in the native species, the introduced SI cies 0. binodis and E . paUipes are active during the dry summer and autur months, and their seasonal activity is not affected by soil moisture, as I results are the same for localities where pastures are irrigated (Dudanup) a where they are not (Busselton; Table 15.4). Nonetheless, soil moisture likely to affect the abundance of these species. Barkhouse and Kidsdill-Sm (1986) have shown that in dry, sandy soils breeding by 0. binodis is restric to the damp soil beneath the pat; hence at higher densities intraspecific cc petition for breeding space should be more intense in dry than in moist soi' The situation in southwestern Australia hears a remarkable similarity to situation in the Mediterranean regions of southern Africa (Davis 1987), wl. the dung beetle fauna consists of two elements. One is gmup of soutll endemic species, which are restricted to the winter rainfallalegions. These I cies are active during autumn and spring but are inactive during the hot SI mer months, and they are largely restricted to regions of undisturbed nat vegetation. The second element, which includes 0.bitrodis, occurs throt out the summer rainfall and winter rainfall regions, primarily in pastures; is the dominant fauna in the pastures of the Cape Province during summel Other species introduced to southwestern Australia, such as 0. cnJfer I wards 1986a,b) and B . bison (Kirk 1983), are univoltine, with adult act

Australian Dung Beetles

'

27 I

in autumn and spring. In southwestern Australia, 0 . coffer and B . bison are prcsent only in low numbers, but they appear to show the Siltlie phenology in 'Australia as in South Africa and Spain, respectively. As further univoltine species with restricted breeding seasons are added to the fauna of southwestern Australia (e.g., Copris hispanus; Ridsdill-Smith and Kirk 1983, the contrast in the seasonality of the native and introduced species will diminish.

-z

Cononunity Structure

1:

I -.I 1'"

I 1 -

The introduction of a suite of exotic dung beetles to southwestern Australia provides an opportunity to examine whether the introduction of new species affects the abundances of the species already present. However, until now most of the introduced species are active during seasons when the majority of the native species are inactive, and the introduced species occur in pastures where most native species are scarce or absent. It is therefore not surprising that while the numbers of the introduced beetles 0. biiiodis and E . pdfipes increased markedly in 1979-84, the abundances of the native species 0.fcrox and the cosmopolitan A'. pseudolividus remained relatively constant (RidsdillSmith and Matthiessen 1988). However, as species with wet-season activity (e.g., 0. eo&) spread and further species become established, competitive interactions between the native and introduced species may become more widespread. It is not known whether any of the introduced species will colonize forested regions, where most of the endemic species occur, and whether the introduced species would consume marsupial droppings, the prefened food of the native species. The endemic dung beetle communities of the Mediterranean climate in southwestern and southeastern Australia are strikingly different (RidsdillSmith 1988). In southwestern Australia, there are ten species of Canthonini and seven species of Onthophagini, all but one of which are restricted to this region (Matthews 1972, 1974). In comparable climates in southeastern Australia, therc are no Canthonini and nineteen species of Onthophagini, but only 25% of them have distributions restricted to Mediterranean climate regions (Matthews 1972). The two regions of Australia have thus developed distinctly different faunas, despite marked climatic similarities. Thc indigenous dung beetle Fauna of Australia is less rich in species than that of the Mediterranean climate regions of the Cape region of kouth Africa, and of southern Spain and southern France, but considerably richer than the Mediterranean climate areas of the west coasts of North America and South America (Ridsdill-Smith 1988). The most obvious difference is the higher biomass of spring-active coprine and onitine beetles in pastures in Spain and France (Ridsdill-Smith and Kirk 1985; Lumaret and Kirk.1987) than in southwestern Australia (Ridsdill-Smith and Hall 1984a). ..*

272

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Australim Dung Bectlcs

Chapter 15

15.6. DETERMINANTS OF RELATIVEABUNDANCE Most of the introduced dung beetles in Australia are adapted to cattle dung in open pastures, and they are less abundant in sheep pastures and in woodland and forest. Provided that a suitable habitat with adequate food resources is available, the geographical distribution of a species is determined by its climatic tolerances, with the caveat that natural climatic barriers, such as the central and southern desens in Australia, may prevent species colonizing otherwise suitable regions. For example, it was necessary to introduce Onthophugus ruurus and 0. binodis separately to both southeastern and Southwestern Australia, where they are now common (Henry 1983; Ridsdill-Smith et al. ,1989); they are scarce or absent'in the warmer subtropical summer rainfall regions and arid zones. Other species have broad climatic tolerances (e.g., E. intermedius) and have established themselves over most of the Australian mainland, including the arid zones (Matthiessen et al. 1986), and yet others remain restricted to summer rainfall regions (e&, S.spinipes and U . garella). Studies conducted to date have been primarily concerned with species associated with cattle dung in open pastures. In the remainder of this section we consider the way species' life history characteristics, intraspecific and interspecific interactions, and dung type determine the abundance of the species and ultimately the structure of Australian dung beetle assemblages. Habitat characteristics are also important, especially vegetation cover and soil type. but these factors have already been discussed in the previous sections (see also Chapter 8).

Life-History Characteristics The native and introduced dung beetles in Australia exemplify a variety or reproductive strategies. Some species, for example, the native beetle Omhophagus granularus and the introduced Onitis cuffer (established in NSW and WA), are univoltine in most circumstances. At Uriana, near Canberra, 0. grunulatus emerges in summer and early autumn, but the newly emerged adults breed poorly or not at all because of the low quality of dung. The beetles breed later in the autumn, but larvae do not enter diapause and die during the winter (Tyndale-Biscoe et al. 1981). Adults overwinter in the soil and breed successfully in spring and early summer. Thus, while potentially muliivoltine, the species has an.annual life cycle over most of its range. Otriris cofer emerges and begins to breed in the autumn both in summer rainlall and winter rainfall regions, and breeding continues during winter and spring, temperature permitting. In the field, 0. cuffer requires ten to twelve months from oviposition to adult emergence, but a facultative larval diapause, induced in early summer, can delay the emergence of some individuals until the autumn one or two years later (Edwards 1986a,b).

'

273

Other species are multivoltine. For example, Oniris alexis has one or two generations per year in southeastern Australia, where it overwinters mostJy as a larva in diapause induced by low temperatures (Tyndale-Biscoe 1985, 1988). The first annual generation develops without larval diapause if there is sufficient moisture, but in times of drought the larvae enter diapause (TyndaleBiscoe 1988). In hot, humid areas this species has the potential for several generations per year (Tyndale-Biscoe 1985). Such a versatile life history, in combination with wide tolerance limits for temperature, enables the species to adapt to a variety of climates, and its distribution appears to be limited only by cold, wet winters (Tyndale-Biscoe 1985). Most of the successful and widespread species, such as 0.gazella and E. intermedius, are multivoltine and have high fecundity and no diapause. Dung beetles are generally most active during the seasons when humidity and temperatures are high, and they are relatively scarce during the dry and cool seasons. Hence beetles are abundant following the break of season in late spring in the summer rainfall regions, and following rain in desert environ-. ments (e.g., AliceSprings, central Australia: Matthiessen et al. 1986). Beetles are scarce during periods of summer drought and during the dry winter in the summer rainfall regions, during extended warm and dry periods in deserts (Matthiessen et al. 19861, and during the cold winter period in the winter rainfall regions.

liitruspeciJc and Ii~terspecific Ititeractions Intraspecific competition for dung has been demonstrated in laboratory and field experiments for a number of dung beetles that now occur in Australia (Ridsdill-Smith et al. 1982; Giller and Doube 1989). Results on the abundances of the native and introduced species in open pastures (papers by Ridsdill-Smith, Tyndale-Biscoe, Wallace, Donovan, Doube, Macqueen, and Fay) and observations on their dung burial behavior (Bornemissza 1969; Doube, Macqueen, and Fay 1988) clearly indicate that there are frequently times when the beetles, have the potential to remove much more dung than is available. In these situations, intraspecific competition for dung or breeding sites must limit their reproductive success. The consequences of intraspecific competition for dung vary &h the duuguse strategy of the species. Ball rollers such as S. spittipes often convert a large portion of the dung pat to dung halls. When S.spinipes is abundant (thousands per pat), the entire dung pat is removed within one day, but only a small proportion of the beetles succeed in making a dung ball (Macqueen, unpuhl.). In contrast, in some tunnelers increasing the numbers per pat above a critical density results in a progressive reduction in the level of dung burial and brood production. For example, Ridsdill-Smith et al. (1982) found that brood pro-

274

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Auslralim Dung Beetles

Chapler 15

duction by 0. binodis increased with beetle density up to 20-30 beetles per liter of dung (up to one hundred brood halls per pat), but then decreased markedly until, at 320 beetles per liter, fewer than 5 brood halls were produced per litre of dung. Intraspecific competition becomes moce intense as dung quality decreases (Ridsdill-Smith et al. 1986), and competition is increased by the presence of coprophagous fly larvae (Ridsdill-Smith et al. 1986) and other dung-inhabiting beetles (Giller and D o u k 1989). The breeding behavior of beetles can have a marQed effect on their success in a competitive situation. For example, the roller S: spinipes may feed in the pat for up to 24 hours before removing a brood hall, whereas Sisyphus fNcosisyphus) rubrus constructs a ball within hours of arrival at the pat (Paschalidis 1974). In this respect, S. rubrus has a competitive advantage over those S . spinipes that spend a day feeding in the pat. However, S. spinipes places its brood balls above ground in grass tussocks, hence its reproductive success is relatively independent of soil characteristics, whereas S. rubrus buries its brood halls in the soil. Sisyphus spinipes has’ an ,advantage in heavy soil regions during dry periods. Both Sixyphus species have a competitive advantage over the slow-burying tunnelers, some of which (e.g., 0. viridulus) do not begin dung burial until.46 days after arrival at the pat (Edwards and Aschenborn 1987; Doube, Macqueen, andFay 1988). When beetles are abundant and dung is removed rapidly, there is diffuse competition between diurnal (e.g., S . spinipes and E . intermedius) andcrepusculadnoctumal beetles (e.g., 0. gazellu and 0 . alexis: Wallace and Tyndale-Biscoe 1983). In conclusion, many introduced. species are frequently so abundant that mutual interference and preemptive resource competition reduce their potential rate of reproduction, hut so far only in habitats and during seasons when native species have always been scarce. As the introduced species disperse and mix with one another, levels of interspecific and intraspecific competition will increase. Amphibians (for example, the introduced cane toad Bufo marinus), reptiles, and various insectivorous and omnivorous birds (e.g., ibis, crows, and magpies) and mammals (e.g., foxes) have been observed to eat dung beetles in Australia, hut such predation appears to have little effect on beetle populations in most circumstances. There are no recorded parasites or diseases of dung beetles in Australia, but Ridsdill-Smith (unpubl.) has found nematodes and staphylinid beetles attacking the immature stages of beetles in’the field. .I

Dung Quality The reproductive performance of many species ofdung beetle has been shown to vary with seasonal changes in dung quality (Tyndale-Biscoe et al. 1981; Matthiessen and Hayles 1983; Tyndale-Biscoe 1985; Ridsdill-Smith 1986; Macqueen et al. 1986). Reproductive performance is highest in dung produced

’

215

by cattle feeding on actively growing pasture, and lowest in dung produced by cattle feeding on hayed-off pasture. In the summer rainfall region at Rockhampton, the breeding rate of E. intermedius is maximal in dung collected during summer and minimal in dung collected in winter (13 and 1-2 broods, respectively, per female per fortnight; Macqueen et al. 1986). In the winter rainfall regions (e.g., Perth, WA), brood production by 0. binodis is maximal in spring dung (100 brood halls per pat) and lowest in summer dung (0 balls per pat; Ridsdill-Smith 1986). In southeastern Australia, the native 0. granU ~ Q ~ Uproduced S five times more brood bails with high-quality than with lowquality dung (Tyndale-Biscoe et al. 1981). However, dung beetles, like other dung-breeding insects (Macqueen et al. 1986), do not have a standard response to changes in dung characteristics. For example, the reproductive performance of Oniris alexis is only little affected by seasonal changes in dung quality (Ridsdill-Smith 1986; Tyndale-Biscoe 1988). 15.7. DUNG BEETLEINVASIONS: THEAUSTRALIAN EXPERIENCE

The continuing introduction of dung beetles to Australia and their spread provide an opportunity to examine three recurring questions about the ecology of invasions: (1) Can predictions be made as to which species will he successful invaders? (2) Can predictions be made as to which communities will he most easily invaded? and (3) Can we predict the impact of the invaders on the communities they enter?

The Success of imaders The success of an invading species is measured by its numerical abundance and by its long-term persistence in the new environment. On this basis there are twenty-two successfully introduced dung beetle species in Australia, several species whose success is not yet certain, and less than twenty species that appear to have failed toestablish. All the species that failed are known !o occur in at least moderate numbers in those parts of Europe, Africa, or Asia with climates similar to the target regions in Australia. The success and failure of the introduced species in northern Au alia is being reviewed by Doube and Macqueen (unpubl.), who conclude hat the keys to success have been climate matching, habitat matching, and our ability to manipulate the species’ reproductive biology-for example, to control the diapause; release method and founder numbers are also thought to he important. Doube and Macqueen (unpubl.) relate African data on the relative abundances, habitat associations, and. reproductive biology of the twenty-two established species to their success in coastal central Queensland. Only seven species were abundant and widespread within a decade of their release. These

T

....

216

.

.

Chapter I 5

species are all relatively abundant in the Hluhluwe district of Natal, South Africa (Fig. 15. I), where they show a preference for grassveld but also occur 'on clay-loam soils in a pastoral environment (Table 15.5). The successful invaders are multivoltine, high-fecundity species. It seems likely that many Kselected species (Edwards 1988a) also have the potential to be successful invaders, but because of low numbers released in the field and low fecundity of these species, large populations would not appear for many years following their release. One such species, Copris elphenor, has become moderately abundant at one locality in Queensland ten years after it was released. In New Zealand, the introduced Mexican dung beetle, Copris incertus, was recorded as abundant in the early 1980s [Blank et al. 1983). nearly 30 years after its release in 1955-58 [Thomas 1960). There is a variety of reasons for the failure of other species to establish in Australia. Some species were difficult to rear in the laboratory because of larval or adult diapause, and adults of uncertain quality were released in low numbers. Other species are now known to be strongly associated with sandveld, bushveld, or the game reserve environment in Africa, and are considered to have failed to establish because their hasic ecological requirements were not met; they were released in grassland on clay-loam soils with only cattle present. Holm and Wallace (1987) suggest that the use of superphosphate fertilizer on dairy properties reduces the probability of dung beetle establishment. invasion of Communities .:

The indigenous dung beetles are gen.erally scarce in open pastures in Australia, hence the first introduced species encountered virtually no interspecilic competition. Some introduced species occupy niches complementary to those of the indigenous species and are thereby partially separated in space and time from them; this is the case with the species introduced to Western Australia (Section 15.5). On the other hand, many of the introduced species, especially the ones introduced into Queensland, share the same pattern of seasonal activity (Fig, 15.2), and at Rockhampton it is common to find five to six introduced species in the same dung pat, resulting in obvious and intense competition between the species. The degree to which such competition inhibits the establishment of additional species is not known. In April 1985, about fourteen thousand Sisyphus rubrur were released at the Rnckhampton study area, and the species'has successfully established a breeding population in the presence of substantial numbers of the six species already present. The fact that local assemblages of dung beetles in subtropical Africa often contain fifty or more species, most of which are rare (Chapter E), also suggests that competitive exclusion is unlikely to prevent establishment of further species at Rockhampton.

Y

TABLE15.5 Numerical abuadnnce and habilat associations of 22 dung bectlc specics in the Hluhluwc district of Natal. Soulh Africa, with their performancc following release in thc lieid in Queensland. Australia.

S/,ecicr

Lcngrli (nm)

Habirar in Afrira

=~lal

yenr~irsl

Cr

CI

Pa

Nutaber

II

YO

8 9 9

79

58 49 38 28 45 69

715 9,980 2.852

69 92 73 -

68 68 85 58 96 33 77

-

6.585 203 65

1968 1971 1968 1972 1973 I972 1976

8 15

I6

n

84

3,101

64

76

39

_ _ -

1,005

1976

16 19

98

I0

7

200

1976 1988

10

I2 98

66 5

15

U

1,283 2,186

I1

10 16 12 15 IY 18

9

I0 20 21

grassveld on clay and sandy soil ill 1983-84. * Thcsc rpccics are known tu be present in the

_ _ _ _ _ _ - 43 YI

88

43 2 63

*

1

*

64

14

50

23s 16

69

_ _ _ _ _ _ -

t

*

1972 1979 1973 1976 1977 1983 1979 1979 1973 1976 1977 1977

Nard region buc were not trapped in 1983-84.

278

I

Chapter 15

The Impact of Invaders The aims of introducing dung beetles to Australia were discussed in Section 15.3. The most obvious result of successful introductions has been the significantly increased level of dung dispersal (burial and shredding) wherever the new species have become established. Secondary responses to increased dung dispersal-reduced numbers of dung-breeding flies and increased pasture productivity-have been less self-evident. However, there is clear evidence from field and laboratory studies that dung beetle activity reduces survival of flies in dung pats (Bornemissza 1970b; Blume et al. 1973; Moon et al. 1980; Ridsdill-Smith 1981; Wallace and Tyndale-Biscoe 1983; Ridsdill-Smith et al. 1986; Doube, Giller, and Moola 1988). Furthermore, at times, intense dung beetle activity appears to have suppressed regionally the level of abundance of the bush fly (Hughes et al. 1978; Ridsdill-Smith and Matthiessen 1988) and the buffalo fly (Macqueen and Doube, unpubl.). Dung burial by beetles increases the growth of pasture grasses (Bornemissza 1970a; Macqueen and Beirne 197%; Fincher 1981), and beetle activity must improve pasture productivity to some extent. The effect of the introduced dung beetles on the overall composition of the dung insect fauna has not been assessed in detail, but many workers studying pasture communities have shown that dung pats protected from dung beetles produce many more dung-breeding flies than pats not so protected, and the numbers of predatory insects are also decreased in beetle-attackcg pats (Rotb and Macqueen, unpubl.; Doube and Macqueen, unpubl.). Whether the same is true of forest.and woodland habitats in Australia is not known,:nor has the effect of the iniroduced beetles on the indigenous species been examined in, detail. However, the introduced dung beetles now comprise a majoc component of many Australian dung insect communities, and in some regions (for example, in coastal Queensland and southwestern Australia), they have radically restructured the dung insect communities in open pastures.

PART THREE

Synthesis

THE ELEVEN CHAPTERS in Part 2 described regional dung beetle assemblages from northern temperate regions to tropical forests and savannas. There are obvious differences among the main biomes of the world in their beetle assemblages. Small species of dwellers (Aphodiinae) with high fecundity hut low competitive ability predominate at high latitudes, where population densities in relation to resource availability are generally low. In contrast, the larger and competitively superior tunnelers and rollers (Scarabaeidae), with relatively low to extremely low fecundity, are numerically and functionally dominant at low latitudes, where populations are often resource limited. This is a beautiful example of r-species being replaced by K-species along a gradient of increasing competition. Although it may be tw simplistic to ascribe the main pattern in dung beetle biogeography to competition, there is no doubt that competition has played a major role. In the next four chapters we attempt to provide a synthesis of four topics: spatial patterns, competition, resource partitioning, and species diversity in dung beetles. The order of the four chapters could he different, but we hegin with spatial patterns (Chapter 16) to emphasize habitat patchiness, the fundamental environmental context within which any consideration of dung beetle ecology must he based. (The next chapter, on competition, takes for granted s o m e findings on aggregated spatial distributions of beetles between droppings, rcviewed in Chapter 16.) In Chapter 16 we also examine albeit very briefly, regional population dynamics, and we review the data on dung beetle infroductions. Chapter 17 summarizes the existing evidence for competition in dung beetles and attempts to erect a conceptual framework about a competitive hierarchy. This chapter should help make sense of the variety of dung beetle communities described in Part 2 for different biomes and for different localities within biomes, varying in soil type, vegetation cover, mammalian species richness, and so on. We realize that the amount and kind of data presently available to formulate and test some of the ideas are very restricted, and while dealing with the most species-rich tropical communities, we are biased by our experience (YC) in West Africa. The situation is undoubtedly sorhewhat different, and perhaps more so than we now realize, in the more seasonal savannas in East Africa and in the subtropical savannas in southern Africa (Chapter 8). Still, it seems useful to look for broad generalizations, even if they need to be modified in the future; the alternative would be to succumb in the complexity of the dozens of special cases, and make endless qualifications. Chapter 18 reviews resource partitioning in dung beetles. We do not aim at an exhaustive summary of the information presented in Part 2. but have rather

282

'

Part3

restricted Chapter 18 to the main resource dimensions for dung beetles. We use as an example the community of dung beetles in West ikfrican savannas with more than one hundred coexisting species. Chapter 19 summarizes patterns in species richness in dung beetles, with increasing latitude, between grasslands and forests, and how species number varies with varying mammalian species richness. This chapter also relates species richness to the thrie processes discussed in the previouschaptcrs: competition, spatial aggregation, and resource partitioning. The final chapter, Chapter 20 is devoted to recording some concluding thoughts about areas in dung beetle ecology in which further research would be well rewarded.

C H A P T E R 16

Spatial Processes llkka Huilski and Yves Cartibefort

INSECTSLIVING I N patchy habitats have typically aggregated spatial distrihutions; some habitat (resource) patches have large numbers of individuals while others, though they appear to be similar, have only a few individuals (dung: below: Hanski 1987b; carrion: Kneidel 1985; Hanski 1987b. 1 9 8 7 ~ ;Ives 1988b: n~ushrooms:Sbormcks et al. 1984; Hanski 1 9 8 9 ~fallen ; fruits: Atkinson and Shorrocks 1984). Aggregated distributions in these insects is no surprise, as aggregated spatial distributions are also the rule in species living in nonpatchy habitats (Taylor et al. 1978), if any habitats are truly nonpatchy for insects. Optimal foraging theories (Krebs and Davies 1981; Stephens and Krebs 1986) predict that individuals using a patchy habitat should distribute themselves and their offspring in relation to the amount of resources in the patches. Parker's (1970, 1974, 1978) results on the yellow dung fly, Scatophaga srercoraria, is a putative example (but see Hanski 1980f; Curtsinger 1986), but generally the predictions of the optimal foraging theory are not supported by spatial distributions of insects in patchy habitats, most likely because the' insects do not have the time and the information-processing capacity to achieve the predicted distribution (Hanski 1990). One could expect that as habitat patchiness increases and the durational stability of individual patches decreases, the level of spatial aggregation in the insect populations further increases. Population ecologists are interested in aggregated spatial distributions for two different reasons. According to one view, by studying spatial distribution patterns we may learn something about the processes involved in the dynamics of populations and communities (Patil et al. 1971: Ord et al. 1980; Taylor 1986, and references therein). The other school of thought,, while ot deeming the causes of spatial distributions uninteresting, is more concern d with their' population-dynamic consequences (Elton 1949: Hassell and May 1973, 1985; May 1978; Hassell 1978; Lloyd and White 1980; Hanski 1981, 1987b; Atkinson and Shorrocks 1981; Chesson and Murdoch 1986; Sborrocks and Rosewell 1987; lves 1988b). Ultimately, it will be necessary to understand both the causes and the consequences of spatial distributions (e.g., Kareiva and Odell 1987), not least because they may be functionally related. The population-dynamic consequences of aggregated spatial distributions

l'

L1

2

284

‘

Chapter 16

Sparla1 Processes ” .

to competing species were outlined in Chapter I , where e , w a s argued that intraspecific spatial aggregation is often much greater than @erspecific aggregation’. The net effect of aggregated distributions therefore is, more often than not, increased intraspecific competition in relation to interspacific competition (Chapter 1). Such a shift in the strengths of the two types, of competition will generally facilitate coexistence of competitors. At this very general Icvcl, aggregation-mediated coexistence is comparable to coexistence based on rcsource partitioning (Ives 1988b), though the underlying mechanisms are fundamentally different. As with coexistence based on resource part/tioning, the question is about the degree of intraspecific aggregation, not of its presence or absence. How much aggregaiion is enough to allow coexistence has been cxplored in the theoretical papers by Atkinson and Shorrocks (1981), Hanski (1981), Ives and May (1985), and Ives (1988a,b, 1990). A single magical figure does not exist, because the outcome of competition is affected by other factors besides spatial distributions, including resource partitioning. Therefore we cannot resolve the role of spatial aggrsgations in the dynamics of competitors once and for all, and for all systems. Our aim here (Section 16. I ) is to docunient and compare the patterns of variance-covariance struaurc in some dung beetle assemblages. In addition, we will discuss the causes of aggregation indung beetles, which, though complex and largely unknown, are worthy of further study. Of the various approaches to the measurement of spatial aggregation (e.g., Southwood 1976; Pielou 1977), we have used two. To characterize the level of aggregation in a set of samples we use the following indices (Ives 1988b):

a measure of v,/x, - 1 intraspecific aggregation. J , =

(16.la)

XI

a measure of interspecific aggregation: C,,2 =

coy, 2

’

( I 6 . I b)

J ,measures the relative increase in the average number of conspecific individ-

uals that an individual of species 1 must face above the number of conspecifics it would meet if the distribution were random (Ives 1988b). C,,* has an analogous interpretation for interspecific aggregation. These measures of aggregatioxhave the advantage of being simple and having a straightforward ccological.interpretation, but they are also useful because they are directly related to the theory of competition in patchy habitats (Ives 1988a,h). Another widely used measure of aggregation is the slope 6 ofthe regression line of the logarithm of spatial variance against the logarithm of mean. which describes the change in variance with increasing mean, and may hc used both in intraspecific and interspecific comparisons. The parameter b has been ad-

I.

.

285

vocated as an iniponant attribute of species’ spatial behavior (Taylor 1961, 1986, and references therein; hut also see Anderson et al. 1982; Hanski 1987d; Downing 1986; Thorarinsson 1986). The value of b does not actually measure the level of aggregation as such, but it gives a rough measure of the degree of density dependence in the change of aggregation. If b equals 2, then no density-dependent processes liave affected the spatial distribution during thc time the average abundance has changed (Hanski 1987d; Anderson et al. 1982). On the other hand, the greater the role of (positively) densitydependent immigration to or emigration from habitat patches, the smaller the value of b, and it is always less than 2. The spatial scale at which aggregated distributions of individuals between resource patches is of importance is the scale o f a local population. individuals that disperse form a pool from which colonizers to patches are drawn (Chapter 1 ) . In Section 16.2 we turn to larger spatial scales. The distribution of species among “population sites” at the regional scale raises new and important questions: Are all species distributed among suitable sites in a similar fashion? How frequently is a species’ presence at a site dependent on inimigratioii from clscwherc, from larger and more permanent populations’! How oCten do local populations go cxtinct? Do species occur at an extinction-iniiiiierationcquilibrium at the regional scale, or is local equilibrium more typical? Our knowledge about dung beetles is far too scanty to attempt answering some of these questions. Still. it s e e m worth raising the issues here, if for no other reason than the dung beetles’ exceptional suitability for such study. In many temperate regions, most dung beetles are entirely or mostly dependent on cattle dung. Pastures define the suitable population sites, at wliich resource supply for dung beetles is easily quantified. Dispersal between the sites is easy 10 measure, at least on a relative scale, because dung beetles are easy to attract to baited traps. Finally, spatial distributions of domestic mammals have changed dramatically .in many countries, and continue 10 do so, providing interesting opportunities lo study nictapopulation dynamics-the dynamics in a set of local populations connected by dispersal-in a changing environment. In Section 16.3 we move to a still larger spatial scale, and to a different type of problem. Dozens of species of dung beetles have been introduced, intentionally or otherwise, into islands and continents where they did not occur before. Some of the chapters in Part 2 have given examples of such introductions and presented analyses of special cases (see particularly Chipter L5 for the large-scale introduction of dung beetles to Australia). Scction 16.3 provides a’brief summary of dung beetle introductions. To where have dung beetles been introduced, and where from? What has been the success .of introductions? ‘What have been the consequences to native species? There is an increasing ecological interest in species introductions (e.g., Crawley 1987). lo which dung bectle introductions add new data. It is also likely that more species of dung beetles will be introduced in the future to tackle the two major

. ..

2n6

.

c h a p m 16

management problems that exist in this field, the accumulation of cattle dung in pastures where the native beetles are unable to efficiently bury the dung of the introduced cattle; and the often large populations of dung-breeding flies, which have ample opportunities to increase to a pest level ih the absence of competitors and effective natural enemies. SPATIAL AGGREGATION ACROSS RESOURCEPATCHES

16.1,

Patterns of Intraspecific Aggregation Let us start with two extreme examples. Macqueen and Doube (pers. comm.) trapped beetles in an Australian pasture with pitfalls baited with pats of homogenized cattle dung. The traps were located either in a grid with 5 rn intervals, or along a transect line with 20 m intervals. The five'intmduced species4eosisyphus spinipes, Euoniticellus'intermcdius, Liatongus mililaris, Digitonthophagus gazella, and Onthophagus sagitrurius-were the only abundant species in the pasture, and all had J values less than 0.67, not significantly different from zero. In other words, the-distributionsof these beetles in the traps were random. Doube in Chapter 8 refers to another study conducted in southern Africa with essentially the same result, th?t is, there was no aggregation of beetles among cattle pats located within short distances from each other (in this case, .however, the average densities were so low that most distributions would appear random). Kohlmann in Chapter I describes a case of the opposite extreme, where one species (Ateuchus carolinae) occurred in large numbers in some dung pats but was entirely absent in other, apparently similar, pats. Several other species, assumed to be competitively inferior to A. carolinac, were present in varying numbers in the pats in which A. carolinae was absent. Such an extreme pattern is unusual (we do not know of another example), and the reilsons for the doninant species to concentrate in only a subset of dung pats remain unknown (Chapter 7). As this study was based on sampling naturally occurring dung pats, it is possible that some differences between the pats contributed to the observed pattern, even if similar-looking pats were collected. The usual pattern of spatial distribution in dung beetles is between these two extremes. Beetles are generally not randomly distributed even among apparently SCmilar droppings, yet the degree of aggregation is less than in Kohlmann's example, and the abundant species typically occur in varying numbers in all or most pats. One factor that undoubtedly affects the level of aggregation is the average distance between the traps or dung pats, though short distances, as in Doube's studies, do not necessarily lead to random distributions. Hanski (1979, 1980b), working in southern England, found large variation in the numbers of

Spalhl Proccsscs

.

287

beetles ainong traps located only > I O in Froni each other and baited with homogenized cattle dung. Two factors in this study were different than in Doube's: Doube's Australian and African studies were conducted in larger, inore open areas; and the dung beetles in England (Aphodiinae) are a much smaller species than those in Australia and Africa (Scarabaeidae). The latter point is related to the continuum from the lottery dynamics to the variancecovariance dynamics described in Chapter 1: the smaller the species in relation to the size of the resource patch, the more toward the variance-covariance end of the continuum its dynamics are expected to he located (Chapter 1). Camhefort's extensive material from West Africa (Chapter 9) provides the opportunity to examine intraspecific aggregation in a very species-rich assemblage and to compare the degree of aggregation among species with different foraging behaviors. In Chapter 9 Cambefort analyzed spatial distributions of beetles among similar-looking, naturally occurring cattle pats, and found the species to be more or less aggregated (Table 9.7). Three factors were related to the level of aggregation: aggregation decreased with the size and average abundance of the species, and cattle dung specialists were significantly less aggregated than generalist species. Here we complement these analyses with parameter estimates of the power function relationship between spatial variance and mean abundance (an interspecific regression). We can ask the question: Does the increase in variance with increasing mean abundance vary among different sorts of beetles? Table 16.I gives the results for six sets of cattle pats sampled at different times of the year in the same habitat. Two kinds of comparisons can be made: cattle dung specialists may he compared with the generalists, and species in four tribcs representing different ncsting behaviors may be comparcd with one another. In the first comparison, the'specialist species tend to have smaller values of b than the generalists (F = 4.84,P<0.05; differences in mean abundance have no significant effect), suggesting that density-dependent immigration to andlor emigration from droppings is more cliaracteristic for the specialists than for the generalists. Thus specialist species seem to ,be more sensitive than the.generalists to intraspecific interactions in the use Of the resource to which they have become specialized. The comparison of the four tribes gives an even more striking result. We compared the b values in Table 16.1 using analysis of covariancc,(with the logarithm of mean abundance as a covariate and'the tribe as the classifying factor. Both the mean and the tribe had highly significant effects (mean: F = 6.55, P<0.019; tribe:'F = 11.38, Pi0.0002). The higher the average abundance, the smaller the slope b, which is not unexpected, because density-dependent processes may he expected to occur especially in the most abundant species (see also Table 9.7). Sisyphini, the small diurnal rollers, had the highest slopes, while Coprini, large and mostly nocturnal tunnelers, tended to have the lowest slopes (Table 16.1). This result suggests that the large Coprini in-

~

,,

288

.

Spetinl Pruccsscs

Chapter16

TnnLe 16.1

of the power function relationship betwecn the VJriJnCC and LhC lncal of

parameter dung b e l l e s in cattle dung pats in West African savanna (Ivory COast, Chapler 9). Species Cattle dung specialists

DaruSrr

1

2 3 4

5 6 Gcncralisls

1

2 3 4 5 6

Sisyphini (rollen)

1 2 3 4~

5. 6

Coprini (large tunnelers)

1 2 -. 3 4 5 6

Oniticellini (small tunnelers)

I 2 3 4 5

~

6

a

1.

$

Mcm

Vw

0.60 , 1.62 0.46 (1.65 0.45 1.50 0.59 1.63 0.65 1.68 0 . 4 9 , 1.52

0.98 0.94 0.92 0.98 0.95 0.96

5.82 6.28 3.63 3.93 3.17 1.27

16x2 174.4 79.6 164.3

1.04

1.71 1.76 1.52 1.76 1.73 1.76

0.99 0.97 0.96 0.97 0.98 U.97

0.47 0.42 0.70 1.01 0.42 1.15

2.39 2.68 1.63 1.96 2.68 2.04

0.93 0.96

0.46

1.62

-0.28 0.41 0.50 0.36

0.77 1.51 1.39 1.29

0.76 0.77 0.75' 0.89 0.SO

-0.04 0.85

0.63 0.60 0.56' 0.68 0.66

o 72

1.65 1.68 1.58 1.75 1.57 1.77

1)

20

91.1

19 19 22 20

18.0

20

6.94 1.55 0.73 2.13 1.32 1.31

582.4 33.4 5.5 333.6 72.0 65.3

15 16

59.6 41.2 13.8 478.9 41.2 18.4

4

0.99 0.96 0.99

2.96 2.18 1.56 4.06 2.18 0.74

0.98 0.87 0.61 0.99 0.96 0.98

1.07 0.75 0.43 2.72 0.67 0.43

5.7 0.6 3.7 22.1 3.0

5

0.98 0.95

11.35 11.61 6.79 5.95 6.70 2 88

L.99

0.98 0.98 0.96 0.96

20 30 36 21) 4

3 5 4

5

4 5 . 5 .'

7

5

1.1

' I 489.9 362.4 ' 9 8 172.3 395.0 8 199.5 7 108 4 8 I

':

.

.

289

terfere with one another and thus become distributed more evenly among the dung pats than the small tunnelers, Onthophagini and Oniticeilini, or the small rollers, Sisyphini. Observational (Kingston and Coe 1977) and experimental results (Giller and Doube 1989) on large tunnelers indicate that one pair of beetles (Heliocopris) or a small number of beetles (Catharsius, Copris) may use all or most of the resource in one dung pat. Relatively low abundance of Coprini is undoubtedly a consequence of their large size and competition. Unfortunately, it is not possible to compare large rollers (Gymnopleurini and Scanbaeini) with Coprini, because in the Ivory Coast the former tend to use mostly omnivore dung (Chapter 9). The values of the J index (Table 9.7) suggested that the size of the beetle, not the tribe, significantly affects aggregation. As thc size distributions of beetles iii the four tribes arc different, it is not possible, with these data, to sort out the effects of size and tribe. Pafferlisof Inferspeci/ic !Aggregafiofi

Interspecific aggregation measures the degree of covariatiou in the numbers of two species across a set of habitat patches. As for intraspecific aggregation, the studies by Macqueen and Doube (pew comm.) and Kohlmann (Chapter 7 ) contribute two special cases. The five species in Australia that were not intraspecifically aggregated did not show any interspecific aggregation either (all C values less than 0.44), while Kohlmann's species represent another unusual case, in which the dominant A . carolifme versus the other species had significantly negatively correlated distributions (Fig. 7.5). In this case it is possible that the dominant A . carolinae somehow prevented other species from immigrating to, or forced them to emigrate from, the pats where it was abundant. Yasuda (1987) has found that the rate of emigration of Liutongus phonaeoides is less dependent on the numbers of conspecifics in a dung pat than on the numbers of another species, Aphodius horoldianus. The usual pattern of interspecific aggregation is not negative association but some-though usually far from complete-positive association between species. An important point is that intraspecific aggregation does not necessarily lead to interspecific aggregation. Hanski (1986) showed that nine coexisting Aphodius species had entirely uncorrelated distributions even if all the species were intraspecifically aggregated (Fig. 5.2).

Causes of Spatial Aggregation 'i

0.79

1.71

0 98

1.49

90 I

27

Aggregated distributions of insects among resource patches located in the

same habitat have two possible causes, heterogeneity among the resource

patches themselves and the movement behavior of insects. It is obvious to anyone who has observed any insect species in the field that habitat quality and resource quantity vary from one place (patch) to another, and such heter-

'

'

290

'

Chapter 16

ogeneity undoubtedly affects the spatial distribution of species. Species with similar resource requirements are expected to he similarly affected, hence heterogeneity among resource patches is expected to increase both intraspecific and interspecific aggregation in a guild of similar species. However, while considering resource patches such as dung pats produced by the vdme species of mammal in one place at one time, it seems unreasonable to assume that differences in the quality of physically similar-looking droppings would he so significant that they alone would suffice to explain the observed spatial distributions of beetles. In any case, such differences must he inconsequential to the breeding success of dung beetles. Now we turn from the environment to the species living in the environment. The more similar two species are in their morphology, behavior, and ecology, the more similar should he their patterns of colonization of a set of habitat patches, because they are similarly affected by the deterministic factors influencing colonization. In agreement with this argument, Hanski (1987b; see also Fig. 5.3) found that interspecific aggregation was significantly higher in guilds of dung-inhabiting beetles with similar biologies than in a guild consisting of biologically less similar species. Cambefort's (Chapter 9) results on West Alrican dung beetles point to the same conclusion: interspecific aggregation was greater in diurnal-diurnal and nocturnal-nocturnal than in diurnal-nocturnal pairs of species; interspecific aggregation tended to be higher in species pairs of similar size than in pairs consisting of a small and a large species; and interspecific aggregation tended to be higher in two species from the same tribe than in two species from different tribes. Diel activity, size, and tribe will affect the prohab es of detecting and colonizing dung pats that are simultaneously available to beetles. For example, short-term variation in weather may change the environment (e.g., direction of wind) for beetles active at different times of the day and colonizing the same set of droppings. Beetles belonging to different tribes and of different size are likely to have many differences in their foraging behavior, tending to decrease interspecific aggregation. In this perspective, lack of interspecific aggregation may be a consequence of all kinds of differences between species, not only those that are directly related to resource use. The more similar two species are in their ecology, the greater not only the overlap in their resource use,; but also the greater their spatial correlation across similar resource patches. I So f5we have assumed that intraspecific aggregation is due to heterogeneity &ong resource patches, differences in the foraging behavior of different species, or to stochasticity in the colonization of patches by insects. Another candidate for intraspecific aggregation is pheromone communication between individuals of the same species. The first convincing demonstration ofpheromane communication in dung beetles was due to Tribe (1975, 1976), working on the large African roller, Kheper nigroaeneus. In this species, both sexes have tegumentary glands and hairs used for secreting and disseminating the

Spatial Pmccsscs

~

'

2Y I

chemical, though only the male has been'observed to adopt a special stance during pheromone emission, apparently to facilitate the dispersion of the chemical by wind (Neuhaus 1983). The product of the tegumentary glands emerges from minute pores as hollow, layered tubules impregnated with very small quantities of substances in which hexadecanoic acid, 2,6-dimethyl-2heptenoic acid, and nerolidol are major components (Burger et al. 1983). The presence of similar morphological structures in many other dung beetles (Pluot-Sigwalt 1982, 1984, 1986, 1988; Houston 1986) suggests that pheromone secretion and communication may be common in these beetles, though in most cases, for example in Onrhophagus binodis, the pheromones are most likely to he used for close-range species recognition and sexual attraction than for long-range attraction (Ridsdill-Smith 1990). A particular stance during pheromone emission similar to that described for K . nigroueiteus has been observed in Carreta, another African roller (Tribe 1976), as well as in the Neotropical roller Catirhun cyatzellus (Bellts and Favila 1984). In the latter species, a chemical that is spread on the dung ball appears to have a repelling function against Crrlliphoru flies, potential competitors. In summary, chemical communication with pheromones probably facilitates closc-range individual, sex, and species recognition in many species of dung beetles, and chemicals may be used to mark balls, burrows, nests, and so on, but it is as yet unclear to what extent pheromone communication may affect the level of aggregation of beetles in dung pats. Our guess is that pheromones are not important in this respect, especially not in the species that occur in high densities. Cunseyuencrs of

Aggregnrioii

I

Our interest in spatial aggregation of dung beetles has been stimulated by the possibility that aggregated distributions facilitate coexistence of competitors (Chapter I ) . Ives (1990) gives the following general result about the minimum effect of aggregation on coexistence of competitors. Let a. and Po be the threshold values of larval competition coefficients above which coexistence is impossible in randomly distributed species, and denote by a, and Pa the corresponding values when species are aggregated. Ives (1990) shows that the minirnuni effect of aggregation on coexistence is given by

+ 1)(J2+

I)KC,.2+ 1 ) 2 ,

(16.2) where J , , J2 and C 8 , 2are defined by Eqs. (16.1). To take an example, given the average values of J and C in Table 9.8, aggregation will allow two species to coexist even if their competition coefficients were six times greater than the maximum possible without aggregation. The interpretation of this result is straightforward for Aplwdius, whose larvae move freely within a resource patch and interact with one another. In the case of tunnelers and rollers, the a:,P.>a,,Pa(J,

,

292

,

.

Spelkal P ~ c c s s c s

Chaptcr 16

crucial interactions occur earlier, among adult beetles competing for the resource to provision their nests (Chapter 3). Nonetheless, the basic point remains essentially the same: aggregated interactions among competing individuals allow coexistence of competitors with greater competition coefficients than would be possible without aggregation.’ The current theory deals with only two species, while in real dung beetle communities dozens of species may be using the same resource. It seems intuitively clear that the two-species model extends to many species, but. where is the limit to guild size if coexistence is solely based on intraspecifically aggregated spatial distributions? Shorrocks and Rosewell (1986, 1988) have made a start in answering this question, and they reach the conclusion that in fungivorous Drosophila intraspecificdlly aggregated distributions would allow some five species to coexist. The expected number of coexisting species naturally dcpends on many factors, most notably on the degree of competition between the species and the degree of in!raspecific and interspecific aggregation; the predicted guild size of five was based on empirical results on these and other parameters in fungivorous Drosophila (Shorrocks and Kosewell 1986; see S t a l s et al. 1989, for another guild of fungivorous flies). In dung beetle assemblages with.dozens of species, there are typically some diiferences in species’ selection of different dung type. soil type, and vegetation cover; in their diel activity, seasonality, and nesting behavior; and in their size and its correlates (Chapter 18). Not all these differences entirely eliminate competition between pairs of species, but they have a potentially important effect in facilitating coexistence. Unfortunately, because of the multitude of species in many dung beetle assemblages with various kinds of ecological differences, it is not generally possible to delineate guilds of like species; competition and other forms of interspecific interactions are diffuse. Examplcs of sets of species with no known ecological differences include Pruogoderus lunism, P. tersidorsis, and P. yuadriruber in South Africa (Doube 1987) and several pairs of Onthophugus in the forests in West Africa (Chapter 1 1 ) . In Chapter 1 we described two types of dynamics in species competing for nonrenewable resources in patchy environments: the lottery and the variancecovariance dynamics. Here we showed that dung beetles generally exhibit aggregated spatial distributions, but also that different types of beetles show consistent differences in the level of intraspecific aggregation. Species that are large in relation to the size of resource patches are expected to obey the lottery dynam‘ics and to show less intraspecific aggregation than small species (Chapter l), which indeed is the pattern found in dung beetles (Fig. 16.1 and analysis of Table 16.1 above). Especially in the ecology of dung beetle assemblages consisting of small species, intraspecific and interspecific aggregation are critical ingredients, though this is only one factor among many factors that need to be considered for a comprehensive understanding of patterns of coexistence.

. .. *

%

.

293

I

.

Lu

2 Q

4 6 LOG OF WEIGHT

a

0

Fig. 16. I, Thc relalionship bctwecn intraspccilic uggrcgalion and llic 1og;~rilImof bcctlc wcight in lunnclcrs iii Wcs1 Aliiun (sanic diih ns iii 'Table 9.X).Aggrcfaliw~011 ihc vcnicill axis is measured by log ( I + I ) . The slope of thc icgrcssioii liiic dilfcrs highly significantly from zero (f = 5.33; P
16.2. METAPOPULATION DYNAMICS Neighboring regions located only a few kilometers apart may have strikingly different communities of dung beetles. Chapter 6 gives one example from southern Europe, where two closely situated sites had little overlap in species composition. In this case there. were differences in soil type due to different parent rocks, probably eitplaining much of the observed difference in species composition (Chapter 6). Restricting our attention to regions without apparent climatic, edaphic, or other environmental differences of significance to dung beetles, we may ask about the patterns of occurrence of species at sets of similar sites. Following Levins (1969, 1970), population ecologists use the term “metapopulation” to describe systems of local population connected by dispersal. What is the role of metapopulation dynamics in dungsbeetles? The metapopulation scale is not very important for the locally abundant and regionally common species, which are present at all sites most of the time and are affected mostly by processes within populations. The metapopulation scale is important for the less cominon species, with local populations occasionally going extinct and new ones being established by immigration from other p o p ulations. A metapopulation may persist only if the rate of establishment of new local populations exceeds the rate of local extinctions when the number ..

,

I.

294

‘

Spatial Proccsses

Chapter 16

of local populations is small (Levins 1969). How correlated the extinction events are across populations also makes a difference (Quinn and Hastings 1987; Gilpin 1990). Species that have a high dispersal rate and uncorrelatcd local dynamics should have more persistent metapopulations than species with a low rate of dispersal and highly correlated local dynamics (Hanski 1989b).

Dispersal The flight-oogenesis hypothesis (Johnson 1969) suggests that females, before commencing reproduction, enter a distinct phase of dispersal. Although valid for some insect species, the flight-oogenesis hypothesis does not account for dispersal behavior in dung beetles (Hanski 1979). Instead of a conspicuous dispersal period, newly emerged dung beetles enter a shorter or longer period of maturation feeding (Chapter 3). Bec‘Juse the consumption of resources by dung beetles does not affect resource renewa!, there are no reasons for immature beetles to move elsewhere to feed before reproduction. The species of dung beetles with the most highly evolved brecding bchavior remain in the same nest caring for their offspring during the entire brecding season (Halffter and Edmonds 1982). Such species probably have a low dispersal rate. In contrast, other species need.to fly between egglaying. Aphodius repsesents this latter type, and it is noteworthy that mature females are relatively more frequent among long-distance dispersers than immature bectlcs (Hanski 1980d). Mature females may benefit of movements in two ways: by depositing their eggs in several dung pats in which the success of their offspring varies independently (“spreading of the risk”), and by possibly locating an area where the density of the species is low. In Aphodius i n southern England, between-pasture variance in numbers decreased during the adult Bight season in most species, and the species with the highest frequency of long-distance movements tended to have the smallest between-pasture variance in numbers (Hanski 1979, 1986). Such observations suggest that the rate of dispersal between populations is high. The maximum rates of dispersal can he examined in species that have been introduced into areas where they did not occur before. Table .16.2 gives estimates for two medium-sized tunnelers, Digitonrhophagus gazella and Onthophagus raurus. The observed dispersal rates are surprisingly similar and very high, from 50 to 130 km per year. These values may not be representative for most dungbeetles, as.,Onthophagini seem to be exceptionally good dispersers (Section 16.3). It is also possible that the estimates in Table 16.2 are inflated by human transport of beetles on cattle trucks, for instance. In summary, large, low-fecundity dung beetles are expected to have low rates of dispersal, but many small species may have very high rates of dispersal. Data on the rate of dispersal of the large species, especially, are badly needed.

’

295

TABLE 16.2 Rate vf dispersal of introduced dung beetles from the initial point

S,,Ki‘,.?

Locoliry

D~fiilo,~lh~~~hn pxella jirr,s

Difiiro,rrlro~~ku~,rs guiellu O~rlhr,pI,uga.~ Iu,,Ic,s

Australia North Americu North America

of introduction.

Rare of Spread. Psilyr

Ref

50-80 (12) 58 (12) 129( 7)

2 3

Refemires: I.Scyinour(1980): 2 , Chapter?;

N o w T h C ligure

ill

1

~~~~~

3, Finchcretal. (1983). pilrcnlhcscr give the nuniber of yevn over which the rile hm been EBICU-

lUtCd.

Exfiricrioit Extinction of local populations of insects is notoriously difficult to prove. The task is easier when the time span of observations is increased. Pleistocene cxtinctions of dung bcctles can be attributed to varying climates and a dramatically declined resource supply (Chapter 5). Regional extinctions of species during the past 100 years have been explained by reduced availability of resources .(Chapters 5, 6 , 9 , and 11). In some cases the key may be the reduced availability of resources in microenvironments particularly favorable for the species-for example, the right kind of dung on.the right kind of soil. Merapopulation persistence depends on the average rate of local extinctions and on the degree of correlation of local extinction events. Hanski (1979, * 1986) calculated that if the average density ofAphodius in pastures in England wcrc lcss than 0.5 bcctlcs pcr cilttlc pat, niany Ceinales would remain unfertilized, and hence the population growth rate would be decreased (the Allee effect). The bimodal distributions of log abundances that are frequently observed in dung beetles (Fig. 16.2) may result from such a critical density in local populations; many or most of the very rare species are likely to be represented by dispersers from elsewhere (Chapter 5 presents evidence supporting this hypothesis for temperate Aphodius). Bimodal abundance distributions are uncommon in the literature (Williams 1964). but this may only reflect the difficulties of sampling most communities of insects as exhaustively as one may sample dung beetle communities. There are little data to examine the degree of correlation in local dyaamics, and cvcn lcss in local extinction events. However, one may guess that the large tropical dung beetles whose emergence is critically dependent on sufficient rainfall (Chapters 8 and 9 and references therein) have highly correlated dynamics over large areas. These species are also expected to have low dispersal rates (see above), which is a combination not favorable for metapopulation persistence. To make things worse, many of the largest dung beetles, such as Hdiocopris, Hererorlitis, and Kheper, are more or less dependent on ‘\

296

'

Spatial Proccsscs

Cliilpter 16

.

297

€3

LL

0

"

U

LOG ABUNDANCE

0

LOG ABUNDANCE

D MONM

MONTH

Uo LOG ABUNDANCE

LOG ABUNDANCE

Fig. 16.2. Four species abundance diitributions in local conwunilics d dung bcctlca. Localttjes: A , tropical savanna ( U k s t Africa, Chaplcr 9); B. nnrlb Iclnperatc ~ 1 B s t U r C (England. Chapter 5); C , r n ~ i n apaslurc ~ (thc Alps, Chaptcr 14); I). Irupical I l l c ~ l (Barm Colorado Island, Panama, Chapter 12). Notc the tcndcncy toward hinlodnlily ill these dislributions. elephant dung, which is a declining resource type in many areas. And linally, the game reserves in Africa, where most elephants now occur, are becolnilig increasingly isolated habitat islands, further decreasing the cllances Of mCt:tpopulation survival. In other dung beetles, local populations haye less correlated dyoatnics t h 1 l is probably the case with large African rollers and tunnelers. Fig. 16.3 shows that there is substantial between-population variation in the seasonal Ilight irctivity of temperate Aphodius. Since breeding success in insects depcllds n~uch on weather conditions, the kinds of seasonal differences i n adult lligbt activity shown ip Fig. 16.3 are bound to lead to substantial variation in brcedingWCESS and hence in local dynamics between populations. To summarize these considerations on dispersal and local.extit~ctionin dung beetles, we propose the working hypothesis that the large, p - f e c u n d i t y species living in seasonal environments in thc tropics Iravc a low dispersal rate and highly conelated local dynamics, while many other Species, lor eXaVie, ternperate ~ ~ / ~have ~ thed opposite i ~ ~characteristics. ~ , making their IiiCtapopuliitions m,ore persistent.

16.3. DUNGBEETLElNTRODUCTloNS Over long periods of time, species may greatly expand their geographical ranges. According IO Ivlatthews (1972), the present fauna or 260 species oI Oiirhophngnr in Australia originates froin at least thirty-four independent invasions of tliaf continent. Long-distance dispersal of dung bectlcs i s likely to be facilitated by man, Icading to accidental introductions of specics to new regions and continents. Paulian (1961) suggests that Digitorirhophagus gozelln was accidentally introduced into Madagascar with cattle at same point between 2,000 and 300 years BP (this very vagile species is also one of the niost successfully introduced species when the introductions are intentional; see bclow). Table 5.2 s u i i n i ~ a r i ~ the e ~accidcntal introductions oFAp/iodiiis tu North Anierica, while Table 16.3 gives such inlorniatioo for Scarabacidac. Except for tlic spread of t;irofiilice/hs crtbiciisis frotu Cuba to Florida, all these species involve Onthuphagini, which is another testimony to the cxceptionnlly g o d powers of dispersal in this cosiriopolitan tribe with more tlian 2000 species (sec also Table 4. I and Chapter I O for the occurrencc of Oiilhopilngus on sniall isliinds in Sauth-E;ist Asia). During the past decades, about one hundred species of dung beetles have been intentionally introduced into Australia, New Caledoiria, Nor-th Anierica, P u c m Rico, arid Hawaii. 01 Ihesc, about forty spccics have become estahlishcd so far (Table 16.4). The two aims of dung beetle introductions have been improverncnt of dung renioval from and enhanccment oF,nutrient cycling i n pastures, and dccrcilsc i n thc ai~ioiintof resuurccs availablc to dung-brccd-

298

Spatial Processes

. Chapter 16

TABLE16.3

Accidental introductions of Scanbacidac dung bcetlcs.

Species

lnrroduced from

Digironthophagus gazella

Tropical Africa Cuba Salvador West Africa

Oniricellus cubiensis Onrhophagus batesi Onlhophagus biruberculatw Onthophagus cervus Onrhophagus consenfaneus Onrhophagus depressus

India Australia South Africa

Onthophagus nuchicornis

Europe

Onrhophagus ruurus Onrhophagus U I I ~ ~ ~ S C ~ U I K S

Europe India

Ref

1,rrroduccd 1 0 Madagascar

I

Florida Maninique Maninique

2

Mauritius New Caledonia Madagascar

Mauritius

USA Australia N Amcrica USA, Mauritius

3 3 4

5

I 4 6 7 6 8 4

References: 1, Paulian (1960); 2, Woodruff (1973); 3 . Mauhcws (1966): 4. Paulian (1961); 5 . Gutierrer e l al. (1988);6, Howden and Canwright (1963); 7, Mallhews (1972); 8 . Finchcr and WOOdNff (1975).

.

299

ductions of dung beetles anywhere. The current consensus is that the introduced dung beetles have made a niajor contribution toward solving the prob,' lem of dung accumulation, hut the success in~controllingthe populations of dung-breeding flies h4s been more variable. In Australia, dung beetles have not made much impact on the populations of the buffalo fly, but large populations of the introduced Onthophagus binodis have essentially halved the bush fly season (Chapter 15; Ridsdill-Smith and Matthiessen 1988). Introductions to other regions have given similar results (Patterson and Rutz 1986). Solving the fly problem would apparently require a nearly complete and rapid removal of dung (Palmer and Bay 1984; Hanski 1987a). which is not likely to occur except underJxceptiona1 circumstances (Chapters 8 , 9 , 15, 17). Following the early suggestions by Campbell (1938) and Bornemissza (1968, 1976). more attention has been given recently to the ideas of introducing some of the predators and parasitoids of dung-breeding flies instead of dung beetles, the competitors (Wallace and Holm 1983; several chapters in"Patterson and Rutz 1986). Two apparently successful cases are the introduction of a parasitic wasp to Mauritius, where it caused a drastic decline in the abundance of the dung-breeding stable fly (Greathead and Monty 1982), and the control in Fiji of dung-breeding flies by Hisrer chinemis (Legner 1986). Other experiences have not been equally encouraging, however (Patterson and Rut2 1986).

TABLE 16.4

intentional introductions of dung beetles.

,

Inrroducedto Austrdba

Inaodnced from

S

Africa

EWOW

Tropical Asia ~

New Caledonia

S Africa

N America

Europe S. Africa .....-

N,,,

Years

NCAs

Ref

44

1

1968-82 1972-82 1968

16 5 I

I I

4

1978

3

2

1 3

1982 1972-77

3

7

3 3

10

I

I

I

3 3

192a-30

0

3

1906-83

10

3

Asia

1

S America

I

1978-81 1981

Puerto Rico

various

8

Hawaii

Various

26

Reference?; I , Chapter I5;2, Gutierrezelal. (1988);3, Fincher (1986). N ~ r e : N , ~ ;the , i %n u m k o f species introduced. while the nexl columns give the y c ; m o l inlruduction and the number of species known 10 have become eslablished, N,,.

ing flies, which in many areas have become a serious nuisance to domestic animals and even to humans (Waterhouse 1974; Bornemissza 1979; Doube 1986). It is not our purpose here to try to assess how successful the introductions have been in achieving these aims. Chapter 15 reviews the experiences from the Australian introductions, which have been the most extensive inlro-

From Where Have Dung Beetles Been Irnroduced, and to Where? In the geographical regions where large herbivorous mammals are abundant, they are trailed by large numbers of specialized dung beetles, searching for droppings with some particular characteristics, for example, large size and a high carbohydratelnitrogen ratio. In contrast, in regions lacking indigenous large herbivorous mammals, the local dung beetle fauna is unlikely to have many species that use their excrements efficiently. The pioneering idea of Bornemissza (1960) was to introduce dung beetles into Australia from areas with similar climates and where cattle, or closely allied large herbivorous ungulates, occur naturally. Nowadays, such areas are primarily Africa and, to a lesser extent, tropical Asia, but also Europe and the Middle East (temperate and Mediterhnean climates). The areas where cattle have been intr duced but which lack a dung beetle fauna that is adapted to use the droppings of large herbivores are Australia and many oceanic islands, as well as parts of the United States (Table 16.4).

P

F o u r Very Successful Species

7

Fora dung beetle to he considered for introductions, it must have two basic characteristics: it must be efficient in burying cattle dung, and it must have the potential to become numerous and widespread. In the beginning of the Austra-

.. .

300

'

Chapter 16

lian introduction program these requirements were clearly understood, but the role of habitat specificity in particular was underestimated, and the biology of beetles in their native counuies was poorly known. As many as fifty-five dung beetle species were shipped to Australia, and forty-one species were relcesed in the field (Table 16.4 and Chapter 15). Of these, twenty-two species have become established, hut only five to seven species are presently really common and widespread in (North) Australia, though others are multiplying rapidly (B. M. Doube, pers. comm.). For closer scrutiny we have selected four species of dung beetles. which have been introduced frequently and are considered to be among the most successful ones in terms of burying large quantities of dung. These species are Ncosisyphus spbtipes (Sisyphini), Onitis alcxis (Onitini), Euoniticclllrs infermedius (Oniticellini), and Digitonfhophagus gazella (Onthophagini) (Fig. 16.4). The key ecological characteristics of these species are given in Table 16.5. One's first impression is that the four species comprise a surprisingly diverse assemblage. They belong to four different tribes of dung beetles. Though most of them are widespread, N . spinipes has a relatively small geographical range in southern Africa. The four species include two small tunnclTABLE16.5

Ecological characteristics of four frequenrly.and successfully intmduccd spccics of

dung beetles.

Species Nurive biome and geogruphicd disrriburion

,.

L

R

T

N

D

A

"

Digironrlzuphngus gurelfa Tropical savanna Africa, Asia

!I

15

30

ST

N

607

YO

Euoriiricelfus inrermedius

9

t2

28

ST

V

45

120

16

15

60

LT

N

60

130

9

I

52

SR

D

100

44

Tropical savanna Africa Oniris rrlexjs

Tropical-subtrapicnl grasslands Africa, Medilerrancanregion

Neosisyphus spinipes

~.

I

Trooical savanna Southern Africa Nores: The following data are given: L, length in mm, R, approximate geugrdphiczl range in million^ of squxe kilometers; T. developmental time in days from egg Io d u l l : N I lypc 01dung katle I~~, L . large: ~". S. small: R. roller, T, lunneler): D,diel vclivily (D. diurnal: N. nocturnal): A. average longevity io days: F, mean lifetime fecundity under lkburslury a m d i l i w s ,

t 302

’

Spalinl Proccsscs

Chapter 16

ers, one (relatively) large iunneler, and one small roller: the large rollers and very large tunnelers are missing. Two species are diurnal while the other two are nocturnal. Clearly, there is not a single type of dung beetle that has been successfully introduced. Nonetheless, there are also important similarities among the successful invaders. All the species are of medium size, from 9 to 16 mm in length, have relatively short times of immature development, from 28 to 60 days, and have high fecundity, from 50 to 130 eggs per female. A closer look at the Australian introductions (Table 15.5) confirms that small and medium-sized species are the ones that have been introduced successfully (ANOVA, PCO. 10; comparing the lengths of the “abundant and widespread species” with the others in Table 15.5). Among the twenty-two species in Table 15.5, the successful species appear to be more abundant than the others in the locality of origin in South Africa (ANOVA, P
Effect of Introduced Species on Native Species Not many observations have been made about the impact of introduced specics on native dung beetles. In some cases not much interaction is expected to occur as the exotic species are introduced into communities that entirely or virtually lack any similar species. An example is the winter rainfall regions in Australia (Chapter 15), where the native species have similar seasonality to that observed in the Mediterranean region: beetles are active in spring and autumn,~whenthe soil’is moist and temperatures are neither too high nor too low. In contrast, the introduced species Onrhophagus binodis and Euoniticelluspallipes are active throughout the dry summer and autumn months ( C h a p ter 15). Sequential introductions of foreign dung beetles in the summer rainfall regions in Australia provide some examples in which previously established

303

species have greatly decreased in abundance when more species were added. Perhaps the best example is Onthophagus sagittarius, which was abundant at a locality in Rockhampton in 1973 to 1979, when the only other abundant species was the introduced Digitonrhophagus garelfa (Table 15.2). In the early 198Os, three other introduced species became very abundant (L. militaris, E . intermedius, and N . spittipes). and the concurrent decline in the density of0. sagiftar-ius to about 10% ofits abundance in the 1970s wasprobably due to interspecific competition (Chapter 15). Another example is the decline of Euoniticcllus inrermedilius following the establishment of Digitonthophagus garella at another locality in Australia (Chapter 15). Digitonrhophagus garella has been identified as a superior competitor in the man-made assemblages of dung beetles in Australia. In North America, D. gnzello and some other introduced species have invaded relatively rich assemblages of nafive dung beetles. Howden and.Scholtz (1986) resampled a locality studied ten years earlier by Nealis (1977). The pooled density of beetles, as estimated by pitfall trapping conducted in the same way on both occasions, was twice as high in the earlier study. But in view of the effect of weather conditions and other such factors on trap catches, the difference does not imply any great change in beetle density. During the ten years, the study locality was invaded by D.gazella, which now accounted for 24% of’all individuals. Another native species, Onrhophagus alluvius, had similarly increased from 0% to 25% .relative abundance in ten years, while the relative abundance of Omhophagus gennsylvanicus had dramatically decreased, from 55% to 12%. Onrhophogus alluvius may have benefited from a gradual change in vegetation, but the earlier dominant 0. petaisylvanicus and some other species probably declined because of competition with D.gazeflu and 0. olluviics (Howden and Scholtz 1986). Note that Cambefort (Chapter 9) found no great changes in the relative abundances of dung beetles over a period of eight years at a locality in the Ivory Coast where no species had naturally or otherwise invaded. On the other hand, Doube (1987) reported substantial.changes in \. in southrelative abundances of species over a period of five years in a locality ern Africa. Stability of both indigenous and introduced populations of dung beetles is a topic in need of further study (Chapter 20). 16.4. SUMMARY

In this chapter we have reviewed three topics and three spatial scales in population dynamics: aggregation of beetles across habitat (resource) patches; dynamics of local populations connected by dispersal (metapopulation dynamics); and dynamics of species introduced from one continent to another. Small-scale spatial aggregation, such as occurs in dung beetles between dung pats, generally has a stabilizing effect on single-species dynamics, and if intraspecific aggregation exceeds interspecific aggregation, small-scale

,,

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1

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304

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Chapter16

aggregation tenda to facilitate coexistence of competing species. There are varying but generally high levels of intraspecific aggregation especially in small species of dung beetles, and we have discussed the causes of intraspecific and interspecific aggregation. Interspecific aggregation is lower in pairs of species belonging to different uibes than in those belonging to the same tribe, and in diurnal-nocturnal pairs of species than in diurnal-diurnal or nocturnal-nocturnal pairs. It decreases with increasing size difference between two species. These and other differences not directly related to resource use may nonetheless affect spatial variances and covariances and thereby the outcome of COITIpetition. We have examined dispersal and extinction in dung beetles and suggested the working hypothesis that the large, low-fecundity species living in seasonal environments in the tropics have a low dispersal rate and highly correlated local dynamics, while other species-for example, temperate AphOdiuShave the opposite characteristics, making their metapopu'lations more persistent. Some one hundred species of dung beetles have been introduced into Australia, New Caledonia, N o h America, Puerto Rico, and Hawaii. Of these, some forty species have become established so far. Several of the introduced species in Australia have become hugely abundant, demonstrating clear density compensation when compared with the species-rich assemblages in their native countries (Chapter 15). The most successful species include a variety of dung beetles in terms of diel activity, food relocation technique, and the tribe, but all are medium-sized, high-fecundity species with a high population growth rate and good dispersal ability, up to 100 km per year.

C H A P T E R 17

Competition in Dung Beetles Ilkka Hariski and Yves Cambefort

INTRASPECIFIC AND interspecific competition occur at least occasionally in nearly all communities of dung beetles (see most chapters in Part 2). In some situations-for t?xaniple, in African savannas on sandy soils in the rainy season (Chapters 8 and 9)--competition is severe and undoubtedly greatly influences the structure ofithe communities. Unfortunately, there is a lack of rigorous experimental work to demonstrate the degree of competition in different kinds of dung beetle communities, and an even more acute lack of results on the coiiscquences of competition vis-&vis the dynamics of populations and communities. Lack of relevant empirical studies, not lack of competition, explains why dung beetles have not featured in the reviews of the incidence of competition in natural populations (Connell 1983; Schoener 1983). Even at relatively low densities, when not all resources are rapidly removed, competition may nonetheless be the only type of interspecific interaction of any importance; other forms of interaction are simply uncommon in dung beetles (Chapter I). Two kinds of evidence can be put forward for competition in dung beetles, and our aim in this chapter is to collate a range of pertinent observations. First, for the rollers in particular, there s e innuinerable anecdotal obs rvations, though from a relatively small number of biomes, of direct interfere c e competition both within and between species, of individuals attemptin to steal dung balls from one another. HalFfter and Matthews (1966) have suggested that interfercncc competition (combat) is restricted to rollers, but the lack of numerous observations for dwellers and tunnelers, which hide mostly in dung pats and in the soil underneath, may well be due to difficulty of observation. Second, numerous observations have been made of preemptive resaurce competition in dwellers (in Apkodirrs, not in Oniticcllus), tunnelers, and rollers: entire droppings are removed or shredded by beetles, sometimes in(a matter of minutes. We supplement observations on preeniptive resource competition with records of high rates of immigration of beetles to dung-baited traps, indicating the potentially large numbers of beetles attracted to single resource patches. Dung beetles provide intriguing examples of how species' life histories have profound consequences on population dynaniics and on interactions between two or more species. Recall the resources required by the three types of

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Competition in Dung Beetles

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Beirne 1975b). 0.binodis (Ridsdill-Smith et al. 1982), Euoniticdlus intermedius (Hughes et al. 1978), and undoubtedly in many other species. Labo-

ratory studies arc useful in demonstrating what may happen when beetle density is very high, but even more valuable would be resulu from natural populations.

Exploitative Competition Table 17.4 gives examples of situations in which entire dung pats are rapidly removed by beetles, and where there consequently is no doubt that competition occurs and affects the populations of beetles. Individual pairs of large tunnelers commonly bury up to 500 g of dung (Edwards 1986a; Edwards and Aschenbarn 1987; Doube, Giller, and Moola 1988). hence even small numbers of these beetles in the same dung pat are likely to compete with one another (Fig. 17. I). As wilh interference competition, we must emphasize that preemptive resource competition o ~ c u r regularly, s though often seasonally, in many dung beetle communities (Kingston 1977; Peck and Forsyth 1982; Heinrich and Bartholomew 1979a; Chapters 8-12, 151, while it is more irregular in other communities. Most observations on preemptive resource competition are from tropical savannas and forests, and the beetles concerned are either rollers or tunnelers. Table 17.5 gives some examples of the rate of immigration of beetles to dung-baited traps. Such trapping results indicate how many beetles would

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species wils either absent U T had il c ~ n ~ l i l idensily it (two pairs of Colwis. four pairs of Oeirir).Thc vCni~al mi. gives the totill amount of dung buried (from Giller and Dovbe 198')).

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have anived at a dropping if the arriving beetles would not deplete the resources. If the number 01 arriving beetles is greater than the number sufficient to remove all of the resource, then there clearly is potential for resource competition. Although trapping results must be interpreted with caution, as they undoubtedly eliminate many biological idiosyncrasies among the species. the numbers of beetles actually trapped are often so enormous-by an order of magnitude or more greater than needed to remove all of the resource-that

314

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Chapter17

difference in abundance is due to some subtle differences in the soil type. known to have a major impact on dung beetle abundance (Chapter S ) , and possibly to predation of the buried dung by termites in Africa (Chapter 15). Another case of apparent but not proven density compensation occurs an mountains, where species richness declines with altitude (Hanski and NiemelS 1990). The average density of montane species has been found to be higher than the average density of lowland species both on tmpical (Chapter IO; Hanski 1989a; Hanski and Niemeli 1990) and temperace mountains (Chapter 14). As resource availability is likely to decrease with increasing elcvatim. this result could well be due to density compensation. 17.2. FROM POPULATION BIOLOGY TO COMMUNITY STKUCIUKE Population Dynamic Consequences of

Beetles' Behavior

Throughout this book we have employed two classifications to organize our thinking: ( I ) dung beetles have been divided into three main functional groups-the dwellers, the tunnelers, and the rollers (Chapter 3): and (2) we have suggested hat their competitive dynamics span a continuum from lottery dynamics to variance-covariance dynamics (Chapter I ) . It is now timc to couple these two classifications and to examine the consequences of the different types of behavior to the population dynamics of dung beetles and to the S ~ N C lure of theircommunities. The key difference between lottery dynamics and variance-covariance dynamics is the pattern of r e ~ o u n edivision and hence the reproductive success among breeding individuals (Chapter I). in the lottery model. the individuals that manage to breed amselected randomly from the p l of individuals, and their reproductive success is relatively even. In the variance-covariance model, all individuals may attempt to breed, but they have very unequal success because of intraspecific aggregation between resource patches. The variance-covariance model may involve scramble competition in contrast to contest competition in the lottery model, but this is not essential; the key point is intraspecifically aggregated competitive interactions among individuals.*What matters, then, are the f a c t m that affect the distribution of competitive interactions and resource division among individuals. The significant interactions in dung beetles occur at droppings, and the key processes are the arrival of beeUes at droppings, possible density-dependent emigration, and Ihe speed by which beetles are able to secure sufficient resources for their offspring. The order of arrival of beetles may be expected to be more or less random when comparing species with similar resource requirements and similar modes of foraging (not forgetting that many assemblages of dung beetles include spe-

Compelilian in Dung Beelles

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315

cies varying in foraging behavior: Chapters IO and 12). On the other hand, some droppings are always easier to detect than others; hence the overall rate of arrival varies between droppings. The dwellers, of which Aplmdius is the main example. represent one extreme. These are relalively small beetles in comparison with the size of the herbivore droppings they mnst frequently colonize. The larvae of Aphodius take some 5 days to hatch (Ridsdill-Smith 1990); hence the offspring initially have little effect on resources in the dung pat, and the colonization phase may last for many days (Hanski 19ROd). During this pcriod many iemales oviposit in droppings. and between-dropping difl'erences in the numbers of eggs and small larvae accumulate. Ovipositing females are unlikely to be able to assess the density of eggs already laid. and only if the instantaneous density of adult beetles in dung pats becomes high. deusitydependent emigration and oviposition may occur (Holter 1979; Yasuda 19R7), decreasing betweedropping variance in the numbers of beetles and their progeny. In summary, relatively small size and the breeding behavior characteristic for dwellers easily lead to variance-covariance dynamics in their populations. The other extreme is represented by many rollers. especially the species in tlic tribes Cymnopleurini. Scarabaeini. and Sisyphini. Mtny rollcrs pilerrr rclitively small omnivore droppings (Chdpter 18). increasing the ratioof the size of the beetle to the size of the resource patch. a key parameter of lottely versus variance-covariance dynamics (Chapter I). Rollers are often so abundant that all the available resource is removed rapidly, on a first-amved. first-served basis. Ideally, all the first PI beetles to arrive gain enough resources to make a dung ball with enough food for one larva, at which point all the r e s o u m is used up and no extra beetles arrive at the dropping. The resource is divided relatively evenly among the n beetles that are drawn more or less randomly fmm the individual p o l . This is an example of lottery competition (Chapter 1). In practice, the division ofresouxes is often not so orderly. As it takes some time to make a dung ball (below), large numbers of beetles m y accumulate before the whole resource is exhausted, and interference can be severe. Large species are typically superior in interfemme competition to small ones (Table 17.2). which may give rise to a bias towad large size in the set of species that manages to breed. Large nuinben of beetles may also disrupt the dropping to the extent that fewer than I I females manage to breed, For example, the small (introduced) roller, Neosis.vpbrs spinipes, may be so abundant in pastures in Australia. with thousands of beetles per pat, that only a small proportion Of beetles is able to make a bmud ball, and much of Ihe resource is "wasted" (Chapter 15; Neosisyphus may be especially sensitive to such interference because it is slow in making a ball). However, this situation does not invalidate the lottery model. Other dung beetles may also interfere with ball making. Heinrich and Bartholomew (19794 describe an extwne case from East Af-

Conipetrtion in Dung Beetles

.

319

to construct the nest in a hurry, apart from possible risk of predation during ball rolling (about which little is known). The rollers can select a favorable spot for bumwing, but there must be soils that are so difficult to penelrate for dung beetles generally that many rollers have great difficulty in making a burrow (Fig. 8.6). The nests of rollers are often shallower than the nests of coniparable tunnelers, though the depth varies much between species (Edwards and Aschenborn 1987) and depends, for example, on soil moisture (Rougon and Rougou 1983;Edwards 1986a; Chapter 13). To take an example, the large tunneler Heliocopris dillorti typically constructs its breeding chamber at the depth of one meter in East Africa (Kingston and Coe 1977), while the syntopic large rollers, Kheperpluorynorusand K . aegyPriOFUm, dig their breeding chambers at depths of 30-40 cm and 20 cm, respectively (Sato and Imamori 1986a.b). As a testable working hypothesis, we suggest that the faster a roller is in making and rolling balls, the worse it is in digging burrows. The size of the dung ball is related to the size of the beetle that has prepared it (Table 17.6; Halffter and Manhews 1966). Balls made by single beetles for feeding tend to be smaller than brood balls. which are often rolled by a pair of beetles (Table 17.6). The food balls are also made in a shorter period of time than brood balls: far example. in Canrl~onpilulurirrsthe average time to make a food ball is 15 min. whereas bmod balls take more than 30 min to prepare (Matthews 1963). The brwd halls may be so large that single beetles have difficulty in rolling them (e.g., Kheperplorynorus; Sat0 and lmamori 1987). The ratio of the weight of the ball to the weight of the beetle varies by the order of magnitude shown in the data in Table 17.6, from 6 in Sisyphus to 79 in Kheper plarynosus (see also the photographs in Chapter 3). Some of this variation is probably due to the difference between food balls and brood balls; but even allowing for this difference, it remains tNe that some species make relatively much larger balls than others and are hence able to provide their offspring proponionately more of the resource. A comparison of the species that use omnivore and large herbivore dung reveals that the former tend to have smaller balls in relation to their size than the latter (Table 17.6). Because omnivore dung is potentially of higher quality than herbivore dung (Chapter 3), the species using omnivore dung may possibly compensate for the relatively small amount of resource they are able to provide their offspring by providing higher quality. n e s e figures may be further compared with the amount of dung that tunnelers provision per offspring (Fig. 17.3). There is no significant difference in this respect between the tunnelers and the rollers that use herbivore dung, though the rollers tend to provision somewhat less food per offspring than the tunnelers: but both of these groups provide significantly more food per offspring than do rollers using omnivore dung. The amount of dung used for breeding per dung pat and per pair of beetles is, however, more than an order of magnitude greater in tunnelers than in rollers (Doube, unpubl.), independent of beetle size, because the nests of tunnelers contain many brood balls and offspring.

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decline with decreasing latitude is not in the number of species of Aphodiinae (Table 19.3) but in their average abundance, indicating that there is nothing intrinsically adverse in all subtropical and tropical environments for Aphodiinae. When the competitive pressure is we&, dwellers can do well at low latitudes. Bernon (1981) found large populations of Aphodiinae in cattle pats in South Africa in winter, when other beetles were relatively scarce. At this time Aphodiinae bred in the pats, while in summer, when competition from tunnelers and rollers was intense, the smaller number or Aphodiinae bred, atypically far the subfamily, in the sui1 below the pat. Cambclon and Wallcr (Chapter 1I) compared dung beetle assemblages that exploit elephant dung pats in savannas and forests in West Africa. The numbers of beetles in forests were relatively low, and elephant dung pats were not removed rapidly like in the savanna. The dweller Oniricell~pseudoplanoruswas abundant in thr forest. apparently benefiting fmm weak interspecific competition. The typical dwellers have little negative impact on tunnelers and rollers. Some species of dwellers, as well as some small tunnelers, have, however, reversed the competitive situation by becoming kleptoparasites of rollers and tunnelers, breeding in the dung reserves collected by the larger species in their nests. The offspring of the host species is assumed to he killed, though there are not many positive observations from the field (Chapter 13). Kleptoparasitic dung beetles are known from temperate regions (Hammond 1976). but they are especially common in subtropical and tropical grasslands (Chapter 9) and even in arid regions (Chapter 13). In the species-rich beetle assemblage in West African savannas, ahout 10% of all dung beetle species are kleptoparasiks (Chapter 9). While the interaction between nonkleptoparasitic dwellers and other beetles . . is clearly asymmetric, it is less straightfornard to draw conclusions ahout possible asymmetries in the interactions between the rollers and the tunnelers. In situations whek preemptive resource competition is severe, the crucial question centers on whi,manages to remove the resource fastest. The removal time has two major components: the time it takes to locate and arrive at a dropping, and the time it takes to remove the resource from the reach of other beetles. There is i o reason to assume thar either rollers or tunnelers should he inherently faster at locating droppings; both are often extremely fast. In tropical forests in Ecuador, Peck and Forsyth (1982) found that humansdung was t y p ically discoveced in less than one minute. Smaller species were the first to anive. but this may simply reflect their greater numbers. An important consideration, however. is that although most rollers are typically diurnal, most of the large and potentially competitively dominant tunnelers are nocturnal (Chapters 8 and 18). If the rate of resource removal is rapid, differences in diel activity give a definite competitive advantage to bath diurnal and nocturnal species at droppings that were deposited during the day and the night, respectively (Chapter 12).

Cuiiipeririirn in Dung Beriles

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323

As to the process of food removal from droppings to underground nests. the rollers seem to have an advantage over those tunnelen that are active at the same time of day. Rollen can s t m preparing a dung ball immediately after landing at a dropping, and once the ball has been made the equivalent amount of resource is away from the tunnelers, though not necessarily from other rollers, which may attempt to steal the ball (Section 17.1). The time needed 10 prepare a ball for transport varies widely. from less than 2 minutes (Klrcper lnevistrintrrs; Bartholomew and Heinrich 1978) to more than an hour (Neosisyplirrs spccicr: Cambefbrt. pers. obs.). A typical ligurc lor nrany?ip;cics is I j 30 min ( M m c h 1982: Scarabneus sacer, 32 min; Peck and Forsyth 1982 Conrlzort ongssmmr, 4 3 0 min; Matthews 1963: Ca,irlroapilrdarir,~, >30 mi"; Sato and Imamori 1986b: diurnal K l q e r , < I hour). The tunnelers are not ready to stan removing dung to their burrow before the burrow has been constructed. Peck and Forsyth (1982) found that O.t?srcrIWII compicillarus twk only 15-20 min to dig a burrow. We would guess that most tunnelers are not so fast, but qumtitalive figures are not available. Some large tunnelers, for example, Heliocopris species, first consmct a rough gallery into which dung is laken, before cnnsmcting the final nest, most probably to speed up dung removal from the dung pat. Another trickused by the largest species of Heliocopris is to rapidly cover the entire dropping with soil. a process that is faster than removing the entire dropping underground (Cambeiort, pers. ohs.). The time needed to cover the dropping may be equivalent to the time it takes to make a ball; hence these large tunnelers may be comparable in speed to large rollers. A female Heliocopris diNoni completed provisioning her nest in 6 lhoun (Kingston and Cot 1977). Doube, Giller, and Moola (1988) make a distinction between two parrems of dung burial in tunnelers. Coprini (Copris, Cniljar$irrs,Mmmvhnrriss) typically coinplete dung burial within 1-2 days. while many Onitini (Oiiitis) bury dung for many days, up to 6 weeks in 0. caffer (Edwards 1986a). The first type of beetles, the fast-burying tunnelers, obviously have a competitive advantage over the second type, the slow-bluying tunnelers. In conclusion. the above considerations suggest theSollowing generalized competitive hierarchy in dung beetles: [ I ) rollers and fast-burying tunnelers. of which many rollers may often be marginally dominant; but because there tends to be a difference in the diel activity of the two kinds of beetles, the possible small difference is not likely to be important in the field the first beetles to arrive have a competitive advantage: (2) slow-burying tunnelers and small tunnelers; and (3) dwellers. However. there are two further factors that enter the picture and need to be considered before the outcome of conipetition in the field can be understood. The first complication is an interaction between competitive ability and soil type. the second one is an interaction between competitive ability and fecundity. Both interactions facilitate the coexistence of inferior competitors with the lop competitors.

. 324

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Compelilion in Dung Beetles

Soil type has only indirect effects on the majority of dwellers. which spend their entire life cycle in droppings; but it is of decisive importance to tunnelers and rollers. which construct underground burrows and nest chambers far their offspring. The tunnelers are, as their name implies, specialist burrowers, wilh a morphology clearly adapted for digging (Fig. 17.2). The rollers, as we have discussed above, have a dilemma: they have two tasks that clearly call for different sorts of morphologies-namely, carving and rolling a ball and making a burrow for it. The difference in the morphology and, by implication, in the burrowing ability of the two groups of beetles suggesrs that the rollers suffer more than the tunnelers from soils that are difficult to dig in. The good competitive ability of the fast-hutying tunnelers is based on speed of burrowing, which must be affected by soil type; hence one may expect an interaction between competitive ability and sensitivity to soil type also among the tunnelers. Figure 17.4 illustrates our working hypothesis about a negative relationship between species’ intrinsic competitive ability and their sensitivity to the soil

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Chapter 17

inrerocrim between Comperilive Abiliry and Soil Type

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.

325

type. The rollers and the tunnelers with the highest intrinsic competitive ability are expected 10 dominate where the soil is most favorable for burrowing; the dwellers are predicted to dominate where burrowing is difficult, or nesting in the soil is impossible for other reasons; and the remaining species occupy the middle ground. Some beetles at the two extremes of the scheme in Fig. 17.4 have escaped the constraints imposed by soil type and low intrinsic competitive ability, respectively. Some Neosisyphur species, which have the longest legs i n dung beetles but which are clearly poorly suited for burrowing, have adopted an alternative nesting behavior: they atlach their brood balls to grass stems (N. spinipes; Fig. 17.2) or simply leave the ball on the soil surface after laying an egg in it (Paschalidis 1974; Cambefort 1984). thus avoiding nest construction entirely. Neosisypkus spirripes. originally an African species, does well in Australia in situations where the grass is not too much affected by drought or intensive grazing (Chapter 15). At the otherextreme shown in Fig. 17.4, some dwellers and small tunnelers have escaped their low status in the competitive hierarchy by becoming kleptoparasites. using the dung reserves in the nests of competitively superior species. The following competition model modified from Lande (1987; see also Hanski 1991) illustrates the populationdynamic consequences of the trade-off between good competitive ability and elevated sensitivity to soil type. Within any region, there is likely to be small-scale variation in soil characteristics, such that some dung pats are located on more favorable spots for digging by beetles than others. Let us consider two species: a competitively superior species 1, which is sensitive to soil type; and a competitively inferior species 2, which is less affected by soil type. For simplicity, let us assume that each female breeds in one dung pat at most (as many dung beetles do). Each female is able to search form pats, but she perishes without breeding if the first 881 pats 10 be located are on unsuitable soil or. in the case of species 2, they are occupied by a superior competilor. For simplicity, let us assume that the dung pats may be located on three kinds of soil patches: the worst patches (fraction U , of all patches) are unsuitable for both species; the best patches (fraction h ) are acceptable for both species; and the remaining patches (fraction U,) are suitable for species 2 but unsuitable for species 1. Competition is entirely asymmetric: species 2 can establish itself and breed in a dung pat only in the absence of species I, while species 1 is not affected by species 2. If p , is the fraction of pats occupied by species I ( O S p , S l ) ,at equilibrium (Lande 19871, (I-(~,+u~+p,h)’”)R =~1, ’

(17.1)

and

p t = I - ( I -k,)/h,

(17.2)

where R.’ is the net lifetime production of female offspring per female, con-

326

.

Cornpcrition in Dung Belles

Chapter 17

'

327

ditional on the mother's finding a suitable pat for breeding (for details, see Lande 1987), and k , = (1 - IiR,')"". The equilibrium fraction of sites occupied by species 2 is pa

I - (l-k)&+(I-Pi)h).

(17.3)

Fig. 17.5 shows that, depending on the structuc of the environment-in other words, on the values of U,,U,, and h--and depending on fecundity. longevity (R,,'), and the foraging ability (m) of the two species, neither species can maintain a population in the environment, species I or species 2 will occur alone, or the two species may coexist. The model could be extended to multispecies assemblages, where the species composition would change with changing habitat quality (soil type, in this case). The point is that the best cuinpetifors are expected to dominate on the soils that are easist to dig, whereas the inferior competitors are expected to dominate on harder soils. The best data set available to test this prediction comes from the subtmpical savannas in South Africa, where Doube (Chapter 8) conducted a factorial trapping experiment involving the soil type (deep sand Venus clay-loam), vegetation cover (grassveld versus bushveld), and type of habitat (pasture versus game reserve). The s p i e s were divided into five functional types, as explained by Doube (Chapter 8): large rollers, small rollers, fast-burying (large) tunnelen, and slow-burying large and slow-buying small tunnelers (omitting the dwellers, which were uncommon). Table 17.7 gives the results of an analysis of variance for the pooled biomass of beetles in the five functional groups. Vegetation cover (grassveld or bushveld) had no significant effect on beetle biomass, though there are individual species that strongly prefer one or the other of the two habitats (Chapter 8). The remaining three factors had a sig-

Functional g r u u ~of berries sui1 type

Hilbirnt type Funclions1 p u p x soil Funcliunvl group x hvbilal Habitat ~ y p cx wii

4 4

I

Rcsidunl

24

295

ToVal

39

1.499

S o ~ r r . rUulil : froin Table E.3. Nixc: Vcpcliliun ~ ( w e rhad 11" significicm cCfm on

R g 17 5 Model of caex~stence(from Hanski 1991) See (he lex1 lor dlrrussmr.

6.50 1.3s

11.36 10.26

0.00I I 0.0122 0.0025

o.ooo1

2.19

O.IW5

3.55

0.07im

b e a k bionuu and w m onlicld from

Ik

miiysis.

nificant effect (Table 17.7): but the most interesting point is that, ofthe twofactor interactions. only the soil type versus functional group interaction was significant, and very strongly so (Table 17.7). The biomass of large rollers (superior competitors) was an order of magnitude higher on sandy soil than on clay-loam, while the slow-burying tunnelers (inferior competitors) showed the opposite pattern, having a biomass twice as high on clay-loam soil as on deep sand (see Table 8.3). It is difficult to see anything intrinsically unfavorable in the sandy soils far the tunnelers; it is more likely that their numbers are suppressed by the large numbers of competitively superior large rollers on sandy soils. The biomass of the fast-burying tunnelers was lower on clay-loam than on sandy soil, though the difference was not as great as in large rollers. The fast-burying and slow-burying tunnelers are differently affected by soil type. and Doube's (Chapter 8) distinction between the two groups is an imponant one.

Inrerocrim between Coinperirive Ability mad Feecundily

HABITAT GRADiENT

320 90 139 S M 108 44

4 I 1

-

Large rollen and the largest and competitively most dominant tunnelers have very low fecundity. down to the absolute minimum of one offspring per breeding season in, for example, Kheper iligroaetzeus, a dominant species in the dung beetle assemblage studied by Edwards (1988a.b) in soulhem Africa. Many large rollers and tunnelers produce around five offspring per breeding season (Table 3.2), though this total may be achieved in different ways: some species (typically rollers) produce a series of clutches of only one from a series of dung pats, while others (typically tunnelers) produce a clutch of, say, five from a single dung pat. The competitively dominant fast-bulying funnelem

328

.

Competition in Dung Beetles

Chapter17

have lower fecundity than the competitively inferior slow-burying t u n n e l e r e around five offspring per breeding occasion in the former. versus twenty to forty offspring per breeding season in the latter (Doube, Giller. and Moola 1988, and references therein). Small tunnelers have even higher lifetime recundity-far example. up to one hundred offspring or more in 0nihophqu.s bbiodis (in the laboratory; Ridsdill-Smith et al. 1982). In Aphodius lifetime fecundity is also typically high, up to fifty offspring or more (Table 3.2). Large rollers and fast-burying tunnelers are superior competitors because of their ability to remove dung la lheir burmws quickly. To ensure that their nests remain undisturbed by other, later-arriving beetles, the nest must be constructed deep in the soil (tunnelers) ur away from the food source (rollers). Large size is an advantage in digging deep tunnels fast; but as the size of the beetle becomes large compared to the size of the dropping, the number of offspring that may be produced becomes necessarily small, creating a selection pressure toward a high level of parental care. Interference competition among rollers (Section 17.1) selects for larger size, though many small rollers are also highly efficient competitors (e.g., Sisyphini). Small rollers typically consfntct many nests in rapid succession during the breeding season; but many large rollers stay in the first nest caring foor their offspring, and they have consequently very low fecundity. Large rollers may often have difficulty in finding a dung pat where a good brwd ball could be prepared (Heinrich and Bartholomew 1979a). which may have selected for increased parental care. Good competitive ability, low fecundity, and high level of parental care constitute a single syndrome of large dung beetles. n e inferior competitors can breed successfully only in droppings lhat for some reason were not much used by the superior competitors: but the inferior competitors, which are typically smaller than the superior ones, may produce a large number of ofkpring in one such dropping. One mechanism allowing the coexistence of the two kinds of beetles is a variation of the one described by Kotler and Brown (1988) for desert rodents: due to trade-offs in eavel costs and foraging efficiency, some species may specialize an rich resource patches, while others use low-quality patcbes more efficiently. The dung beetle case is very asymmetric, however, and if all or most fresh dung pats were suitable for and were detected in time by the superior competitors, the inferior competitors would be excluded from the community. In practice, the superior codpetitors are not likely to use all-dung pats. These species search for fresh dung, and some pats may remain little used while fresh-for example, because of temporarily unfavorable weather for foraging. Other pats may be located in microhabitats that are unsuitable fur lhe superior competitorsfor example, pats located on hard soil. The important point is that (he relatively small size and high fecundity of the inferior competitors help them survive even in a highly competitive situation. Even a single dung pat not used by the superior competitors may produce dozens of individuals of an inferior competitor.

.

329

17.3. SUMMARV Intraspecific and interspecific competition occur occasionally in nearly all dung beetle communities, and in some communities, especially in tropical grasslands and forests, competition is constantly or seasonally severe: droppings are removed by beetles in a maiter of hours. Competition may occur between adults and larvae. and beetles may compete for food and for space, the latter either in droppings or in t h e soil underneath, where tunnelers conSINCL their nesls. The kind of Competition that may occur is dependent on the breeding behavior ofthe species. Paradoxically, competition is most obvious in the species in which only adult beetles c o m p t e only for food (rollers), while competition is generally weakest in the species in which both adults and larvae may compete for both food and space (dwellers). We have given examples of various types of competition. We discussed a competitive hierarchy in dung beetles, in which good conipetitors are able rapidly to remove food from the reach of other beetles. 'The top competitors are rollers and the large, fast-burying tunnelers; the weakest competitors are the dwellers. Competition in the rollers and large iunnelrrs is ofthe lottery type, while the variance-covariance model gives a better description of competition in small tunnelers and dwellers. In rollers, the two tasks of makin8 and rolling balls and digging burrows in the soil call for different types of morphology. and we may assume that rollers are generally more inept than tunnelers in making burrows. The good competitive ability of fast-burying tunnelers is based on the speed at which dung can be buried, and the speed must be affected by soil characteristics. We therefore propose tha1 there exists a negative relationship between the competitive ability and the sensitivity of the species to soil characteristics. This hypothesis predicts a shift from the dominance of rollers and fast-burying tunnelers on sandy soils (easy to dig) to lhe dominance of slow-burying tunnelers and dwellers on more difficult soil types for dung beetles. Quantitative data from African savannas and numerous other observations support this prediction. Small-scale heterogeneity in soil characteristics may provide spatial refuges for t b inferior competitors, while dung pats not detected rapidly by the top competitors may b% used efficiently by inferior competitors with relatively high fecundity.

. .

Resource Panilioning CHAPTER 18

Resource Partitioning Il!& Hanski and Yves Cambefort

IN CHAPTER 16 we emphasized the role of spatial aggregation in dung beetle ecology, and how intraspecific aggregation between droppings may promote coexistence especially in dwellers and small tunnelers, the two groups of dung beetles with the largest numbers of species (Chapter 4). This perspective was inspired by the fact that most dung beetles use essentially the same resource, which they find in the same place. Hence classical resource partitioning seems a priori an insufficient explanation of coexistence of many similar species frequeotly engaged in severe competition (Chapter 17). Nonetheless, it must be recognized, on balance, that there are various kinds of ecological differences among cooccurring s p i e s of dung beetles, many of which may facilitate coexistence. For instance, there are subtle and not so subtle differences in the type of dung used, and how it is used, by different species; there are differences in diel activity and seasonalily; and there are differences in habitat selection at small and large spatial scales. Not only in dung beetles but in all animals in general coexistence of competitors in natural communities is affected by many factors. Various kinds of nonequilibrium mechanisms of coexistence have been much explored recently (Chesson and Case 1986). but as emphasized by Chesson and Huntly (1988). Ule nonequilibrium mechanisms do not wipe ont resource partitioning and other equilibrium mechanismsthe challenge is to develop anintegrated theory embracing both equilibrium and nonequilibrium mechanisms. Schoener’s (1974) analysis of resource pwitioning in animals led to the conclusion hat “habitat dimensions are important more often than food-type dimensions, which are imponant more often than temporal dimensions.” Dung beetles fit lhhe first part of Schoener’s generalization: the contrast between grassland and fpiest assemblages is indeed great in tropical biomes where most species are found (Chapters 1 I and 15). What seems to be special about dung beetles is the critical importance of temporal dimensions. In this chapter we discuss resource partitioning in dung beetles based on information in Part 2 of this book and in the literature. We focus on four sets of dimensions. First, the kind (quality) and size (quantily) of resource patches selected by coexisting species: What do they explain about dung beetle guilds

,

331

and communities? Second, dung beetles span four orders of magnitude in size. and size differences may affect their competitive interactions. Third. dung beetles show habitat selection at the scale of a single dropping and at larger spatial scales, the latter often based on soil type and vegetation cover. And fourth, most dung beetle assemblages have well-defined guilds of diurnal and nocturnal species using the same resources. and in many biomes coexisfing species show striking phenological differences not explicable by specialization to different resources. In the final section of this chapter we turn to multidniensionill resource partitioning via an example from West AfTican savannas. which has one of the most species-rich communities of dung beetles found anywhere. The main conclusion we draw from this analysis is that the four dimensions discused in the earlier sections collapse into two composite dimensions: size of the species i s correlated with diel activity, and food selection is related to seasonality. The dominant species in the community are dislrjbuted nonrandomly in the space defined by these composite dimensions. 18.1.

SELECTION OF

RESOURCETYPE

The two main types of food resourcc used by dung beetles a x (large) herbivore dung and omnivore dung. In tropical forests in particular. many dung beetles are attracted to both dung and carrion, or even exclusively to carrion. for reasons Io be discussed below. Carnivore dung attracts relatively few dung beetles, which comprise a mixture of species that colonize dung and carrion (Hanski 1987a), undoubtedly reffecting differences and similarities in the chemical composition of these resource types. A small number of species, mostly fnund in tropical forests, has specialized on very particular resources, or has a very particular foraging behavior. A broad generalization, though largely based on experience from Africa, is that rollers tend to use relatively more omnivore rhan herbivore dung, while many large tunnelers use herbivore dung exclusively. We have suggested in Chapter 17 that the limited amount of food that the rollers are able to secure in a VanspoMble ball may bias their food selection toward high-quality omnivore dung, while’the large size of many tunnelers makes breeding impossible except under the large droppings of large herbivores. The extensive data from the lvoly Coast in West Africa (Chapters 9 and I I) allow a quantitative comparison of the numben of omnivore and herbivore dung specialists and of generalist species. If a specialist is arbitrarily defined as a species with more than 90% of individuals (see Appendixes B.9 and B.11) caught from one food type, the figures for savanna are forty-three omnivore dung specialists, sixteen herbivore dung specialists, and thinyane generalists, while the respective figures for rain forest are eighteen. eighteen, and two (rare species with fewer than ten individuals trapped have been excluded). These

I 332

Chapter 18

figures demonstrate that most species use pnrnarily one or the other of the two main types of dung

Specier Specialiiirrg in Large Herbivore Dung The most obvious group of species specializing in large herbivore dung consists of the large, nocturnal tunnelers, especially Coprini, though herbivore dung is strongly selected also by Oniticellini, which are mostly small, diumal species.'and by some large (Kheper) and small rollers (Neosisyphus]. The comprehensive data sets from subtropical and tropical savannas in Africa give a more detailed picture of Food selection in large assemblages of beetles and demonstrate that there are species specializing in herbivore dung in nearly all groups of species (Appendix B.91, suggesting frequent divergence in food selection in many taxa. The largest dung beetles may use various kinds of dung for their own nutrition, but during the breeding season they are constrained to use large herbivore dung because of the large quantity of food needed for their larvae. For example, the large Heliocopris species bury from 1.8 to 2.6 kg of dung for brwd formation (Klemperer and Boulton 1976; Kingston and Coe 1977), and the largest species can breed only under elephant dung pats (e.g., Heliocopris dilloni and H.colossus; Kingston and Coe 1977).

Species Specializing in Omnivore Dung While many species strictly specialize in large herbivore dung, there is generally a less strong preference by beetles for omnivore dung. Some species show seasonal shifts in the type of resource used. In West African savannas, many Pedario, Caccobius, and Cleplocaccobius species select omnivore dung early in the season, sooh after the rains have started, but later on shift to herbivore dung (Chapter 9; Appendix B.9). Young (1978) has reported seasonal shifts from coprophagy to necrophagy in dung beetles on B m Colorado Island in Panama. It is possible that such shifts are related to varying food selection between feeding (immature) and breeding (mature) beetles. Mobile adult beetles may search for the nitrogen-rich omnivore dung for their own nutrition, even if they provision their nests with the often'more abundant and carbohydrate-rich herbivore dung. An analogous difference in the nutrition of adult3 and larvae has bein commonplace in the evolution of coprophagy in beetles (Chapter 2). It is also possible that shifts in food selection are related to seasonally varying quality of herbivore dung. Kingston (1977) found that the nitrogen content of elephant dung varied seasonally from I% to 5%. being hiehest in the middle of the rainv season (see ChaDter 15 for studies conducted iniustralia). Still missing are &urate field obs&vations on the kind of dung used for feeding a d breeding by different sorts of dung beetles. .

..

Resource Parlitionins

.

333

Rcsoirrcc Seiecrim in Tropical Forests One of the tenets about animal communities in tropical forests is that they consist of a very large nuniber of highly specialized species (MacArthur 1972; Pianka 1974: Pielou 1975). This is not so with tropical forest dung beetles. In Africa, there are more species of dung beetles in savannas than in forests (Chapter I I), presumably because resource availability to dung beetles is generally higher in savannas, and has been so for a very long time. Second, many tropical forest dung beetles have a broad diet, one that is broader than the diet of their relatives in savannas. Dozens or even some hundreds of tropical forest species worldwide are attracted to bath dung and carrion, though it is not known whether they use both resources for breeding as well as for feeding. A parallel shift from a relatively n m o w food selection in temperate species to a wide food selection in tropical forest species has been documented for hark and ambrosia beetles, which Beaver (1979) attributes to rarity of most host trees in tropical forests: high degree of specialization would be disadvantageous because of difficulty in locating a particular host species. This quantity hypothesis may be contrasted with a quality hypothesis: there may be some qualitative differences in resource characteristics in tropical forests facilitating or favoring the widening of food selection. Availability of resources to dung beetles in most tropical forests is relatively low because of the generally low density and biomass of large mammals and low availability of any particular type of dung (Hanski 1989a). Halffter and Matlhews (1966) attribute the shift from coprophagy to necrophagy in many South American dung beetles to the general predominance of forests in tropical South America (true until recently), the absence of large numbers of large herbivores in the forests (and on grasslands;Janzen 1983b). and to the relative scarcity of necrophagous insects, potential competitors to necrophagous dung beetles, in South America. This quantity hypothesis mdy explain why necrophagous dung beetles are significantly less numerous in Africa (Chapter I I ) than in South-East Asia (Chapter 10) andSouth America (Chapters 12, 19). Until recently, large herbivores have been present in relatively large numbers in African forests, where a large number of dung beetles has specialized to use their dung instead of that of omnivorous mammals (Chapter I I ; see tigures in the beginning of this section). Two forms of the quality hypothesis are plausible, From a nutritional point of view, carrion is more similar to omnivore dung than to large herbivore dung (Hanski 1987a). and as most tropical forest mammals are omnivores, especially in South-East Asia and South America, tropical forest dung beetles may be expected to use carrion more often than the savanna species. Second, it is possible that many species consume c k o n only as adult food while still provisioning their nests with dung. In this case, carrion would represent a highqualify (niuogen-rich) resource of which the mobile adults may take advan-

334

'

Resource Partitioning

Chapter 18

tage. We have suggested in Chapter 2 that coprophagy has evolved from saprophagy via several steps, the first one being a shift in adult diet to highquality mammalian dung from the relatively low-quality vegetable diet. In an analogous manner, tropical forest dung beetles may be in the process of moving from dung to carrion. Exrreme Feeding Specialimions

Some dung beetles have become extremely specialized either in their mode of foraging or in food selection. To the former category belong the tropical forest species that forage in the canopy (Chapten 10 to 12). Same species may even breed in the cmopy, possibly using the sail that accumulates on large branches. In the other extreme, many dung beetles live in the bunows and nests of mammals, especially in arid environments (Chapter 51, while other species are found in caves and in ant nests (Halffter and Matthews 1966). The constant race to get to the resource first has led to some striking adaptations. In South America several species of small dung beetles (Trichillum, Peduridiurn, Llroxys) live in the pelage uf sloths (Ratcliffc 1980; Howden and Young 1981; Chapter 121, and they probably move to the excrement as sum as it is produced. Since sloths bury their dung (Ratcliffc 1980). these species may be the only ones to have access to this resourcc. Some Australian Onfhophogus (Mocropocopris)hold onto the fur of macropods with their prehensile tarsal claws (Chapter 15). The female seizes the fresh dung pellet, falls with it lo the ground. buries the pellet, and lays one egg in it (Matthews 1972). Onrhophagus b+zasciafus, 0.unifasciarus, and Caccobius vulcanus in India have taken the next logical step and occasionally colonize the resource before it actually exists, by entering the human intestine (Halffter and Matthew 1966; Perez-Inigo 1971). Other forms of extreme food specialization in dung beetles are described by Halffter and Matthews (1966) and by Gill (Chapter 12). 18.2. SIZEDISTRIBUTIONS Size Differences and Loco1 Coexisrence Size variation in dung beetles covers four orden of magnitude, from the smallest species of Panelus (about I mg) to the largest Heliocopris species, weighing more than 10 g of fresh weight, or four times the size of the smallest mammals, such as the smallest shrews. Size has far-ranging consequences to all aspects of animal ecology (Peten 1983: Schmidt-Nielsen 1984). Size differences in species using the same resource are often attributed to past competition, or to size-dependent assembly of local communities from a regional species pool (MacArthur 1972; Case 1983; Rummel and R o h a r d e n 1985;

-

.

335

Roughgarden et al. 1987). Many dung beetle communities are intensely competitive (Chapter 17), and several mechanisms related to size may facilitate coexistence: I. Size may affect food rclection. This happens especially in the ease of the largest species, which are dependent on the large droppings o f the largest herbivorous mammals. The asymmetry between small and large species i s reversed when compared with predators (Wilson 1975). Since in dung beetle. the Itrgeest. nut the smallest. spccies have the narrowest range of resou~ccsavailable 10 then>. 2. Sizc may affect the way a pPnicular dropping i s used. For example, Holler (19821 demonstrated differences in the pans of cattle pats used by different species of Aplrodius. and such differences are likely to be size-dependent. In Iunneler$. the UEC of space in Ilie soil below the dropping must depend on the size of the beetle, 11 lea* if very small and very large species are compared. 3 . Sire has special importance in rollers. because of frequent interference competition and because of the relationship between the size of the k c l l e and the size of the dung ball (Chapter 17). 4. Our findings (Chaprers 9 and 161 about dccreoring spatial covatinlcc with illcrevsing size difference in a pair of species suggest yet another. more rubrle inahanism by which size differences may facilitate coexistence. by decreasing intcrrpecilic aggregation in relalion tu inlrsspeeilic vggregillion (Chupicr 11.

While examining the spacing of species in size or along some resource dimension, it is informative to compare the most abundant or dominant species with the rest of the species in the community. Species-rich assemblages of invertebrates are likely to be mixtures of species in terms of their status at a particular site (Pulliam 1988): some species have locally breeding populations, while others are represented by "sink" populations, maintained by dispersal fmm elsewhere. Many of the rarer species may not have local populations at all (Chaptcrs S and 16); hence size may be irrelevant to their presence or absence in the community. or it may be more related to their powen of dispersal than to their competitive ability. Among the locally breeding populations, interspecific interactions are most frequent among the most abundant species. Thus if coexistence and dominance of competing species is dependent on their size relative to the size of other species, we may expect the most dominant species to be more evenly spaced out in size than a random selection of species (Hanski 1982). This approach avoids many of the difficulties of deciding what is a sensible "species pool" to which a particular community should be compared (Harvey et al. 1983). Several chaptws in Parl 2 reported on dung beetle assemblages in which cooccurring species are well separated in size. In three cases, in Aphodios in northern temperate regions (Chapter 5 ) . in Phnnoess in subtropical Nortli Amcrica (Chapter 7), and in rollen in African savannas (Chapter 9). the most dominant species in abundance or biomass were better spaced out in size than

4

336

'

Chapter 18

Resource Partitioning

were species in a random selection of equally many species from the community. Dominance in these assemblages is thus dependent on the species' size relations. Of the above mechanisms. numbers 2 and 4 are likely to be important in Aphodius, numbers I and 4 in Phonaeu, and numbers I , 3, and 4 in the rollers.

AFRICA

,

337

S O U T H AMERICA

a:

Comparison berween A f ~ c aond Sourh Arnerico

v)

Africa and South America have large dung beetle faunas with litlle taxonomic overlap (Table 4.1). In the rollers, South America is dominated by the old tribe of Canthonini, followed by the endemic Encraniini and Eurysterniini, while the African Communities axe dominated by Scarabaeini, Gymnopleurini, and Sisyphini. In the tunnelers. South American communities have large numbers of Dichotomiini, Phanaeini, and Onfhophagini, whereas the bulk of the African tunnelers belong to Onthophagini, Coprini, Onitini, and Oniticellini. In spite of these taxonomic differences, size distributions of rollers and tunnelers are strikingly similar on the two continents (Fig. 18.1). In the rollers. there is a clear distinction between small and large species on both continents. though the small rollers tend to be even smaller in Africa (Fig. 18.1). In the tunnelers, the size distributions of genera have identical parameter values on the two continents (Fig. 18.1). This distribution is not much affected by the very large African Heliocopris species. Similar large coprophagous species may have existed in South America before the extinction of the Pleistocene megafauna (Janzen 1983b). The largest extant South American species (Coprophanocur) are necrophagous.

z

Yw

Z

2

18.3. TEMPORAL RE$OIJRCEPARTITIONING

Diel Acn'vity Dung beetle communities often consist of about equally large guilds of diurnal and nocturnal species using the same resource. Many species have short diel flight periods (Figs. 9.4 and 10.2); for example, many "nocturnal" species are in fact crepuscular and may fly during less than one hour per ?4 hours (Chapter 8). Differences in diel activity are critical in dung beetles for three reasons.

.

.

First, if there is interference competition, which can take place only among individuals active at the same time, differences in diel activity increase the relative strength of intraspecific competition. Interference competition is common in dung beetles (Chapter 17). Second, competition is occasionally 50 severe in dung beetles, especially in tropical savannas and forests and among the species that use the relatively small droppings of omnivorous mammals, that all or most ofthe resource is removed within a few hours (Chapter 17). In

f

0t'ig. t X . 1 . Sire distrihutians uf gcnera and species uf mltc~s;and l u i i n ~ t ~ in r s Atriua said South Amcricu (dam fmm Plales 4.1 10 4.8). The species dislrihiitiun war calcu~ l a t d hy ,nulliplying the genus distribution by the iivinber of species in the genus. 181 Ihe rullers. Canthonmi are sti~wnwith a lighter Shading (nule Ihc major diflercncc

I

338 , Chapter 18

this case differences in diel activity give a species a definite advantage in competition for droppings that appear during or immediately prior to its time of activity. Species are typically either diurnal or nocturnal, undoubtedly because different adaptations are required for day and night activity. Therefore, a superior competitor cannot exclude a species that flies at a different time of day, provided that enough resources become available while the inferior species is active, and that the latter is able IO remove resources fast enough to a safe location, before the time of activity of the superior competitor. Third, even if beetles do not manage to remove all of the resource within 12 hours or so, differences in diel activity decrease interspecific aggregation in droppings (Chapter 16). which decreases the strength of interspecific competition relative to intraspecific competition and facilitates coexistence (Chapter I). Figure 18.2 compares s e e of co-occurring diurnal and nocturnal dung beetles from different biomes. Northern temperate dung beetle communities are dominated by Aphodius, most of which are diurnal, perhaps because nights tend to be too cold for flight activity (Landin 1961; Koskela 1979). However, since Aphodiur are dwellers and spend days or even weeks in droppings, where the larvae complete their entire development, differences in diel activity would not be very significant in Aphodius, in any case. In contrast, in tropical biomes diurnal and nocturnal (including crepuscular) species are approximately equally numerous, though oflen either the diurnal (especially in grasslands) or the nacturnal guild (in tropical forests) dominates in terms of biomass (Fig. 18.2), probably reflecting diel differences in the rate of resource renewal. Diel activity is a relatively canservative trait in dung beetles, as most species in most tribes are either diurnal or nocturnalicrepuscular. In Africa and

Resource PanitiuninL.

'

3 9

probably elsewhere as well, all Sisyphini and Oniticellini are diurnal, while the clear majority of Coprini are nocturnal. Gymnopleurini are mostly diurnal, though there are some nocturnal species of Garrefa, and even one Gjr?inoplerrrrc~@roJir,iss) is nocturnal in West Africa. The largest rollers, Kliupcr and Scorobaeus, have both diurnal and nocturnal species. Most tropical Onitini are nocturnal, but Plearorziris appears to be diurnal, and so are many temperate species (Doube. pers. conim.). It is tempting to speculate that the exceptional species in largely diurnal or nocturnal tribes have shifted their diel activity because of interspecific competition with congeneric or ecologically similar species. The two most species-rich genera of dung beetles, Onthophages and Aplmdins. are notable for a variety of diel activities represented by different species (Fig. 9.4). Kohlmann (Chapter 7) gives an example of B species (Mrgotkoposo,tra cmdeiei) that is diurnal in some regions but nocturnal in others. Doube (Chapter 8) and Cambefort (Chapter 9) have emphasized a broad difference in diel activity among members of the functional groups of dung beetles. As a rule, large tunnelers are nocturnal, while most rollers tend to be diurnal; small tunnelers include both diurnal and nocturnal species. Recalling that, as another broad generalization, rollers tend to use more omnivore dung and large tunnelers use primarily herbivore dung, the difference in diel activity between the two groups has two possible explanotiuns. Either something in the roller behavior is better adapted to daylight conditions and something in the tunneler behavior is adapted to darkness; or the difference in diel activity reflects a difference in diel changes in the rate of production of omnivore and herbivore dung, Among herbivorous mammals. the larger species need to spend more time foraging than smaller species. up to 75% of n twenty-fourhour day in the African elephant, with the result that the ntio of dnytinie foraging to nighttime foraging decreases with body size (Owen-Smith 1988). Elephants tend to show three peaks of activity: in the early morning, in late afternoon, and around midnight (Owen-Smith 1988). and as the largest amount of dung is voided at the end of the feeding period (Tribe 1976). it seems probable that more fresh elephant dung becomes available to nocturnal/ crepuscular species than to diurnal species. Many dung beetles have "dusk and dawn" Right activity, which may coincide with the peak production of dung by diurnal and nwtumal mammals, respectively (Chapter 12). SeOSO!lUliQ

Fig. 18.2. Proponions Of diurnai and noclumai dung beetles in terms of species. individuals. and biomass in five assemblages: A, nonh lcmpcrstc paslure (Chapter 5: 25 spccics): 8 . sublropical s i l ~ m n a(Chapter 8; 120 rpecicr);C . Lropicd si~vimna(Chapler 9: i W species); D. tropical foresl in Africa (Chapler I I : 75 spccicr); E. lropicill fwcst in Panama (Chapter 12; 59 species).

Seasonality in insects is generally controlled by three factors: resource availability, temperature, and rainfall (Wolda 1988). In dung beetles. rate of resource renewal varies little if at all seasonally, though resource availability and quality inay still show seasonal variation. During hot and dry weather. dung becomes quickly unsuitable far most beetles (Chapter 13). hence resource availability as experienced by beetles may vary with varying tempera-

340

'

R ~ S O U ~ Panilioning CC

Chapter18

lure and rainfall. Studies conducted in Australia have demonstrated that variation in dung quality affects the breeding success of many dung-breeding llies and beetles (Hughes and Walker 1970 Matthiessen 1982; Macqueen et al. 1986; Ridsdill-Smith 1986, 1990), though other species are little affected (Chapter 15). All three possible combinations of temperature and rainfall (soil moisture) as limiting factors are well documented for dung beetles. In northern temperate (Chapter 5 ) and montane regions (Chapter 14), temperature is the key factor restricting dung beetle development. In subtropical (Chapter 8) and tropical (Chapter 9) grasslands, rainfall demarcates the dung beetle seasons, though the proximate factor is soil moisture rather than atmospheric humidity. Some species take advantage of riverine or otherwise moist soils during the dry season (Cambefort, p e n obs.). Both temperature and rainfall are critical in the Mediterranean climates (Chapters 6 and 15). where winter is cold but midsummer is very dry, and dung beetle activity is concentrated in spring and autumn. Some species have, however, adopted an exceptional phenology. The dweller Aphodiw C O ~ S ~ L I Winferior , in competition to rollers and tunnelers, breeds during the cold winter months in southern Europe, when the superior competitors are dormant (Chapter 6). Other species occur throughout the dry summer period (Lumaret and Kirk 1987; Ridsdill-Smith and Mallhiesen 1988). The shortest favorable seasons for dung beetles occur at high altitudes an mountains (Chapter 14) and in strongly seasonal tropical grasslands. for example, in East Africa (Kingston 1977; Fig. 8.7). In the dry season in savannas, dung dries out quickly (Chapter 13), and the soils may become so hard that tunneling becomes difficult or impossible (Chapter 8). Beetles can survive in the soil during long periods, perhaps even several years, awaiting the heavy rains to soften the soil and their brood balls (Kingston 1977; Kingston and Cue 1977). The large Haliocbppris dilloni emerges in the evening of the second to the fifth day after mare tha6IOO mrn of rain has fallen (Kingston and Coe 1977). In the more humid Guinean savannas in West Africa, where the soil never dries out completely, some species appear before the first rains, taking advantage of the relative abundance of dung at that time of the year. Cambefort (Chapter 9) found that one-year4d individuals of Cymnopleurus coerulescens were the first to emerge, often preceding the beginning of the rains, while the young individuals emerged after the first rains. Neosisyphus spinipes attaches its brwd balls to'grass tussocks and is hence less affected by soil moisture. In Australia it emerges regularly at the same time of the year regarcless of rainfall (Chapter 15). Other temperate and tropical biomes have long, favorable seasons for dung beetles. In temperate regions. coexisting Aphodius typically show a clear seasonal succession of species, which is especially striking in &e dominant species (Chapters 5 and 14), suggesting that seasonality has been molded by interspecific competition. In the West African savannas where two rainy seasons

'

341

are separated by a short dry season, conditions are favorable for dung beetles for most of the year (Chapter 9). Some species breed continuously and may produce several generations per year, up to five generations in Sis?phas in southern Africa (Paschalidis 1974). with numbers increasing throughout the breeding season. Other s p e c i e s f o r example, most Gymnopleurinikonly breed in the very beginning of the first rainy season and spend the m t of the year in the soil. Seasonal dormancy (often diapause) is expected to occur whenever the cost of dormancy is less than the (negative) net benefit of remaining active. The literature on insect dormancy is primarily concerned with abiotic environmental factors, such as temperalure and humidity (e.g., Tauber et al. 1986; Danks 1987); but in taxa such as dung beetles. in which competition is occasionally scverc, it is likely tliat intraqpecific and interspecific interactions will also affect the costs and benefits ofdormancy versus activity (Hanski 1988). Whenever the degree of competition varies seasonally, some species (inferior competitors) may do better by becoming dormant during the period of most severe competition. It is possible that Gy,itnopleurus in West African savannas spend most of the year in the soil to avoid competition with Sisyphus in the late rainy season. It is important to recognize that competition alone is not sufficient to make dormancy. or "escape in time,'' advantageousvariation in the degree of competition is essential. In nonseasonal environments, dormancy is not expected to occur, regardless of competition, since an individual may gain nothing by postponing development. I n tropical forests in Sulawesi. Indonesia, the most abundant species occurred at remarkably constant numbers throughout the year. while the species with more seasonal occurrence were, on average, significantly less common, even during the peak of their seasonal occ~rrence (Chapter IO). Peck and Forsyth (1982) have reported an almost aseasonal activity of dung beetles in an Ecuadorian rain forest with no severe dry season. In a more seasonal forest in Panama, most dung beetles occur throughout the year (31% of species) or are more abundant in the rainy season (41%). but a lew species are restricted to the dry season (Howden and Young 198I: Chapter 12). In the clearly seasonal forests in the Ivory Coast, dung beetle activity broadly follows the seasonal pattern of rainfall (Chapter I 1 j.

18.4. SPATIAL RESOURCEPARTITIONING: HABITAT SELEC~ION

Dung beetles may show habitat selection at two spatial scales: at the scale of

a single dropping and its immediate surroundings, and at the macrohabitat scale, where the two most frequently studied factors are soil type and vegetntion cover.

342

.

Chapter I8

Microhabitat Selecrion Resource partitioning is conceptually related to interspecific competition: different species are assumed to use different resources because of past or present competition (MacArthur 1972). Microhabitat selection in dung beetles is not, however, a powerful mechanism for facilitating coexistence. Whenever competition is severe, (he entire resource patch is consumed rapidly, and the critical question is who is fastest, not, for example, which p m of the dropping some species will use first. Severe resource competition, approaching the Iottery type described in Chapter 1, is characteristic far many tropical communities (Chapter 17). In other communities preemptive resource competition is not common, and much ofthe resource remains unused for several daysar even weeks. Different species may now he found in different pans ofthe dropping, apparently using it in different ways. Halter (1982) divided. the northern European Aphodius into top specialists, bottom specialists, periphery specialists, and generalists, on the basis of which part of dung pats the species were most frequently found in. In southern Africa, different species of Sisyphus and Neosivphus tend to use different parts of cattle dung pats (Paschalidis 1974). Sisyphus sordidus and S. seminulum make their food and brood balls at the edge of the pat or in crevices on its surface; Neosisyphus infuscarus and N . mirabilis are found under or in the edge of the pat; and N . fortuitus, N. rubrus, and N . spinipes utilize the more central parts of dung pats. Such microhabitat selection, whatever its causes, increases intraspecific interactions and therefore amplifies the effects of spatial aggregation,of beetles between droppings (Chapter 16). Intraspecific aggregation between and within droppings, apart from increasing intraspecific competition in common species, may be imponant in facilitating mate finding in rare species (Holler 1982). Tunnelers and rollers c,onsVUct their nests in the soil below or some distance away from the dropping. There are clear differences among different species in nest location and architedure (Halffter and Edmonds 1982; Edwards and Aschenbom 1987). Such differences, which comprise another element of resource partitioning at the within-patch scale, can be important even ifpreempfive resource competition is severe. The major behavioral difference between the rollers and the tunnelen k best understood as a form of resource partitioning at this scale: rollers largely avoid competition Tor space in lhe soil by rolling their share of the resource some distance away from the food source.

Macrohabitat Selection The contrast in the species composition of dung beetles in open grasslands and forests varies with latitude. Table 18.1 gives three examples from north lempeme, south temperate, and tropical biomes. In north temperale regions, forests are generally poor in dung beetles, though there are some continental

differences: for example, Norlh America seems to have more forest species of Aphodius than Europe (Chapter 5). Most of the species that can be found in woodlands in England are common pasture species (Appendix 8.5).South temperate forests have more dung beetles than norlh temperate forests, but most of them are still ubiquitous species present both in open habitats and in forests. and typically they m more abundant in open habitats (Chapter 6). From subtropical Costa Rica, Janzen (1983hj has reported some of the dominant species from both pastures and forests. Finally, in the tropics, both open grasslands and forests have a rich fauna of dung beetles, and there is practically no overlap in species composition (Chapter 1I). The general pattern thus is a change from much overlap in species composition between the grassland and forest assemblages ai high latitudes to no such overlap nt low latitudes. These changes undoubtedly reflect changes in resource availability in forests and grasslands with decreasing latitude: tropical forests have more resources for dung beetles than ternperate forests. The contrast between forest and prassland habitats may be greater at low than at high latitudes, but one may also speculate that the higher diversity of beetles at low latitudes has led to a greater degree of habitat specialization. Several chapters in Part 2 have discussed in detail the effect of vegetation cover on dung beetles in paaicular biomes (see especially Chapters 5, 6, 8, I I , and 15). Other studies on macmhabitat selection in dung beetles include Koskela (1972). Howden and Nealis (1973, Nealis (1977). Doube (1983). and Fay (1986). Soil type has both direct and indirect effects on dung beetles. Soil type may indirectly affect all beetles by changing the conditions in droppings. Walerlogged soils are an example of habitats that are generally poor for all dung beetles. Lumaret and Kirk (Chapter 6) contrast two kinds of paslures in southern France on compact limestone and on a flinty limestone with m a r k The latter site was poorly drained and occasionally flooded, and had very low density of dung beetles, apparently because of high mortality of beetles and (heir larvae in the soil. A p m from the indirect effects, soil type is of little importance to dwellen. which spend most of their life cycle inside droppings. In contrast, soil type is of decisive imporlance to tunnelers and rollen. which

344

,

Rewurce Pmilioning

Chapter18

construct underground burrows and nest chambers in the soil. Several of the chapters in Part 2 have documenled changes in dung beetle assemblages fmm one soil type to another, and in Chapter 17 we outlined the expected effects of soil type an different kinds of species, Doube's (Chapter 8) data from southem Africa allow a quantitative assessmen1 of the distribution of 120 species of dung beetles in four soil types. In a principal component analysis, more than two thirds of Ihe variance in beetle numbers is accounled far by the first component, reflecting general abundance differences between the species (Table 18.2). The second component (20%of variance) describes a conhast between sandy soils versus lom and clay soils, while the third component (5% of variance) reveals a cunlmt between the latter two sail types. Many species are more or less reseicted to particular soil types. as discussed in Chapter 8. After the effect of the first principal component is factored out, the species that are located farther away from the origin of the plane of the second and third components have higher biomass than species located in the center (Table 18.3). This result indicates that the dominant species tend to be specialists on particular soil types. Regional species richness of dung beetles may be greatly enhanced by variation in soil type.

18.5. MULTIDIMENSIONAL RESOURCE PARTITIONING: AN EXAMPLE FROM WESTAFRICAN SAVANNA

Four Primmy Dimensions Collapsed inlo Two Dung beetles do not divide resources along one resource dimension at one time but, like the populations of most animals and plants. populations of dung beetles are affected by several dimensions simultaneously. In this section we examine multidimensional resource partitioning with one paITicularexample. the dung beetles of West African savannas, described in detail in Chapter 9. This assemblage has 119 species (Appendix B.9; there are also four species recorded from carrion or vegetable matter). Figure 18.3 presents the distributions of the 1 I9 species along the four dimensions we discussed separately in the previous sections: type of resource (omnivore versus herbivore dung), size of the beetle. diel activity, and seasonality. Most species in this assemblage show a clear preference for either omnivore or herbivore dung (Fig. 18.3). I h e size distribution is not normalized

80

TABLE18.2 Principal component analysis of the ~ ~ c u r n n of e e dung beetles in four soil types in southern Africa Soil Type

PCI

Deep sand Duplex (rand over clay)

-0.40

clay

Skeletal loam Percenraee of variance

-0.56

-0.52 -0.50

PCZ

PC3

PC4

-0.81 -0.14

-0.13

0.41 -0.81 0.34 0.23

O.M 0.1 I

0.32

-0.69

0.48

20

13

5

Source: Data fmm A ~ p e n d iB.8 i

SIZE

FCOD 40

60

; (0

2

, 345

2

40

20

0 '

20 40 60 80100 SEASONAL

-05

TABLE18.3

Unwveighted least squares linear regression of the logarilhrn of beetle biomass against FCt and the dislance from the origin ofthe plane of PCZ and PC3. Vorioble CO"S-1

PCI Dirlance

Coeficient

SE

1.78 -0.35 0.72

0.12

0.05

14.51 -7.11

0.13

5.61

f

P
<0.0001

NU^: PDncipal components fmm the analysis in Table 18.2. n = 120, o v ~ r a I IF ? = 0.54.

=

611.51.

Fig. IX.3. The four panels give drrr on food selection (the horimnlal axis gives pmpurlion uf individwsis attracted to omnivore dung). size (loprithmic t r a 3 f o n t i O e ) . did activity (diurnd YCCSUS n ~ c t ~ r n n species), l and wasoiiality (the IhorizontPl axis gives pruponion uf individuals caught i n ApriCMay) i n dung heerlca in We51 African snvil,,nil.

346

'

Resource Panitioning

Chapter 18

by logarithmic transformation. but it remains skewed toward large size (Fig. 18.3). Diel activity is recorded only as diurnal or nocturnal, though both gmups include species with more restricted times of activity. Many species have an "early" seasonal occurrence at the study site in the Ivory Coast, being active primarily or exclusively in April-May, following the beginning of the rainy season, while other species have a longer or later seasonal occurrence (see also Fig. 9.3). Data on the positions of the 119 species along the four dimensions were subjected to a principal component analysis to find out the dimensionality o l the community. The first two principal componenls accounted for most of variance, 40% and 31%. respectively, because of two correlations between the original variables: nocturnal species tend to be larger than diurnal ones, and while most omnivore dung specialists have an early seasonal ~ccurrencc, the herbivore dung specialists lend to have a late seasonal occurrence (Table 18.4). The I19 species are well spaced out on the plane delined by the l i n t two principal components (Fig. 18.4).

. ." . - 2 1 - 1

A "

.

347

02

0

0

1

3

2

PRINCIPAL C O M P O N E N T 1

Nortrundom Communi@ Structure The competition-centered community ecology (MacAAur 1972: May 1973; Roughgarden 1979) is much concerned with the distribution of species along resource dimensions, and ecologists often examine whether the spacing of the species along one or more such dimensions is more even than expected by chance (Schoener 1974), which is often taken as evidence for past or present competition. Overdispersed niches have been documented for a variety of species, for example, for lizards (Pianka 1975; Schoener 1974), granivorous desert rodents (Bowers and Brown 1982), insectivorous mammals (Hanski 1991) and intestinal helmints (Bush and Holmes 1986). For the reasons explained in the section on size distributions (Section 18.2), we have compared here the spacing of the most dominant species in the community along resource dimensions, with the spacing of all species on average. Dominance has been meaTABLE18.4 Correlations belween the first two principsl componenis (Fig. 18.4) and thc hmr rcourc cc dimensions in the West African dung beeile assemblage.

Resource Dimensio,z Beetle sire

Food type

Diel activity Seasonaliiy

Percentaee of Yariance

.

Sm'lll values In . . .

PCI

PCZ

Small species Omnivore dung specialisis Diurnal species Early season species

-0.sz

-11.47 -0.43

0.54

-0.5

0.42

-

0.48

-11.61

L

UI ,001

0

20

40

60

RANKED S P E C I E S

-

80

Fig. IX.4. ( A I Loadings uf the I I 9 species of dung beeller along the 6rsl two principal ;tnulyris bvrcd on thc variablcs shown in Fig. 18.3. For conelalions DI tlic caiuponcnls will1 thc original vwiables, sec Table 18.4. The lifly iiiost doininon1 species llrrgerl biotn;ms) linve h c m indicnlcd with il bliick dol. ( 8 )The prohilbilily lhat tbc Irn~ostdoininant species (horizunlill axis) hilve the s n i i i ~average dislance fmnl the nrigin in pancl I A I thnn equillly many nndomly selected spcies. C C ) I I I ~ I I I I Ciii ~ ~ iin S

348

'

Chapter 18

sured by biomass, the individual weight multiplied by numerical abundance, because of huge size differences among the 119 species, from 3 to 5,800 mg in fresh weight. Our approach is to compare different subsets of the most dominant species with a randomly selected group of equally many species from the total of I19 species It is apparent that the dominant species have a highly nonrandom distribution in the plane of the first two principal components: the dominant species are located farther away from the origin than are all species on average, while many of the rarer species are clustered in the center (Fig. 18.4). Furthermore. the average distance between two dominant species is signilicantly greater than the average distance between two uncommon species (the painvise distance among the 59 most dominant and the 60 least dominant species was less than 2.5 in 51% and 78% of pain, respectively; the diffccrencc is highly significant). m e pattern in Fig. 18.4 is just the opposite to the one described as centrifugal community structure by Rosenzweig and Abramsky (19861, in which the dominant species occupy the central positions in habitat space (Fig. 18.4 is not, ofcourse, a description only of habitat selection). Two conclusions may be drawn from these results. First, cenain combinations ofecological parameters are more frrequent among the dominant species than could be expected by chance. Thus in the early season omnivore-dung guild, reiatively large diurnal rollers (Gymnopleurini) arc dominant (10 "I' 14 dominant species), while the late season omnivore dung guild is doniinated by small diurnal and large nocturnal species (8 and 7 of 17 dominant species, respectively). The late season herbivore guild is dominated by large diurnal and nocturnal species (5 and 10 of 18 dominant species). Almost missing campletely are early season species specializing in herbivore dung, regardless 01 diel activity and size. Although absent in West African savannas in the Ivory Coast, such species occur in localities with a short rainy semon. for example, in the drier parts of East Africa (Kingston and Coe 1977) and in southern Africa (Doube, pers. comm.), where dung beetle activity is severely constrained by soil moisture (Fig. 8.7). Our secondconclusion is that the distribution of the dominant species along the two composite dimensions in Fig. 18.4 is less clustered than the distribution of species with lower biomass and hence with smaller impact in resource use. We suggest that this pattern is due to the frequently severe competition in this community of dung beetles. 18.6. SUMMARY This chapter has examined partitioning of four kinds of ecological dimensions by dung beetles: the t w e of IesouTce. !he size of beetle. habitat selection. and

Resource Partitioning

'

349

tropical forests, many dung beetles use carrion and decaying fruits. The size of dung beetles varies by more than four orders of magnitude, and in several assemblages the most dominant species in abundance or biomass are more evenly spaced out in size than are all species on avenge. Partitioning of space for breeding in !he soil below and in the vicinity of droppings is the key form of small-scale spatial resource partitioning, while at larger spatial scales habitat selection with respect to soil type and vegetation cover Is commonplace. The species-rlch tropical communities have typically about equally large guilds of diurnal and nnctumal species using the same ~csource.Dung beetles provide examples of many types of seasonality to entirely aseasonal dytiaiuics in some tropical forests. In a West African savanna community. which represents one of the most species-rich dung bectle assemblages, with I19 species, the dominant species in biomass have a nonrandom distribution among all the species with respect to composite resource dimensions (principal component analysis). Cettain combinations of ecological parameters are more frequent among the dominant species than could be expected by chance, but the distribution of the dominant species along the composite dimensions is also significantly less clustered than the distribution of the uncommon swcies.

Species Richoess

C H A P T E R I9

L;llitudinal change in tlic numbcr of species and Ihe relsliw (pooled) abundance of rhc three futlcliunnl groups ofdung b a i l c s in upen grilsslonds.

Rei. Ab,mdmln,lrr

S/XC,<S

IIkka Hanski and

Loculi,!

Yves Cambejart

Norria rumpcmrc

mechanisms that may allow their coexistence in spite of frequently severe competition (Chapter 17), namely, aggregated spatial distributions (Chapter 16) and resource partitioning, including interspecific differences in foraging and breeding behavior (Chapter 18). Ultimately, one would like to have a theory capable of predicting patterns in species number and other such general attributes of communities. We do not have such a theory, only some building blocks that may prove useful for constlucting the theory. Our purpose in this chapter is to summarize global patterns in species richness of dung beetles and to relate trends in species number to these building blocks: varying level of interspecific competition, aggregated spatial distributions across habitat patches, and resource partitioning. One particularly interesting case is the insect community inhabiting cattle dung pats, a resource now universally available from north temperale to tropical biomes. In some regions, cattle dung has been present Tor long periods of time. In other regions it complements or replaces other, similar types of dung; and in still other regions cattle pats represent an entirely new kind of resource for insects. A comparative study of the insect communities exploiting this single resourcc in different parts of the world provides some interesting opportunities for a community ecologist. two

19.1. PATERNS IN SPECIES RICHNESS Latitude and Altitude The common latitudinal pattern in nearly all taxa is an increase in species number with decreasing latitude. Table 19.1 compares local dung beetle assemblages in open grasslands, from northern temperate pastures (61"N) to topical savannas. Species belonging to the three functional groups of dwellers, tunnelers, and rollers have been treated sepmlely. The dwellers, largely consisting of Aphodiur, are the most widespread group of dung beetles, with no great change in species number with latitude, at least not in terms of species

35 I

T ~ L 19. CI

Species Richness

LOCALCOMMUNlTtES of dung beetles may have dozens of species using the same resource (Chapters 6, 8-12). In the previous chapters we have discussed

,

I

Finland N Englmd s England

R

D

T

-

100 tu0 100

-

T

Lolilude

D

61" 54-N

52"

I8 I4 23

44"N 42"N

14 22

16 14

-

26

250s

68 104 72 75

12 19 13 18

53 + 7 5

I -

2

-

R

+

R

q

-

+

i I

2 3

S,,Z,,l, r
S France B"lgXia

4

5

8

6

74

9

4 5

-

Tropic01

s Africa tvury CUlSl

6-N

28 27

Zaire Kenya.

2's

R

3 3

29

6

39 4

9

? 2

8

3

'I 3

6

6 7 8 4

ReJ#rorcs,r: I. Hzmski und KorkeluIIY77): 2. WhilellYW0):3.CL;lpirr5:4.Cllvpler6:5. B e y n a y e r andZichiricva~SlulluvrlIY751:6. Bcrnon 1 1 Y S I l ; 1 . Chapicr9:S. Walterl19781: Y. Kingstan (19771. N o w U. dwellcn: T. Iunnclcn: R. ruIIcr$ * Elcphrnl dung only.

number in I o d communities. The rollers represent the other extreme. with substantial numbers of species being found only in subtropical and tropical communilies. The tunnelers show a more steady increase in species nuniber from nonhem tanperate to tropical communities (Table 19.1). The pattern is different in numbers of individuals, which reflect better than species number the interactions among the three functional groups. The nonhern temperate communities are entirely dominated by Aphodius (dwellers), with only a few species of tunnelers (Geotrupes, Oitrlrophogus) acd no rollers. The southern temperale communities present a mixture of species, with tunnelers generally being the dominant group. The tropical communities are dominated either by tunnelers or by rollers, depending on season (Chapter 9: rollers are often most abundant soon after the start of rains), soil type (Chapter 8: rollers are most abundant on soils that are easy to dig), and dung type (Chapter 9: many rollers specialize in omnivore dung). A detailed picture of the distribution of beetle biomass among the functional groups in south African habitats is given in Table 8.3, Table 19.2 gives some examples of numbers of coexisting species in local communities, expressed as the expected number of species in a random sample

I 352

,

Chapter19

Species Richness

TABLE19.2

Species richness of dung beetles in different biomes and habitats (rpecier in the f a n lies Scarsbacidae, Aphodiidac, Geotrpidae, and Hybosaridae). Biome and Hnbilor

Specie~Nun,ber(*SD)

R?J

N emperate pasture

13.5t0.8

I

S tempeate forest

16.321.6

2

S tempcrate pasture

1 Y . 6 1 1.5

3

Tropical prim- forts1 rich in mammals Tropical second- forerr rich i n mammal3 Tropical secondary forest poor in mammals

48.7+2.1

4 4

rmprcal mulane torcst Tropical gallery forest Tropical savanns with elephants Tropical ~avannawilh cattle Tropical savanna without large mammals

39.6r1.9 21.1 i o . 9 16.0

4 4

12.6+1.4

4

5o.4+ 3.4

5

47.3*3.2 29.7r2.6

5

5

Refirrnrrr: I . C h a p t e r 5 ; 2 . L u m ~ ~ ( u n p u b . l : 3 . C h ~ r e r b : ~ . C h a p t ~ r 1 l : 5 . C h a p t c r ~ .

N o w Species richness was estimated by rarefaction (Simberlofi 1979) and is erpressed as the expected number vf species in a sample of 3W indlvldUlualr.

of three hundred individuals. These figures range from about ten in north temperate pastures to about fifty in tropical savannas in Africa. Species number decreases with increasing altitude. The highest recorded altitudes for dung beetles are from the largest mountain ranges, between 4,000 and 5,000 m in the Himalayas (Chapter 14). The decline in species number with incmsing altitude is slower on larger mounlain ranges than on isolated mountain peaks (Chapter IO), undoubtedly because of an area effect (MacArthur and Wilson 1967; Mayr and Diamond 1976). Mammalian Species Richness

Three aspects of mammalian species richness have direct consequences for dung beetles. The general abundance of mammals sets the level of resource availability to dung beetles. The range of different kinds of mammals determines the range of dung fypes available to beetles, while the size of mammals is of special imparlance to the largest species of dung beetles, which are more or less dependent on large droppings for breeding. These three aspecls of mammalian communities are often related to one another. The African game parks are favorable for dung beetles in all three respects, which undoubtedly goes a long way toward explaining why they have more species of dung beetles than any other ecosystem.

'

353

In West African savannas, both the diversity of dung beetles and their average size are highest at localities with a rich fauna of mammals, including the elephant. and lowest at localities with only small mammals and man (Fig. 9.6). The expected number of species in a sample of three hundred individuals was fifty in savanna with elephants, forty-seven in savanna with cattle, but only thifly in savanna without large mammals (Table 19.2). Similarly, African secondary forests with a rich mammalian fauna had forty species among three hundred individuals, while forests with a poor mammalian fauna had only twenty-seven species (Table 19.2). On the other hand, it is noteworthy that both in the data in Table 19.2 and in Table 8.3 for southern African localities, grasslands with only catrle and grasslands with wild large herbivores have similar levels of species richness. These results suggest that abundance of large herbivore dung is more important lor high species richness than the range of dung types available (the pastoral regions probably have some omnivore dung 10 support species specializing in this dung type). The largest species of dung b e e t k are dependent on the dung of the largest herbivores. The extreme example consists of the one hundred species or sb that use exclusively or primarily elephant dung to provision their nests (Cambefon. an unpublished estimate). When elephants and other large herbivores go extinct. the largest dung beetles are doomed. This is probably what has happened lo many Heliocopris species. Heliocopris is an old genus with a much more extensive geographical distribution in the past than at present (today il is mostly restricted to Africa). For example, Heliocopris is known from the Japanese Miocene (Fugiyama 1968). and there are old and a few recent records from Borneo, Java, and Sumatra, which had or still have (remnant) populalions of elephants. lanzen (1983b3 suggests that many large dung beetles may have gone extinct in South America with the extinction of the Pleistocene megafauna: ground sloths. gomphotheres, glyptodonts, horses, and so forth. Africa is the last continent that still has a rich mammalian megafauna (Fig. 19.1). and a rich fauna of very large dung beetles (Plates 4.1 and 4.8); but locally and regionally the largest beetles are threatened also in Africa. Some large species of Hereroniris have successfully bred in donkey dung in the absence of elephant dung, but the size of individuals reared with the relatively small donkey droppings is smaller than the size of individuals bred with elephant droppings (Chapter 9). Disappearance of elephants creates a strong directional selection toward smaller size in the largest dung beetles and, incidentally, provides interesting material for the study of the evolution of body size. An interesting example of the reverse situation is presented by Sulawesi. which has large herbivores (fares1 buffalo) but no species of Carharsius and Synapsis, the largest South-East Asian tunnelers. Sulawesi has many species of Copris, however, and the largest Copris in Sulawesi are larger than the congeneric species in Borneo, where there are Cafharsius and Synapsis. Large

f ~~

354

'

15

Q

a: Y w

10

Chapter19

AFRICA

L

l5

1

ASIA

l5 10

'0

5

5

K W

3

z

15 NAMERICA l 5

S AMERICA l 5

10

10

10

5

rn -

Fa EUROPE

AUSTRALIA

5

A B C D E

A B C D E

IlIcrL A B C D E

F i g . 19.1. Numbers of megaherbivore genera represented in six co~lincnldfaunsn during different periods of time: A , Pliocene; B , Early Pleistocene; C. Mid-Pleismcene;D,Late Pleistocene; E,"R.%ent (from Owen-Smith 1988).

species of Copris have probably evolved in Sulawesi to occupy the niche Of the largest tunnelers.

Comparison of TropicalForest Regions An interesting continental'comparison can be made in the species inhabiting tropical forests in South-East Asia, Africa, and South America. There are obvious differences in the mammalian faunas between the continents, especially in the absence of large herbivores in South America and most of South-East Asia; but if the comparisons are resuicted to species using omnivore and small herbivore dung (most species), there are no qualitative differences in resource availability. Tropical forests in South-East Asia, Africa, and South America typically have 50 to 60 species of dung beetles. lsolaled fragments of forest (Peck and Forsyth 1982; Nummelin and Hanski 1989),riverine forests, and forests With clearly impoverished mammalian fauna (Table I I .4) have fewer species. Lo-

SpiesRichss

'

355

cal species richness in extensive tracts of forest is surprisingly constant and apparently little related to the size of the continental species pwl. Thus the total number of dung beetles (Scarabaeidae) recorded for Borneo is 120, of which some 60 were found in a comprehensive survey of the Mount Mulu National Park in Sarawak (Hanski 1983). South America has about 1,250 species, of which some 55 were found in a locality studied in Colombia (Howden and Nealis 1975). Clearly. not all South American species can be expected to occur in Colombia, but the result remains nonetheless striking and suggests an upper limit to the number of locally co+ccurring species. In fernul of the kinds of species present in tropical forests, there is relatively little difference between South American and South-East Asian communities, while the African forest communities are different from both (Table 19.3). This divergence is not unexpected, because while the South American and South-East Asian dung beetle faunas evolved on foresled continents, the African fauna has fundamentally originated in savannas. In the taxonomic composition, canthonine rollers are well represented in South America, are quite numemus in some regions in South-East Asia, but enlirely absent or very rare in Africa. Rollen on the whole are represented by only a few uncommon species in African forests (Chapter I I), while typically in South-East Asia one 01 two large rollers (Poragynirtopleurus)play an important role in local COIIIIIIU-

TABLE 19.3 Tropical forest dung beetle assemblages in South-Ea~tAsia, Africa. dSough America.

SE Asia

SA m d m

Africa

I

2

Rollcn

13

Tunnelcrs Dwellers

48 I

4 37 4

5 70 15

4 62 17

?

28

81 2

-

Diurnal species Nucturnal species

4

7

7

Unknown

62

45

30 45 15

Coprophagous species Necrophagous spccics Gencrzlistr & uthcrs

I2 13

8

25

84

5 9

3

?

Unknown

29

Perching on leaves

-

3

38 17

21 35

-

3 33 26

34

6

-

-

16 9

IO

10

7

15

~

356

'

Chapter 19

nities, and South American forests have typically several abundant species of Canrhon (Chapter 12). The most striking difference among the continents is in f w d selection. In South America and South-Fast Asia, many species use both dung and carrion or are entirely restricted to carrion, whereas the vast majority of African forest species are coprophagous (Table 19.3: c a m p c n g localities 2, 3, and 5, for which best data are available, x2 = 20.6, df = 2, P
1

2

111

19.2. THE INSECT COMMUNITY IN

CATTLE DUNG

Cattle dung is currently available in large quantities in open grasslands virtually everywhere in the world, allowing comparisons between species assemblages that were drawn from different ecological and evolutionary backgrounds to the same resource. The three main kinds of insects in cattle dung are dung beetles, dung flies, and predatory beetles (Chapter 1). The interaction between dung beetles and dung flies is competitive and typically asymmetric. Dung beetle activity increases the mortality of Hy eggs and larvae (Tyndale-Biscoe and Hughes 1969; Bomemissza 1970% Blume et al. 1973; Sands and Hughes 1976; Doube 1986; Fay and Doube 1987), and where tunnelers and rollers are the dominant dung beetles (subtropical and tropical grasslands). dung-breeding flies have a reduced chance to breed because of resource preemption by beetles. However, the experiences with introduced dung beetles from Australia (Doube 1986; Chapter I S ) and the southern United States (Palmer and Bay 1984; Legner 1986) indicate that a nearly complete removal of dung by beetles is necessary to suppress the density of dung-breeding flies to a low level. The interaction between Aphodius (dwellers) and dung-breeding Hies is more symmetric: Ily larvae can complete their development by the time Aphodius larvae hatch in droppings, but the immature stages of flies are vulnerable to disturbance by adult beetles. Low or only moderately high abundance of dung-breeding Flies in many temperate regions, where Aphodius dominate among dung beetles, cannot be attributed to competition with beetles, but it is known that predatory beetles often inflict heavy mortality on fly eggs and larvae (Hammer 1941; Macqueen and Beime 197%; Valiela 1969; Olechowicz 1914; Roth et al. 1983; Doube, Macqueen, and Fay 1988). The often large numbers of small Oxylelinae (Staphylinidae) beetles in cattle pats (Koskela 1972: Hanski and Kaskela 1977) probably do not have a significant impact on either dung beetles nor on dung flies. Their feeding habits are not well known, but they use some decomposing material that is present in droppings. Table 19.4 describes the species composition of the beetle community in-

I

3

-

-

I

28

43

1

-

14 31

6

-

2u

-

1 3 4 147 20

3

3 10

_

8U

6

-

5

5

16

4

3U

3 3

I1

9 4

4

21 79

9

7

8

4 _

2

5

-

t

4

-

4 8 I1

15 31

64

4

2

2

Nme: Lucalifier and data for North temprmc: I . South Finland IHanrki and Koskla 1977: includes f u n s spccic~): 2. Minnerue. USA ICervcnka 19861; Su6rrop;col Ausllmllo: 3. Rackhoinphn (Chapter s):Su6trop;cul A j r i m : 4. South Africa (Beman 1981): 5 . Sovth Africa (Davis ei al. IYSR: Clepkr s. repionill study. iiidvdes uc,ullatidal: 6. Niger ~Chapiur11. x t n - d e s c m : l i q , r c d Afiir.0: 7. ivory Coast (Cliapcer Y figures for families other than Scarabaeidae m from i( shun-term swdy usma pilfalls bnied with human dungl: Troiirol Amcnco: 8 , Fnnch Guirnr I Y . Canibefott. unpubl.1.

habiting cattle pats in different parts of the world. Comparable data are available from Europe, North America, Africa, South America, and Australia, which differ in terms of climate, original and modified habitats suitable for large herbivorous mammals, the species pool of large herbivores and dung beetles, and geographical history. Paralleling the extent of natural grasslands, the native fauna of large herbivorous mammals is very rich in Africa but poor in South America. Continentwide comparisons reveal certain palterns in the beetle community inhabiting cattle pats (Table 19.4). First, there are temperate regions. including most of Europe, where an extremely species-rich community of beetles and flies (Skidmore 1985;Chapter 5 ) colonizes cattle pats, with up to two hundred species being present at one locality, including dozens of predatory beetles that a n microhabitat generalists. The characteristic feature of fhis community is the great diversity of both dung-breeding flies (Table 5.1) and predatory beetles. Staphylinidae appear to be more diverse in Europe than in North America (Table 19.4: for North America see also Harris and Blume 1986). but this may be partly due to the better-known European fauna. The numerical and functional importance of dung beetles increases with decreasing latitude, with a shift from the domi-

viiwisnv

65E

.

3dOtlfl3

t

360

’

Chapter 19

where a few species have become hugely abundant, for example in Australia? Does predation mediate local coexistence of dozens of dung-breeding flies in Europe?

ROLLERS

OLD MODERN

19.3. MECHANISMS AFFECTING SPECIES RICHNESS Our purpose here is to return to the three processes that were discussed in the three previous chapters, and lo relate lhese processes to the observed panerns in species richness. Interspecific competition (Chapter 17) is often severe in dung beetles, and makes coexistence of similar species more difficult. Of h h e mechanisms operating in the opposite direction, facilitating coexistence and maintaining species richness in local communities, we have reviewed spatial aggregation (Chapter 16) and resource partitioning (Chapter 18).

LLL

SMAl

nL

LARGE AUSTRALIA AUSTRALIA NEOTROPICS NEOTROPICS AFRICA AFRICA

Competirion and Species Richness Two tribes of dung beetles, Canthonini (rollen) and Dichotomiini (tunnelers), are considered to be older than the others (Chapter 4). Canthonini are well represented in South America, Madagascar, and Australia, while Dichotomiini are really dominant only in South America (Table 4. I). In Africa, where the number of extant dung beetles is highest, the old tribes have relict distributions (Chapters 4 and 9), suggesting that they are in the process of being replaced by the more modem tribes. Fig. 19.3 gives the numben of dung beetle species in South America, Airica, and Australia, separately for the old (Canlhonini and Dichotomiini) and more modern tribes, and separately for the four functional groups of small rollers, large rotlers. small tunnelers, and large tunnelers (Plates 4.1 to 4.8). The species are relatiiely evenly divided among the old and more modern tribes, and among the four functional groups (Table 19.5); but there is a significant interaction between the age of the mibe and the functional group, and a nearly significant interaction between the age of the tribe and the continent (Fig. 19.3, Table 19.5). These interactions support the idea that the more modem vibes are replacing the older tribes of Canthonini and Dichotomiini. One might expect that species number is smaller in communities in-which competition is regularly severe than in communities in which compelition is weak or nonexistent. This is not generally the case in dung beetles. The most competitive dung beetle assemblages occur in lmpical forests and in subvopical and tropical grasslands (Chapter 17), but these biomes also have the most species-rich communities of dung beetles. In extensive tracls of tropical forest on all three continents, one locality has some 50 to 60 species of dung beetles (Section 19. I), while comprehensive surveys of submpical and tropical grasslands in Africa have uncovered some 120 to 140 species per locality in West

TUNNELEF

rmfi 19.5

Analysis of variance lor the nuniben of differeni kinds of dung beetles on differenr Conlinenla.

ss Continent (AI Funclionil group ( B I Old “5 ,mudcm IC) A’B A*C B T A’BT TWnl

2

F

P

6.01

2.48

12.74 3.52

0.007

3 I 6

0.03 1.28 1.84

0.14 0.91 3.92

0.718 0.543 0.082

4.43

6.24

0.028

2 3 6

23 I

1.41 17.48 67.99

0.089

362

'

Chapter 19

Africa (Chapter 9), East Africa (Kingston 1977; Cambefort, unpubl.), and southern Africa (Chapter U; Edwards 198Ua). In northern temperate regions. where competition among dung beetles is generally weak, local communities have typically some 20 species of Aphodius (Chapters 5 and 14). The lalitudinal change in species diversity is naturally affected by many factors and may tell us little about the consequences of competition. Of the mechanisms that may facilitate coexistence of competing dung beetles, we have examined aggregated spatial distributions (Chapter 16) and resource partitioning (Chapter 18). We shall now consider the likely contributions of these mechanisms to species richness in dung beetle communities.

Aggregation and Species Richness The lottery and the variance-covariance models reviewed in Chapter I yield different predictions about the number of regionally coexisting species: in the lottery d e l , the best competitor will ideally dominate the community, and in practice we would expect low species richness. In contrast. variance-covariance dynamics facilitate coexistence, and many similar competitors may coexist in spik of competition. Of the functional groups of dung beetles (Chapter 3), dwellers and small tunnelers best fit the assumptions of the variance-covariance model, while rollers and large tunnelers have dynamics appruaching the lottery model (Chapter 17). If eveqthing else were equal, we would expect lowest species richness in rollers and large tunnelers. and highest species richness in dwellers and small tunnelers. At the global level, there a x some 1,650 species ofAphodius, which comprise the bulk of the dwellers. However, competition is not generally strong in northern temperate communities (Chapter 17). where Aphodius dominate (Table l9.l), and it would be misleading to compare them with the mostly tropical rollers and tunnelers. In the old tribes of rollers (Canthonini) and tunnelers (Dichotomiini), there x e about equal numbers ofipecies, about 800 species in bath but in the modern tribes the tunnelers outnumber the rollers by a n order of magnitude, with about 3,500versus 350 species. Thus, while lhe modern tribes have been replacing the old ones in Africa and Eurasia, species number has apparently decreased in the rollers but substantially increased in the tunnelers. Thedifference is particularly striking in small species (Fig. 19.3): modern small rollers, although now entirely dominant in most of Africa, number only about a third of the extant species of Canthonini, the old rollers, while in small tunnelers there are twenty times more species in modern than in old tribes. This difference is consistent with the prediction based an lottery dynamics in rollers and variance-covariance dynamics in small tunnelers. Turning to a smaller spatial scale, local communities in Africa have typically five to ten times more species of tunnelers than rollers (Table 19. I). Fig.

Species Richness

'

363

19.4 shows the rank abundance distributions far the rollers and the tunnelers in six West African localities, expressed both in numbers of individuals and in biumass (the latter reHects better than the former the impact of the species in resource use; data from Appendix B.9). It is apparent that while in rollers a few species strongly dominate local communities, the distribution of species abundances is more even in the tunnelers. Furthernkore, there are guilds of apparently very similar yet coexisting tunnelers, while coexisting rollers show striking size differences (Chapter 18). supporting the hypothesis that two or more similar tunnelen but not rollers may coexist in the same community. It is not clear why the old tribes of tunnelers and rollers show a different pattern. It would be instructive Io c o m p m the population biology of representative species of old and modem rollers. The fact that the old tribes in Africa have largely been replaced by the modern ones, and now remain primarily in southern Africa and Madagascar, suggests that in Africa members of the modem tribes are better competitors than species belonging to the old ones. In conclusion, the difference in species richness of small rollers and small tunnelers is consistent with the mdiction based on the difference in their pop-

ROLLERS 50

INDIVIDUALS

40

'I Yd

a

0

TUNNELERS

I

5

10

15

20

INDIVIDUALS

30

0

5

10

15

20

RANK ORDER OF SPECIES Fig. 19.4. Rank abundance lists fur rollerr and tunnelem in West African savannas in terms 01. ihunibcrs of inclividuils mid biomass (data fmm Appendix B.9).

I 364

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Species Richness

Chapter 19

dation dynamics, with rollers fitting the lottery model of competition better, while small tunnelers fit the variance-covariance model better. Resource Partitioning and

Species Richness

A possible explanation for the observed trends in species richness (Section 19.1) is resource partitioning: species number is higher where the range of resources is greater, or where for some other reason the means of dividing the resources are better. Of the trends in species richness described in Section 19.1, the increase in species number with decreasing latitude. which is especially dramatic in forest species, is most probably related to resource partitioning. One obvious example is the presence of about equally large guilds of diurnal and nocturnal species in tropical savannas and forests, and the huge size variation of tropical dung beetles in comparison with temperate beetles (Chapter 18). Different soil types have different but overlapping assemblages of dung beetles (Chapters 6, 8, and 18). which increases regional species richness. On the other hand, there is no strong evidence to suggest that panilioning of different resource types is important in maintaining species richness, apan from the broad difference between species specializing in omnivore and herbivore dung, and the very specialized species living in tropical forests. In southern Africa (Chapter 8) and West Africa (Chapter 9),the game parks that have a range of wild herbivores and the pastoral systems that have only cattle show similar levels of species richness (previous section). The contrasts in dung beetle diversity between African savannas and forests with rich and poor mammalian faunas (previous section) may have more to do with the aninunl than diversity of dung. The recent declines in regional species number in northern temperate (Chapter 5). southern temperate (Chapter 6). and tropical biomes (Chapler 9) may more to do with the changing management of cattle and other domestic. mammals than with changes in their relative numbers. Intensively grazed pastures may be generally unfavorable for rollers, which may explain the decline and disappearance of many large species in southern Europe in this century (Chapter 6). The interaction between breeding behavior and sensitivity to soil type (Section 17.2) suggests that species number declines when the, environment becomes more homogeneous in terms of soil type.

.OF

19.4. SUMMARY

This chapter has summarized patterns in species richness of dung beetles and the mechanisms underlying these patterns. Local species number of dung beetles in open grasslands increases from about 20 in northem temperate pastures

.

365

to about 120 in tropical grasslands (10 and 50 species in a random sample of 300 individuals, respectively). The species composition changes dramatically with latitude, from near complete dominance of Aphodius (dwellers) in nonhem temperate regions, to a varying mixture of tunnelers and rollers in tropical biomes. The number of species of dwellers does not decrease with decreasing latitude; but their decreasing relative abundance is due to compelition with tunnelers and rollers, and possibly to a faster rate of drying out of droppings in tropical than temperate climates. making the dweller life history inferior in the tropics. Species nchness of dung beetles is generally related to ni;lliimalian species richness, but cattle dung alone appears to suppon as many species in tropical grasslands as a range of wild herbivore dung. Canle dung is presently available in large quantities all over the world, allowing comparisons among species assemblages that were drawn from different ecological and evolutioilary backgrounds to essentially the same resource. Three types of insect conimunities occur in cattle dung: (I)a species-rich community of dung beetles (mostly Aphodius), dung-breeding flies, and predatory beetles in northem temperate regions; (2) a species-rich community dominated by dung beetles (tunnelers and rollers) in grasslands in Africa; and (3) species-poor communities in regions lacking native large herbivores and hence have only few insects adapted to use cattle dung, In some of the latter regions, for example in Australia, some dung-breeding flies have increased enormously in the absence of effective competitors and natural enemies. Patterns in global species richness suggest that the modem tribes have negatively affected species richness in the oldest tribes, Canthonini and Dichotomiini, which are now well represented only in South America, Madagascar, and Australia. However, the mm1 competitive extant dung beetle assemblages in tropical grasslands have also the highest numbers of species. up to 120 or more. Two mechanisms that contribute to coexistence of large numbers of competitors are aggregated spatial distributions and resonxe partitioning.

Epilogue

CHAPTER 2 0

Epilogue Ilkka Hanski

DUNGBEETLe ecology has reached an exciting stage. New data are accumulating and new ideas are being contemplated. An ecological context is emerging into which old and new pieces of natural history observations fit. Yet so little work has been done in population and community ecology of dung beetles that it is easier to ask new questions than to review old ones. While assimilating the data and the ideas presented in this volume, my two recurrent feelings were that we are still in the dawn of unraveling many of the more significant ecological questions about dung beetles, but also that many of them are tractable and are just a matter of doing the right thing in the right place. 1 have compiled below a list of seven observations, concepts. and ideas that are worthy of further study. 1. COMPETITION IN THE DUNGINSECT

COMMUNITY

The key interspecific interaction discussed throughout this hook is competition. Although there is no doubt that competition occurs i n many dung beetle populations (Chapter 17) and hdS probably played a signilicant role in the assembly of local communities (Chapter IS), there is a need for experimental field studies lhat quantify the population-ecological consequences of competition, and a need for experiments that deal with entire dung insect communities. The balance between the three main components of these communities. consisting of dung beetles, dung-hreeding flies, and predatory beetles, varies from one biome to another (Section 19.2), but the direct and indirect interactions among them remain little studied (for some interesting examples see Valiela 1969, 1974: Doube, Macqueen, and Fay 1988). A better understanding of these interactions has great practical value in the biological control of pestilent dung-breeding'flies (Doube 1986; Legner 1986: Chapter 15). Considering dung beetles in particular, it would be informative to conduct experiments in which certain types of beetles were excluded from droppings, for example, by taking advantage of the striking differences in beetles' diel activity. Introductions of foreign dung beetles offer unique opportunities to conduct interesting experiments and to make valuable observations. The species that have been most successfully introduced so far are relatively small,

.

367

multivoltine, high-fecundity species (Chapters 15 and 16). while many natural dung beetle communities in subtropical (Chapter 8) and tropical grasslands (Chapter 9) are dominated by large, univoltine. low-fecundity species with highly evolved parental care-the classical K-species. What happens when the latter species are introduced into new areas and have had sufficient time to become abundant'? Do they outcompete or, more likely, significantly suppress the abundance of the mare r-type species introduced earlier? Some observations from Australia and New Zealand demonstrate that it takes dozens of ycars bclirrc the largc, low-lecundity spits bccun~cabundant [Chapter IS). 2. TYPE 1 A N D TYPEIIDUNGBEETLES

To be a successful competitor a dung beetle needs to possess two traits: it must

be able to locate a resource patch quickly, before other beetles have had a chance to remove all of it, and it must itself be able to remove, to a safe location, a sufficient amount of resonrce for breeding. Paradoxically, some beetles appear to do just the opposite: they arrive late at droppings and provision their underground nests slowly. or they breed in droppings, remaining vulnerable to disturbance by other insects. I shall denote the two kinds of beetles as Type 1 and Type 11 species, respectively. The other classificatims of dung beetles described by Doube (Chapter 8) and Canibefart (Chapter 9) are refinements of the basic dichotomy between the Type I and Type II beetles as defined in Table 20.1. Type 1 beetles are superior competitors in preemptive resource competition. and their dynamics often fit the lonery model (Chapter I). They are adapted IO use fresh dung as fast as possible. while Type IIspecies are adapted to use oldcr dung. The distinction between Type Iand Type 11 species is rclnted to the idea of species being either efficient in locating resource patches bur inefficient in exploiting them, or vice vena (Kotler and Brown 1988). Small. high-quality omnivore droppings are often entirely dominated by Type 1 beetles, whereas the larger herbivore droppings have typically both Type 1 and Type II beetles. Mast rollers and the fast-burying tunnelers (Chapter 8) are Type 1 species, while the slow-burying and many small tunnelers, dwellers. and kleptoparasites are Type 11 species. Type 1 species are superior competitors because they are fast in securing resources for their exclusive use. Type 1 beetles are often but not always large, while Type 11beetles are typically small or relatively small. In tunnelers, large size allows fast burrowing and fast remove1 of large quantities of dung underground. In rollers, large size is an advantage in interference competition (Section 17.1). The cost of large size is reduced fecundity (Section 17.2). Many Type I beetles invest much time and energy in constructing their nests in places where disturbance by later-arriving beetles is not likely. Rollers bury their brood balls some distance away from the food source and effectively

. .

1

... .~ .

368

'

TARLE

Chapter20

Epilogue

20.1

A Simple Clasiificitim ofdunp, heeller into two basic types

Afwibure

Type 1Berrlrs

Represenled by

Mm1 rotten;

t""neterS

Type I/ Beerlea

fart~burying Slow-hurying tunnelcrr: dwellers; kieptopara~ sites

Type of resource used

Arrival

at

resource patch

Rate of exploitation

Omnivore and herbivore

Hcrbivirrc dung: species

dung; spccics arc sdnptcd to use fresh dung

arc adsprcd

Fast

Often slow; beetles t ~ a t the e resource patches nut used by 'Type I spccies

Maximally fast

Slow hut perhaps more

LO " I C

older

dung

"~

efficient

Competitive ability

Good

PCX .

Type of population dynamics

Lottery

Variance-cuvoriancc

Fecundity

Low in large species, high in small species

Gcnerdly high

eliminate any disturbance, but the cost is lost contact with the food source. Type I tunnelers may minimize disturbance by digging deep burrows below the dropping. We may expect a negative relationship between the depth of the nest in the soil and the speed of n a t construction. Such adifference is obvious between the fast-burying tunnelers (Type I species) and dwellers (Type 11species), but studies on different species of tunnelers would be especially interesting (some supporting observations are described in Chapter 6 on Onlhophogus and by Edwards and Aschenbom 1987 on Oniris). Other open questions include: Why are some Type 1 beetles very large and have extremely low fecundity and extensive maternal care (e.g., Kheper, HeliocopriJ), while other Type 1 species are small and have high fecundity and no or only limited rnaternal care (e.g., Sisyphus, Digironfhophagusgazeflo)?And are Tvoe.ll beetles more efficient in using the resources than Type I beetles?

3. SOIL TYPEA N D DUNGBEETLES Both rollers and tunnelers are more or less affected by soil characteristics, and, as suggested in Chapter 17, the best competitors, the Type I beetles (Table 20.1). have the disadvantage of being generally more affected by adverse soil type than the inferior competitors. The weakest competitors, the dwellen, are

'

369

the least affected by soil type, since their entire life cycle is completed inside llie dung pat. Tlie trapping studies by Doube in southern Africa have praduced interesting results on the effect of soil type un different functional groups of dung beetles (Chapter 8). More such observations are badly needed. It would be interesting to obtain results not only on a large spatial scale (as in Table 8.3) but also on a small scale, comparing the use of dung pats located on patches of different types of soil. Small-scale patchiness in soil type may be an important factor muintaininp. high species richness in the nwst competitive dung bcctle coniinunities by preventing Type 1beetles from dominating the community. Inforniative experiments Io tesl this hypothesis would be straightforward to conduct. 4. AGGREGATED SPATIAL D~STR~BUTIONS

One of the major organizing concepts in this book has been the distinction between two kinds of competitive dynamics: the lottery and the variance-covariance dynamics (Chapter I). In reality there is not a sharp distinction between the two but rather a continuum, and the question is where, along this continuum, different kinds of dung beetles are located. In general, large and Type I beetles lit the lottery model better, while small and Type I1 beetles tit the variance-covariance model better (Chapter 16). Note that variation in the quality of the dung pat or the soil below it may also generate intraspecific aggregation (point 3 above). but such aggregation is conceptually different from the one considered here, which occurs independently of any variation in the quality of resource patches and is not due to adaptive behavior, as the first kind of aggregation may be. In practice. however, the two kinds of aggregation may be compounded. Different chapters in this book have reported contradictory results an the likely importance of aggregated distributions in dung beetles. Doube (Chapter 8) concludes that such aggregation is unlikely to be of any significance in South African grasslands, while Cambefon (Chapter 9; seealso Chapter 16) finds much aggregation, and interspecific patterns related to aggregation, in West African savannas. One reason for these conflicting results is probably a difference in the spatial scale in the two studies, the replicate dung pats being located only meters apart in Doube's study but dozens of meters apan in Cambefort's study. Doube (Chapter 8) is concerned with large tunnelers, while Cambefort's (Chapter 9) analysis includes many kinds of species. As explained above and in Chapter 16. aggregation is not expected to be an important Factor in the largest tunnelers. whose dynamics approach the lottery model. Another question is what is causing the observed aggregation of species? One passible answer is that aggregation reflects differences in the detectability

I 370

’

Chapter20

of dung pats; another possibility is that aggregation is due to the behavior of the beetles colonizing the pats. These two mechanisms may both contribute to aggregtion. but note that the difference between large versus small species, and between Type I versus Type 11 species, supports the second hypothesis. Consistent patterns of interspecific aggregation (Fig. 5.3) also support the behavior and biology of species as determinants of aggregation. Experimental studies are needed to elucidate the causes of intraspecific aggregation.

Epilogue

’

311

be interesting to know whether kleptoparasitism varies with the depth of the nest and, more generally, what features of dung beetle breeding behavior are possibly affected by kleptoparasitism. Predation might be expected to be heavy on adult rollers, because most of them are diurnal and very conspicuous while rolling dung balls. Systematic observations would be valuable, provided that the observer takes care not to scare off the potential predators. Unfonunately, in many regions of the world most of the original predators may have alrcady gone extinct or are scarce.

5. POWLXIIONBIULOOY01: KoLLus Rollers present many fascinating and little-explored problems in population biology. Questions about breeding behavior, parental cooperation, sexual selection, and so on are largely beyond the scope of this book (for a fine example, see studiesonKhepernigroueneusbyEdwards 1988a.b; Edwardsand Aschenbom 1988, 1989). Interesting population ecological questions focus on the kinds of balls made by rollers. Do beetles generally make balls as large as is economically feasible? Does the type of dung affect ball size, as suggested in Chapter 17? A comparative study of the ability of rollers to prepare and roll dung balls versus the ability to dig burrows would be most rewarding, and should not be too difficult to carry out, as both the type of dung and the kind of soil offered to beetles may be experimentally varied. Also of interest are the differences and similarities among rollers belonging to the old and modem tribes (Chapter 4). There are only a few small, modem rollers. most of which are very abundant, and a larger number of mostly uncommon old, small rollers. Does this contrast reflect a difference in their population dynamics? For example, do the modem but not the old small rollers fit the lottery model of competition? The pattern between the old and modem species is essentially reversed in large rollers, as there are very few old, large rollers (Fig. 19.3). It is possible that the o1d;large mllers have mostly gone extinct.

6. PREDATION ON DUNG BEETLES While competition is the dominant interspecific interaction in dung beetles, it would indeed be surprising if predation were as insignificant as the meager information now available suggests. One could imagine that large dung beetles that often occur in ,huge concentrations would present an excellent food source for many predators. Many of the patterns examined in the previous chapters may be related to predation, including the cases of probable mimicry in African rollers (Chapter 9) and the generally nocturnal habits of large lunnelers. Kingston and Cae (1977) have suggested that predation by the ratel Mellivoru copensis may explain the great depth in the soil, down to 120 cm, at which the huge Heliocopris dilloni excavates its breeding chambers. Kleptoparasites are often abundant in the nests ofHeliocopris (Table 9.3). It would

7 . TEMFURAL SrnulLI-ru OF CUMMUNITIES Several chapters in this book have examined temporal stability of dung beetle populations (Chapters 5-9, 15). Doube (Chapter 8) and Cambefort (Chapter 9) reached opposite conclusions about beetle assemblages in African subtropical and tropical grasslands. According to Doube (1987), there is great variation in relative abundances of species, even in the relative abundances of different functional groups of beetles (Chapter 8), while Cambefort (Fig. 9.7) found striking constancy of relative abundances over a period of eight years. The reaon for the disparate results can hardly be due to differences between subtropical and tropical grasslands. A possible explanation, however, is that Doube’s community of beetles using herbivore dung on clay-loam soils in a game reserve has many Type 11 species (Table 20.1) and is apparently much less competitive (Chapter 8 ) than the community of largely Type I beetles using omnivore dung in Cambefort’s study. These results suggest that the structure of the most competitive (Type 1) dung beetle communities is more constant than the structure of communities not so strongly and consistently affected by competition. consequently including many Type I1 species. Cambefon’s results are in agreement with the classical competition theory, which assumes a stable equilibrium point (Chesson and Case 1986). Temporal v a r ation of populations on clay-loam soils leads to discontinuous competition, which may facilitate coexistence, assuming that different species have some differences in their responses to fluctuating density-indepenqent mortality or whatever factors ure promoting instability. Surprisingly. the two communities that have apparently different 5011s of mechanisms allowing coexistence are still about equally rich in species.

.

.

~..

I ~~

Appendix A

APPENDLX A gives data on resource availability at the study localities that are dcalt with in detail in the chapters in Part 2. and for which Appendix B gives lists of spccies of dung beetles and ecological information. The data in this appendix are not equally comprehensive for all localities, nor can the data be presented in a uniform format. Appendix numbers refer to corresponding chapters. APPENDIX AS 0.ford. E,,glmul. ,,"rr/, re,nperure region. ,

Thc lergc hcrbivorcs cvnsist of cattle in the pastures and deer in the woodland (Hmski 1979).

A I W : N I ~ IAX. 6 s<,,,llJ<,r#t F'm,,ce, ,sonr/, le,,,/""fe

regimr.

I n the s m d l arm of thc Garrigue north of Montpellier where most of the ecological studies on dung beetlcs have been conducted, some 6,700 hectares are used for sheep grazing. of which iibout onc half is used intensivcly. The number of E W ~ Spresent in 1982 war 4,410. Thc shccp wcrc distributcd among twelve flocks, three of which wcrc lcss than 150 hcad in s i x and thrcc murc than 450 head. A herd ofcattle (LOO animals) was cstablishcd in llic silmc arcs in 1984. APPENDIX A.7

Srr,zrrr Crui A
APPENDIX A.8 Mh:i Gamc Reserw. .sotdw,-ri Ajiricu, .ssbrropical s u v u ~ ~ ~ ~ u . ~ . Thc tupgraphy, vcgetatiun covcr, and fauna o f t h e Mkuzi G a m Rcservc have been dcscribcd i n Edwards and Aschcnboru (1988) and Osberg (1988). The size of lllc ~CSCIYC is 25,000 ha. It is prcdominantly Ilat, consisting of open bushvcld with small areas of opcn grassveld and dense bush. Soil types range from deep sand to heavy clay. Thc mainnis1 fauna is diverse and it included. in April 1984, 8,100 impalas (45 kg), 820 icbras (310 kg), 180 giraffes (1.200 kg), 40 white rhinoceros (1,800 kg). 100 black rhinoceros (1.100 kg). 1.400 wildebeests (220 kg), 680 kudus (145 kg). 3.100 nyalas (85 kg), and 480 warthogs (66 kg), as well as some smaller antelopes. baboons (23 kg). vervet monkeys (5 kg). small mammals. and a few hyenas (75 kg), cheetahs

374

'

AppendixA

AppcndixA

(40 kg), and jackals (7 kg). Most species occur throughout the reserve. Zebras and rhinoceros produce coarsetextured herbivore dung. Wildebeest dung is similar to that of small cattle. Giraffes and antelopes pmduce pelleted dung. Mammals in Mkuzi Game Reserve.

A r r a ~ ~ Ai .xII

.r,,,, Lurruo f h r y C m s r )

Mokokou (Gobon). tropir"1Jiwesr.s ;,I AJ\fiia.

Biomass fkglhu)

Dunl: Prrx/rrctio,z* (kgiholyr)

38.4 30.3

750 400

T y p e ./Mr~rrrr~rol.s

TOP

Makokou

II

L0,lllO

Kudcnls

10

17 34

Pholidoln C;imivor;i Proboscidians Hyracoidea Arctiodilctyla

3 13

13

4 10 3 3

I

I 16

I

I 12

0

APPENDIXA.9

Numbcr of spccics

55

81

Ivory Cousl, West Africa. rropical swannos.

Biomass (kglha)

Type of Mammals Large herbivores (>ZOO kg) Medium-sized herbivores (>20 kg) Small mammals ( < 2 kg)

unknown

* Rough estimate.

TABLE A.9

Abokouamekro Kakpin Now

Biomass (kgllioj

Type of Mammals

Dung Production (kgllrrrlyr)

Large herbivores Medium-siied mqmmals

2 20

40 300

Large herbivores Medium-sized mammals

I40 20

2,900 300

Large herbivores Medium-sized mammals

50 35

I ,000 525

1

Primates

ill.

Mammals in Ivory Coast tropical savannas.

hmto

375

TAHLE A. I I Numbcrr uf iiianmilliiln spccier and their estimated bioinasses in three forest localities.

TABLE A.8

tocaliry

'

No data available for small mammals.

APPENDIXA. 10

Durnogu-Bone Narional Park, North Sulawesi. tropicrrl foresrs in Soailr-Eollur Asici. Larger mammals are represented by the abundant crested macaquc, Macacrr rtigru; thc Sulawesi wild pig, Sus celebensis; the babirusa. Babyrousa bubyyrusro; thc Sulnwesi dwarfed buffalo (moa), Bubalur depressicornis; and the introduced dew, Crrvtc.s iimorensis (Muss& 1987). Small and medium-sized mammals am very abundant. Durden (1986) collected ca 15 species of rats within a small area of lowland forest, obtaining the rough density estimate of 20 individuals per IO0 trapnights for the small and medium-sized mammals (Durden. pers. comm.). This is a very high density for tropical forests. l l e only native carnivore is the civet, Mocrogolidia musschenbroeki (Musser 1987). Small lizards, Sphenomorphusamabilis (Muller) andS. temmincki (Dumeril and Bibron), are conspicuously common in the forest floor.

3

30-50

1

5 26

2 5 4

5-10

7ii$.A n u n y m ( 1 9 7 9 ~and ) Mcrz (1982); Malolorr, Anonylla (19X7);Lcz,rltO. (1974).

Bourliere C l

APPENDIX A.12 &WO

Colwmlo Islmd, P U I I U ~ rropicul N. firesr it2 Souflr America.

,

Tl'ntli.a A.12

Estimacd duiig production of nonvolant terrestrial mammals. SpeciPs Tupirpi,.rrs bainlii 0d"c"iIms \~irginiul!~f5 Tuya,s.~rrI(IJuctt

Mrrrrmu rmr#ir.rr,,u F
Afrles ,qeo/frqi Do,v?pr,.s rw,wwairzcrirs E i m borbcro

Tur,rar,d,ru lIlr.ricrrrlu Clrr,l,,ep,l3 h<,J,,l"lllli Coe,idoa r-uilischildi

Namo nuricu PermJluwu Bradypus itflrsc'rlas Ccbus capucirzas

Do.r?/~rortopsncfura

Weight fkX)

300.0 40.0 23.0 15.0 13.5* 8.0 5.5 5.0 5.0* 4.5" 4.5* 3.5 3.0* 3.0 3.0* 2.8 2.6 2.0

Populoriori

Biomtars

Size

(kg/llU)

8 10 I40 30 12 600 1,300 14

I.53 0.25 2.0s 0.29 0.10 3.06 4.55 0.04 2.55 0.07 0.23 3.34 0.29 0.69 0.57 14.27 0.23

800

25 80 1,500 150 364 300 8,000 140 I .5m

1.91

Dimg Producfion (kg//IU/Yr)

2.23 0.68 (a) o s 2 (b) I .28 0.46 17.87 (c) 54.20 (d) 0.26 16.93 0.48 0.90 ( e ) 3.05 (f) 2.32 5.53 4.57 13.02 ( f ) I .94 14.64 (C)

I

376

I

AppcndixA

Appendix A

TABLEA.12 (cont.) Species Philander opossum Sylvilagus brasil1ens;s Didelphis marsupialis Aotuv rrivirgatus

Proechimys semispinosus Saguinus geoffroyi Caluromys derbianus Sciurus grrrnarensis Cyclopes d i d a c t y h Heteromys desmoresrianus Oryzomys spp. Marmosa robinsoni

. 317

"*NOISE

Weight

6%)

Populatioit Sile

1.4 1.3* I .0 0.8 0.8 0.8 0.35* 0.25 0.23 0.1 0.07 0.06

200 I00 700 40 2,800 40 300 2,700 -.

I ,000 2,000 400

Biomass Whal 0.18 0.08 0.45 0.02 1.43 0.02 0.07 0.43 0 . 13 0.06 0.09 0.02

Durig Pwducti,,,, (k,q/lraiwJ 1.91 0.87 5.42 0.26 18.70 0.26 1.24 X.65 11.24 ( c ) I .6Y 2.90 0.68

~

Notes: Weights fmm Eisenberg &Thorington (1973). except tho% marked with an asterisk (*), are averages computed from Nowak & Paradiso (1983). Eatimutes ufpopulvtiun s i x from Glanz (1Y82). wilh the exception of Herwornyr. which is from Eiscnhcrg & 'I'hwinglon 11973). Dung production given in kg dry wcighllhccrarClyeu. Unlcrr otherwihc indicntcd. dung pmduclion estimated fmm body weight ( W i n 81. using quation y = 0.85 W - " " (Blucwcirs ct al. 1978). Estimates cunvened IO dry weighl assuming 50% water c ~ n t e n t .(a1 McCullaugh (1982) gives average daily fecal output of 300 g dry weight fur while-mild deer. 0d0coilt.1~virg;~iu,,,,.~. (b) Zervanos & Hadley (1973) calculated fecal w*er Ius$ of U.21% body weighllday (wilh rccal waler mntent averaging 75%) for collared peccary, T o y a m rajacu. whlch corrcspunds tu fccnl output of 0.07% body weighuday (* weight). (c) Assuming 50% digestive enicicncy. Sniythe el al. (1982) estimated that a 3 kg agouti. Qr<~yprocluPUIII'IUILI. and a 9 kg piaca. A ~ u u i rp < t ~ < , , consume 128 and 290 g dry weight of loudiday. mspcclivcly. There villucs correspond IO acrecation rates of 21 and 16 g dry weightlkg bady weight per day. respectively. (d) Nagy & Miltun (1979) calculated that howler monkey, Alouqifa polliota, consumes an average uf 53.5 g dry masslkg of monkey psr day, of which 61% is voided a5 feces. (e) Montgomery (1985) estiniirtcd an o ~ t p u of t 80 g dry dung every two days for banded anteater. Taomondua rnericmo, with avcmge weight of 3.73 kg. Adult silky anteaters. Cyclopes didactylus. produced an nvcrage 01' I . 17 8 dry dung per day. (f) Montgomery and Sunquist (1975) determind a dclccnion rate 01 2 . 5 g dry fecedkg body weight per diry far three-loid sloth. Brodyplypw itfuuwrrrus. Similar mtcs arc a s s u ~ ~ ~ e d for the two-toed sloth. Choloepus ho/fmonni.

which

APPENDIX A.13 Niamey, Niger, arid regions. Cattle (zebu) are kept by pastoral populations. APPENDIX A. 14 Vanoise Narionnl Pork, France. and Grimns Nariuwl Park. Switzerland. montane regions.

k r g e lierbivures (>ZOO kg). Biomass 33.0 kg/ha (dala for 1979). Cattle(2.700) remain insidc the park limits (52.839 hnj from May to September, occupying 62% of the loWl area available.

Medion-sired ma~nrnals(>20 kg). Biomass 37.9 kg/ha on average. Domestic mammals (32.6 kgiha, data for 1979) remain inside the park limits from May to September. Wild niamn~ds(5.3 kgiha, data for 1986) remain in the park all year round, using 90% of its tovsl arcs (10% is icc and permanent snow). The most iniponant medium-sized inammals arc shecp (18,000; 32.0 kgiha); goats (540; 0.6 kg/ha); wild goats (Copra i6ex. 70U; 0.9 kgiha); chamois (Rupicapra rupicapm, 4,700.4.4 kgiha). Sn~ollnt~znrn~~t1.s (<20 kg). Biomass is unknown. The main small mammals are mar11101s (Munnota m d n n o t a , scvcral thousand) and hares (Lepas tinridus, scarce). CRlSONS

Large herbivores (>200 kg). Domestic mammals are forbidden inside the park limits ( 17,000 ha). Cattle and sheep are abundant outside. M~~.diurri-si~rd ~ w ~ n n u(>20 ~ l . ~kgj. Biomass 12.4 kgilra on nveragc (daea for 1985). consisting u i red dccr (Ccrvss elophsr. 2.130; Y. 1 kglhn): chamois (Ridpicapro rifpicapru. 1.230; 2.3 kgiha); wild goats ( C o p r a ibex. 238; 0.9 kgiha); and roe deer (COprenlas capreoltrs, 57; O. I kgiha). Smoll ,rras,nrals (<20 kg). Bionmss unknown. Small mammals include foxes (Vlrlpes vulpes, 70-90 individuals); marmots (Marmota mannofa, 8W1.000 individuals dis-

tributed at fifty sites); and hares (Lepus timidus, 5006M)).

A W E N D ~A. X 15

Badgingurra National Park, southwe~tenzAustralia (3V24'S. 115'27'EJ.

Western gray kangaroo (40 kg), a herbivore, biomass 12-20 kgiha, dung production 16-21 kgihalyr (G.W. Arnold, pcrs. comm.). Other species are present but have low biomass: rabbits, foxcs, cats, naive marsupials (small species). and reptiles.

.

.

.

,.

Appendix B

APPENDIXB gives ecological information for the species recorded in the study localities described and discussed in the chapters in Part 2. See Appendix A for resource availabilities in these localities and the map on pp. 72-73 for their climates. The list of species for each locality is as complete as possible;

APPENDIX

B. I I

but because the different studies have lasted for different lengths of time and have varied in sampling intensity, the localities should be compared with caution. Somewhat different types of information are available for different 10calities, hence the data cannot be presented in a uniform format. The following abbreviations are used where applicable: LE = length in mm; FWt = fresh weight in mg; DWt = dry weight in mg; N/D = diel activity: N, nocturnal (or crepuscular), D, diurnal; LF = larval food:C, coprophagous, S, saprophagous (decaying plant material). APPENOIX8.5 Wyiham Wood, near Oxford. southern Englind, north temperare region.

APPENDIX8 . 6

i

Sovihern France, souih remperuie region. APPENDIX8.7 Sonia Cruz A c u i l m , Mexico. subrropicnl Norih America.

APPENDIX8 . 8 Mkwi Game Reserve, southern Africu. subrropical savannas.

APPENDIX B.9 Purl I Abokouamekro, Ivory C o a t , Wesi Africa, tropical savannas. Part2

SLx savanna localiiies in Ivory C o a i ,

We31Africa, 198041.

N o r r Appendix numbcrs rcfcr to corresponding chapters. Tables relating to lhcsc appcndixcs bcgin un the next page.

TABLE 8.7

Dung beetle samples from Santa Cruz Acatlan. Seaional Occurrence

DWr I , Aphodius 1ividzi.r (Olivier) 2. 0,irhophagns mericmus Bates 3. OirrlrophagrrsIeconrei Harold 4. Phmaeas palliarits Sturm 5 . Phanueas quadridens Say 6 . Phniioeas adoni5 Harold* 7. Dirhornmias curoli~rr~s (Linnaeus) 8. Courorruocs fromicornis (Erichson)'

0.005 0.13 0.011

0.33 0.27 0.19 2.08 0.32

N

LE

N,.,, ,.N

5 360 2.14

i 255 '

6 II 16 135 20 I I 1 I4 26 18 22 1

~

132 0.06 0.80 0.06 0.005 0.11 0.003

8.36 6.35 0.36 3.36 0.36 0.005 0.57 0.005

Mar Apr May

Jun

Jul Aug Sep

IO 2

117 89 5 47 5 I 5

12 52 4 38 3

50 45 2 28 2

44 31

27 17

9 1

3

4 I

3

2

2

6

21 17 IO

2

Ocr Nov NID Hub

12 2

N

P G

N U D D

G G G G P F

D

N

N

~~~

LF C,S C C C C C C C

Norer: Monthly sampler were collected with two traps baited with human dung. each trapping session consisting of 7 days and 6 nights (lord of 72 lrap~nightrand 81 trapdays in 1975). Species believed not IO be breeding locally are marked with an arterirk ( 9Nm.n is mean number of individuals collected per trsp-day (average for whole year), while N",., i s maxirum abundance of the rpecicr (mean number of individuals per trap-day in June). Habitat (Hab) abbreviations:P. disturbed: C.grassland; F. forest.

TABLE 8.8 Habirat associations of dung beetles in

Mkuzi Game Krserve. Average Nlimbrrprr Trap

NlWlhU

Specits

DWr

FG 1 I . Amuhalcur coirl(e.ws Boheman 2 . Kheper clericus (Boheman) 3. Kheper cupreas (.Caslelnau) 4 . Kheper lumurdi (Macleay) 5 . Kheper nigroueneus (Boheman) 6. Pachylomero fernoralis Kirby 7. Scurabaeus galems (Westwood) 8 . SraroboerLi g o v i Casrelnau 9. Scarabueus ramberiunus Peringuey

668 1,135 995 1.216 1.135 1,507 I.000 1,071 500

FG II 10. Allogymnoplearur cunsociar Peringuey 1I . Allogymnopleurus rhalarsinur (Klug) 12. Garrera nirens (Olivier) 13. Garrera unicolor (Fahraeus) 14. Gymnopleurus virens Erichson 15. Odonfoloma spp. 16. Scaraboeur ebrnus Klug 17. Sisyphus alveurus Boucornont 18. Sisyphus calcararus Klug 19. Sisyphusfurcicuiutus Boheman 20. Sisyphus forruirus Peringuey 21. Sisyphus gUZUnK5 Arrow 22. Sisyphus goryi von Harold 23. Siryphus infuscarus Klug 24. Sisyphus mirabilis Arrow 7 5 Sinmhur ruhrur Parchalidis

95 85 207 264 480 I 300 28 12 41 50 II 10 32 40 27

NID

G%

650

N

4

D N

49 50 I00 57 55 56 67 40 58 67 97 54 69 80 0

Cuirghr

I 136 1,189 2,715 3

I03 532

D D D D N N

1,744 3,553 138 35 89

D

1

N D

3 1

607 14 279 28 864 249 2,265 14

D

U

D D

D

D

D D

D D

D

D D

100

100 57 14 34 4 73 51 23 81

Uaplcr

Loam

13.8 0.0 0. I 8.8 31.7 208.7 0.3 8.3 43.0

22.2 0.0 0.0 2.0 27.6 22.0 0.0 0.2 1.3

15.8 0.0 0.0

1.7 0.3 0.0

46.6 0.3 0.0 0.0 0.0

8.8 0.4 0.0 0. I 0.0

0.2 285.8 0.1 0.0 0.3 0.0 0.0 0.0 3.8 0.0 10.8 0.1 0.4 2.0 116.2 0. I

0.4 10.1 2.4 0.0 1.4 0.3 0.1 0.0 24.3

1.4 0.3 7.6 4.4 1.4 0.0 0.0 0.1 12.3 0.0 8.5 1.0 63.1 7.5 11.9 6.5

143.8 0. I 3.9 0.0 4.8 0.0 0.0

Sotid

0.0

3.8 0.3 11.8 9.3 29.4 0.8

0.0

Clay

0.5

0.0

14.3 1.2 3.1 1.3 17.7 4.5 35.3 1.0

TABLE 8.8 (corir.)

Species

26. Sisyp1ph.r seiiiiniilum Gerstaecker 27. Sisyplphur sordidus Bohemnn 28. Sisjphur spinipes (Thunberg) 29. Sisjpher SQ. y FG 111 30. Carhnrsiirs nearpandion Harold 31. Carharsiurpa,idio,i Harold 32. Carharsiirs phiies Kolbe 33. Carharsiiir sp. 34. Carharrias rricornerirs (Ue Geer) 35. Coprir antpifor Klug 36. Copris elpheaor Klug 37. Coprir ernnirlus Klug 38. Coprir fnllncionLs Giller 39. Copris ,nesarm~husHarold 40. Copris near macer Peringuey 41, Coprirpirnrricoliir Boheman 42. Heliorupris nrropur Boheman 43. Hclioroprir k a , n n d ~ a r(FLbricius) 44. Helioropris nrprrozrrs Boheman 45. Mrrmarlmrsias pseiidoopncn Ferriera 16. Meramrl,ors,l,s rrog/m(Yres 1Boheman)

FG IV + VI 47. Cyprochiru~umbiguris (Kirby) i n r e r m d i u (Keichcl 48. Et,oniric~~ll!ir 49. Linrongr,s milirurix (Castclnau) 50. Milichtrs opicniis (Fahraeur)

I

DWr

Number Caughr

Average Number p e r Trap

NID

G%

3 62 55 0 83 0 31

0. I

4 21 23 8

2,325 1,670 148 12,

D D

300 300 235 350 384 112 389 20 417

12 I

N N

sa

80 80 1.800 2,280 1.770 80 40

31 17 26 I4

26 I1 32 ,328 37 39 I 30 5 4

D D

N

N N

N

N N N

N N N

3 2 13 176 213

N

78 15 31 407

D D N

N N N N

N

18

38 52 76 69 0 43 60 100 100

50 31 61 90 41 100

87 31

Duplex

Loam

36.8 136.8 2.8 0.3

45.5 2.3 4.3 0.0

51.0 0.0 4.6

I .O

0.0 0.0 1.8 0. I 0. I 12.6 0.7 1.6 0.0 0.6 0.2 0.0 0.0 0.0 0.3 0.4 I .5

0.0 0.0 0. I 0.0 0.0 4. I

Sand

0.0 0.8 2.6 I .O 1.4 0.0 0. I

0.4 0.3 0.3 0.3 0. I 0.0 14.3 16.3 1.2

0. I 0.3 1.6

2.7 0.4 0.8 10.0

0.1

1 .o 1.1 0.0 1.6 0.0 0.0 0.0 0. I 1.1 0.0 0.0 1.9

0.4 1.5 29.4

Clay

73.4 0.1 2.2 0.7

0.0 0.0 0.3 0.0 0.0

11.0 0.3 0.9 0.0 0.4 0.0 0.0 0.0 0.0

0.0

0.0 0.0 I .4 0.5 0.4 2.8

51. Onirir olrris Klug 52. Onirir dewpror PCringuey 53. Otririrjdgidits Klug 54. Onirir mrirrarur Klug 55. Onirispicricol/is Boheman 56. Onirir v i r i d h s Buhrman 57. 0,8rlrophagus nci~dorrr.sFahraeeus 58, Ottrhophagas acyurpebenr d'Orbigny 59. O,trhuphnges oeroginosas Roth 60. Onrliophagsr a l c w s i d e s d'Orbigny 61. Onrhophogiir aurricrpx d'orbigny 62. Omhophugus briranus PCringuey 63. Onrhophagrrs near curbonurias Klug 64.Onrhophagus near crrrbonorias Klug 65. Omhophagus corbonrrriur Klug 66. Onrhophages corniculiger d'Orbigny 67. Onrhophagus cribripennis d'Orbigny 68. Onrhophagur dcpressrrs Harold 69. Onrhophagus diver Harold 70. Onthophagus ebenas Peringuey 7 I . Onrhophagur gazelia (F.) 72. Onrhophagus inrersririalis Fahraeus 73. Onrhophagur lacuslris Harold 74. Onthophagu near leroyi d'Orbipy 75. Omhophagus obrusicornis Fahraeus 16. Onrhophagur near pailidipennis Fahraeus 77. Onrhophagus pallidipepennis Fahraeur 78. Onrhophaguspiebejur Klug 79. Onrhophagus quadriruber d'Orbigny 80. Onrhophagus stigmosus d'Orbigny 8 1. Onrhophagur rersidorsis d'Orbigny 82. Pedaria sp.1 83. Pedaria sp.2

Ir9 35 I 204 321 BO 22 I 55 12 II 27 42 15 25 25 25 25 16 15 39

33 52 22 35 12 21

10

5 25 104 9 79 10

12

9 2 349 22 5 I 6.701 30 858 182 3.639 667 3 348 8,359 I 5 I 1,772 14

102 2,824 39 1,522 50 82 1,625 714 30 619 407 126 22

N N N N

N N

D U

D D

D

N N N

N N D N D N

N N N

N

D

D

U N D D D N N

67 100 28 11 100

0 29 0 22 63 49 48 67 62 52 100 O 100

19 50 72 64 O 26 66 61 39 48 43 22 33 M 91

0. I 0.2 5.7 0.0 0.0 0.0

462.9 0.5 14.8 5.4 279.3 0. I 0.1 0.1 109.3 0.0 0.0 0. I 125.0

0.1

1.6 2.3 3.3 10.9 0.9 4. I 87.4 20.8

0.0 43.9 3.4 2.0 0.0

0.3

0.6

0.0 6.3 0.9 0. I 0. I 93.9 0.3 30.3 3.2 23.7 7.3 0.0 0.4 336.2 0.0 0.0 0.0 22.5 0.3 3. I 55.8 0.0 52.2 3.2 2.5 25.5 30.6 0.3 4.0 8.0 6.8 0.2

0.0 21.5 0.8

0.5

0.0 0.4 0.5 13.9 2.5 0. I

2.3 0.3 42.6 151.4 0. I

0.0 0.0

0. I 0.8 3.0 238.8 0.0 44.6 0.0 0.3 18.0 2.0 0.0 1.6 32.3 0.5 2.4

0.0 0.0 2.8 0.4 0.0 0.0 1.3 I .3 17.3 4.9 0.2 46.7 0.0 0.1 150.2 0.0 0.4 0.0 0. I 0.3 1.8 18.0 0.0 34.0 0. I 0.1

10.5 6.8 2.3 2.6 1.o I .4 0. I

TABLE 8 . 8 (conr.)

Species

84. Pedaria sp.3 85. Pedaria sp.4 86. Pedaria sp.5 87. Pedaria sp.6 88. Pha1"psflrrvocincras (Klug) 89. Sorophorirs costarus (Fahraeun) FGV

+ VI

90. Cacco6iirs nigritrilur Klug 9 I.Cnccobias ~,iridicollisFahraeus 92. Coccobiiis sp. I 93. Caccobius sp.2 94. Caccobiirs sp.3 95. Cnccobiits sp.4 96. Caccobiris sp.5 97. Caccobiicr sp.6 98. Caccobirrs rp.7 99. Drepanocerrrs fasridirus PCringuey 100. Drepanocenrs frexi lanssens 101. Drepaiioctr-ar i,nprerricollis Boheman 102. Drepanocerus ki+ (Kirby) 103. Drepnnocrrzrr larir-ollis Fahraeus 104. Drrpattocerru parriiii (Boucomont) 105. Etioniricellirs nenpri lnnrsens

i

DWr

17 17 12

12

36 23 4 3 3 3 4 3 I 4 4 5 2 10 4 4 8 4

Number Caughr

Average Numberper Trap NiD

G%

Sand

Dupler

288 213 9 4 182 447

N N N

75 74 56 75 87 70

23.3 17.3 0.6 0.0 0.4 0.0

0.6 0.4 0.1

18 ,324 13 17 1,306 49 71 2 3 4

D D D N D

I .4 21.4

0.1 4.8 0.0 0.3 2.4

134 603 49 10 I

D D

56 69 39 29 38 2 70 100 0 75 73 8 28 29 70 100

II

N D

D

D N

N

N D

D D

D D

Loam 0.1

0.0 0.1 0.4 9.4 46.5

0.1

3.3 1.6

0.0

Clay

0.0 0.0 0.0 0.0 5.3 4.7

0.2 0. I 0.0 7.6 0.3

0.4 0.0 0.0 0.0 0.5 0.4 22.8 0.9

0.5 0.4

0.0 0.6 0.3 0.0 0.1 0.0 0.0 0.0 0.2 0.0 0.0 0.5

16.1 4.1

9.1

0.1

0.0 0.0

0.0

1.3

0.1

0.0

0.0 0.0

0.0

1.2 106.3 4. I 5.5 0.2 0.0

0.3 1.3 0.0 0.0 0.0 0.0 0.0

0.0

0.1 0.3

___106. 0,rrhupknger apiriomr d'Orbipny 107. O,,rliophngirsflavolim6~r~,~ d'Orbigny 108. Omliophngris lan~elligrrGerstaecker 109. 0,rrhophngei near s ~ y i l l a r s sKlug II O . Onrhophagss sugillarus Klup I I I. Omkoplrages near vincnts Erichson I12. 0,trkuphayirs vincrrcs Erichson I 13. Oiirhophagirs pugioiiaiit5 Fahracus I 14. O~rrllophagi~spullirs Roth 1 15. Onrhopkagus signarur Fahraeus I 16. Onrliophagiis srellio Erichson 1 17. Onrhopkogiri verricollis Fahraeus 118. Tiniocellrcr spinipes (Roth)

17 4 6 3

8

N D N

9 9 17 I 4 3 20 7

126 33.111 424 39,026 14 I32 32 1,725 1,631 7,080 27 810

N N D D N N D

29 29

5 3

D D

3

D

D N

25 01 68 3. I 32 186.8 25 34.7 371,245.1 57 0.2 55 7.6 22 0.4 65 134.1 79 132.0 63 117.3 70 1.4 60 5.4

0.2 6. I 1.180.4 0.6 1.465.8 0.9 I .5 0.9 6.3 3.6 334.0 0.7 17.3

0.4 0. I 354.6 0.0 330.8 0.0 0.0 0.5 3.9 0. I 8.5 0.3 56.0

0.2 I .3 1.155.6 0.1 320.8 0.1 1.9 1.0

0.8 0.3 133.1 0.0 7.4

FG VI1

119. Oniricellus formorur Chevrolat 120. Oniricellus planorus Castelnau Total Source: Doubt, Macqueen. and Davis (unpubl.). NO~CI: Pitfall traps were baited wilh a mixture of

139,998

100

0.0

0.0

0.0 0.1

0.3 0.3

0.3 0.0

42

4,205

4,030

1.711

2,291

67

pig. horse. and cattle dung fur 24 hours on Iwu occasions in December 1981. Trapping conducted in bushveld end grassveld on four soil types. Overail. 88 traps were set and 120 species and 139,998 individuals were caught. G'h, percentage of individuals caught from grassveld; FG. functional group of beetles (Chapter 8). was

388

.

Appendix B

.

AppcndixB

389

TABLE B.Y(I) List of Scarabaeidae dung beetles collected at Abokouamekro. 198&81. Ham,,,z I),,,>,>

1. Scarabacus gory; (Lapone) 2. Scrrmbaeus palemo Olivier 3. Allogymnopleurus umbrinus (Gersl.) 4. Garreto nitens (Olivier) 5. Gymnopleurus coerulescens (01.1 6. Cymnopleurusfulgidus (Olivier) 7. Cymnopleurus profanus (Fabricius)

8. Gymnopleurus puncticollis Gillet 9. Anachnlcos u r e s f e n s Bates 10. Anachnlcos sururalis Janssens 11. Neosisyphus ormarus (Gary) 12. Neosisyphus baoule Cambefon 13. Neosiryphus gkdiaror Arrow 14. Neosiryphusposchalidi~~~ Camb. 15. Sisyphus biormutur Felsche 16, Sisyphw costarus Thunbcrg 17. Sisyphus desoegeri Haaf 18. Sisyphw goryi Harold 19. Sisyphus seminolurn Gerstaecker 20. Catharsius crossicornis Gillcl 21. Caihorsius ereocles Lapane 22. Carhnrsius sesostris Waterhouse 23. Copris carmelita Fabricius 24. Copris eorlorius Gillet 25. Copris inferioris Kolbe 26. Copris orion Klug 27. Copris renwarri Nguyen & Camb. 28. Lirocoprlspuncrivenirir Wat. 29. Metacotharsius obortivur (Fairm.) 30. Metacorharsius inermis (Lapone) 31. Metacothnrsius rchodensir Balth. 32. Coprurhinrr suboeneu lanssens 33. 34. 35. 36. 37.

Heliocopris animor (Olivier) Pedarirr coprinarum Cambefon Pedaria dedei Cambefort Pedario durandi Paul.. C. & M. Pedaria human0 Cambefon

38. Pedorio renwarti Cambefort 39. Oniris alexis KIug

40. Oniris cupreus Laporte

41. Oniris reichei Van Lansbcrge 42. Cyptochlrus distinctus (Janssens)

DIN

FWi

I

I1

N

1.675

15

32 I20 397 2 1,479 92 I77 1,618

D

540

D D D D

140 310 62 62 I15

N

D N N

D D

D

130 1,738 517 49 80

2

9 17

5

111

v

Iv

4 25

I

2

I

I47 2 22 39

6

2

6

2

II

5

X

5

6

16

IO

I 42 77

3 IO

1,835 1,123 39 3 2

918 2,325 36

29 6 545 1.926 X

2

I

220 1.650 x I

2 I

2

I

I 30 7

4

I

4

N

5,800

4

N N N

35

18 I

I

5

2

23

5

I

I

91

10

6

4

7

I

N N

D

II

5

10

30

56

I

312 5 36

4

41 I 707 4

178 34 25

699 468 18

137 106 4

32

89

3

90

I2

6

499 43 42

1

6 28 3 I

216 17 27

58 22 3

48 13 6 I

103 24

II

164 26

d

138 21 13

8

168 21 4

2 6

2 4

2 2

2 4

10 2

13

7

9

3

2

1

I

130 40

N N N

19

9

N

35 35 35 35 375 463 411 145

25

I 2

N

30

v

I

I3

136

D

c

I

.N N

15

VI

I

104 46 D 14 D. 68 D 17 308 175 D 12 N 1,221 N 1,267 N : 566 N 464 N,' 194 N 365 N 216 I N 853 '

V

____

4

5'

D

n

IV

I1

I

9

155

D

VI

I

I

2

9 I

6

20 1 2

i

2

51 2 4 6 6 12

4 99 I2 6 3 65 6

3 I

2

119 37

10 144

68

392

.

AppendixB

AppendixB

.

393

TABLE B.9(1) (coni.) H u m n Dung DIN Onrhophagus ghonensis Balthasar Onrhophagus imbellis d’Orbigny Onthophogus juvencw Klug Onrhophogus lamorlellus Cambefort 90.OmhophaguslamfmnsiisCambefort 9 I.Omhophagus lnrigibber d’Orbigny 92. Onihophagus lioides d’Orbigny 93. Onrhophugus longipilis d’Orbigny 44. Onrhophagus louderioe Cambefon 95. Onthophqus mamhouewis Camb. 96. Onthophagus marginifer Frey 97. Onthophagus mocquerysi d’Orbigny 98. Onrhophagus ~ U C I U ~ O L Thomson US 99. Onthophogus mucmnifer d’Orbigny 100. Omhophogus naevius d’Orbigny 101. Onrhophaguspicarus d’Orbigny 102. Owhophogus pullus Roth 103. Onrhophagus relicdnrvr #Orb. 104. Onrhophagus rufonororus #Orb. 105. Onthophagus rufodllcm d’Orb. 106. Onrhophogussanguineus d’Orbigny 107. Omhophogus sangvinolentus d’Orb. 108. Onrhophogussovonicola Cambefort 109. Omhophagus semivirescens d’Orb. 1 10. Onthophagus sinwsus d’Orbigny 11 I.Onrhophugus subsulcorus d’Orbigny 112. Omhophagus rersipennis d‘orbigny 113. Omhophogus tripwritus d’Orbigny 114. Onrhophagus ulufa Balthassr 115. Omhophogus variegutus (Fabricius) 116. Onrhophagus vincrus Erichson 117. Onlhophagus vuarrouri Cambefort 1 IS. Onrhophogus vulruosus d‘Orbigny 119. Pholops iphis (Olivier) 120. Pholops v a n e l h (-Van Lansberge) 121. Proogoderus uu~urus(Fabricius) 122. Proagoderus cornbeforti Palestrini 123. Srrandius obliyuus (Olivier) 86. 87. 88. 89.

N D N

D N N D

D D D D

N D

N N

N N D

D N D

FWr 22 14 25 4

50 6 35 5

N D

N D D

D D

N

IV

v

4

3

60

62

342

15

5

16

42 4 59

3

3

v

VI

71

19

127

322

491

c

v

96

I

25 41

Y

IO

4

27 3 44 48 77 3

I

I1 3 104

5

6 I

I

I

-5

87

II

8

7 3

16

5 1 21

I

I

34

I 22 781

4 I

2

4 294

22

1,260 146 I

I I

I

650

7

5

I1

17

57

8

185

2

2

I8

I 20

1 I 3

I

24

134

15

7 6 34 2

8 56

3

I 1 48 32

2

11

18

22 5 I 24 12 3

9

2

37

8

9

3

7 4 29 2

1 2

2

5 1 9

I 1

I

2 2 2

1 1 2

I 2

4 2 26 8

5 5

Nores: The rollowing dam are given fur each species: diel aclivity, rrerh weight. number of individuds CUIIsled in human dung-baited lraps in the six bimonthly perids (I: kbruury-M;lrch. e a . ) , thc yilrne fur bceilcr exlracled from ~atlledung pals; and lhe numbers of h c l l e ~eaughl in cimiun-bililcd (raps (C) and iii vcgcrable matcriill (V).

IV

3 34

1

19 31 18 I24 68 213 I82 204

Ill

II

I

1Y

14

I

2

212

7 13 3 17

VI

I 3

366

I1

N

111

3 5 338

16 62 II IO

38

N N

-

2 34 12 4 695

4

D N D D

II

4

44

N

D

I

Cattle Dung

I

I

TABLE B.9(2)

Numbers of Scarabaeidae dune beetles collected in six savanna localilies. 1980-81 Localrrier

Species I . Kheper fesrives.(Hnroldj 2. Kheper subaen& (Harold) 3. Scarabaeus goryi (Laporte) 4. Scarabaerrspalemo Olivier 5. Allogymnoplerrrus umbrinris (Gerst.) 6 . Allogymnopleurus youngai Endriidi 7. Gorrera aiureus (F.) 8. Gnrrera nitens (01.) 9. Gy,nnapleurrrs coerulesrenr (01.) , . 10. G?,~nr,pleurr,sfrrlgid~,~ (01.) 1 I , G~mnoplnrrasprofanlcr(F.) 12. Gy,nnopleerus punrricollb Gillet 13. Anuchalcos arrrescens Bates 14. Anachalcos conve.rit5 Boheman 15. Anachalcos cicpreirs (F.) 16. Anochalcos sicrurulis Ianssens 17. Odonroloma relicrum Cambefort 18. Neosisyphus nrmulii~(Gory) 19. Nemisyphus baorile Cambefort 20. Neosisyphus gladiator (Arrow) 2 I . Nemi.rypIrm paschnlidijor Camb. 22. Sisyplucs biarmaros Felsche 23. Sisyphns c o s r m t s Thunberg 24. Sinphas dcruegeri Haaf 25. Sis?phus gaxmrs Arrow 26. Sisyplrw g o r y Harold 27. Sis?phcrr lobi Cambefort 28. Sisyplrus seniindum Gerst.

79. Carharsircj crarsicorni5 Gillet 30. Corharsius ereocies (Lapone) 31. Cnrhorsirrsfasridiiorss Thoinson 32. Cutharrius psercdo1.vcaon Ferreiril 33. Carharsius sesorrris Waterh. 34. Copris angusrur Nguyen 35. Copris carinelira F. 36. Coprir ooriariur Gillet 37. Coprir eburnercr Nguyen 38. Copris garellarum Gillel 39. Copris inrerioris Kolbe 40. Copris megucernroidrr Waterh. 41. Copris moffurrsi Gillet 42. Coprir orion Klug 43. Copris orphunus GuCrin 44.Copris renwarri Ng.& Camb. 45. Litocopris muticur Boh. 46. Lirocopris punctiventris Waterh. 47. Merucarharsius abortivus (Fairm.) 48. Merocathursius inermis (Laportc) 49. MeracatharJius rchadensis Balth. 50. Coprorhina suboenea Janssrns 5 1. Delopleurus gilkri Ianssens 52. Heliocopris anrenor (01.) 53. Heliocopris colossus Bales 54. Heliocoprix horoldi Kolbe 5 5 . Heliocopris myrmidon Kolbe 56. Pedaria coprinarum Cambefort 57. Prdaria criberrima Waterh. 58. Pedaria decorsei BOUC. 59. Pedaria dedei Cambefort 60. Pedaria durandi P.,C. & M. 6 I . Pedoria fernnndezi Cambefort

I

2

3

5

4

6 4 I

17

30

I

460 428

2.676

7

27 I 4

57 145 436

19 40 6 8 4 593 168

2 1,644 129 209 1,657 I

3 13 32 30 122

67 1,677

89 29 61

30 3

7

5 I

10

I I4

6

20

II I22 222 75 I4

19 12

45 189

1,279

5,375 4.549 54 264 4.973

I12 I 2 102 61 126 6

8 3 139

5,881

933

2.901

2.800

16,679

8.718

1,032

418

2 31

209 9

29

267

8

4

2

7 26

4 I

326

2

468

I

4

2

I I5

36

5

42

8

16 3 4

18

12

31 2

1,418 36 I

I 78 2

5 40

7

24 4

811

3.821 115 2.822

18

so 4 I50

9

4 6

2 3 4 I 7 5

I1 332 6 41 8

5

25

49 145 I

5

2

io

768

20 I 4

5

I

1

9 1

2

22

I

7 1 I

L

I20 38 12

io 14

U

7

TABLE B 9(2j (CON

j

LoculiriEs

Species

63. Pedariu onungoe,rsis Cambefort 64. Pedaria renwuni Cambefon 65. Hereronitis poulioni Janssens 66. Oniris nenezcs Van Lansberge 67. Onifix affzis Fclsche 68. Oniris alexis Klug 69. Oniris cupreus Lapone 70. Oniris lobi Cambefon 71. Oniris mrilridenrarus Gillet 72. Oniris nigeriensis Ferreira 73. Oniris occidemalir Gillet 74. Oniris reichei Van Lansb. 75. Oniris robusrur Boheman 76. Oniris siburenuis lanssens 77. Oniris splrinr (F.) 78. Oiliris violucercs Van Lansb. 79. Cprochirus disrincrur (Jams.j 80. Drepunocerus bechwei lanssens 81. Drepaiiocencs caelarrrs (Gerst.) 82. Drepuiiorerus endruedxi Endrodi 83. Drepu,rocere~luricullis Fahr. 84. Drrpunoceres mnrshnlli Bouc 85. Drepu,rocenrr soegwi Balth. 86. Drrpunocenrs sirlcicollir (Lap.) 87. Eironiricellr~sfimigorr(s (Bouc. j 88. Ei~o~~irlrellar i n r m w d i m (Reiche) 89. Erioi~iricelhrskawmrrrs (Jamsen,) 90. Euoiiiricellui nuricornir (Reiche)

9 I . E~ro,iiricellr~spunrrs (Kraatz) 92. Euo,riricellur ribarmsis (Kolbe) d'Orb. 93. Linroiigasfi~l~osrrintrlr 94. Oniricdr~s f o r m o s ~ Chevr. ~s 95. O ~ r i i i r r l l a s p l ~ ~ ~Lap. run~s 96. Tiniocellzrs spinipes (Rolh) 97. Cuccobiirs urtihrucirer d'Orb. 98. Cuccobirir urrberri d'Orb. 99. Cuccobius cui~arusd O r b . 100. Cnccobius Jerrugiiirris 1Firhr.j 101. Cncmbius inops Peringuey 102. Cuccubior ivorrnsis Camb. 103. Cuccobiur lnmorrei Camb. 104. Coccobiuu mirabil~prmrrarusCamb. 105. Cowobius penragonus d'Orb. 106. Coccobius punciarissimas Harold 107. Combefrrius bidenriger (d'0rb.I 108. CambeJorrius lrrrnizunui (Camb.) 109. Cleptocuccobius bdfhurarianus (Cambefort) 110. Cleprocaccobius convexfrons (Raffray) I 11. Cleprocaccobius dorbignyi Camb. 112. Cleprocaccobius signaricollir (d'Orb.1 113. Cleprocaccobius uniserier (d'Orb.1 114. Diasrellopalpus lumrllicollis (Qued.1 115. Digironrhophagus gazrllu (F.) I 16. Euonrhophngus curbonarius (Klug) 117. Hyalonrhophagus nigrovioloceus (d'Orb.1 1 18. Hyolonfhophaguspreudoalcyon(d'Orb.1 119. Milichus apicalis (Fahr.) 120. Milichus serrarus d'Orb. 121. Onrhophugur vlridorsir d'Orb. 122. Onthophagus onrennolis Frey 123. Omhophagus atridorsir dOrb. 124. Onrhophugus baoule Camb.

I

3

2

2

4

190

6

5

2

a7

1

2

I

I 2

2 I21

28 12

6

17

I

3

2 12 4

I 51 56 I

1

28

2

44

4 3

2

18

13

2 52 2 5

57

3 465 3,276

12 265 I43 66

177 2

24 I 31 1 7 2 1

7

9 8 2 3

19

3 I 1 8

5 18 4 I22 11

19 8 62 I

239

19

2.132

45 I

188

25

1.334

979

9 3

245

I

41

6 I 1,206

I I 592 43 228 93 24 37 IO1

75 4 679 6 85 2 26

I57

I ,400

55 3,374

818 I

669

4,818

20

2,655

4 12

16

1,032 I 21

3

24

3 832

1 6 4 196

191

38

I81 I 3 80

1

16

I07 I 225

23 3

90

52 287 5 1,172

362 3,011

I70 42 883 2,352

53 6

917 222

479 93 46

13 542

67 107 80

8

993 33

63 69

7

151 I15

171 82 122 65 I

39 3 131 60 1.659 108

1,071

7

135 2 14 42

177 179 5

1 1

2 1

II 139 307 4 45 1 4

14 I09

49 4

I 8 P

I

101

8

6E

PLE

Z 19 98 I

Z61

L 62 05 U 111 9E 101

P

*

699

Z L6E

1

oz

Z

Z

PE

I EZ

I

L 1

P

1 Z

IZ

E

5

55

I

6Z 9SP'E 9z I I 9z I Lz8'1 01

Z E 9E L

8SZ 88Z'Z

E Z

oz

zs1

I 116 I EPI

P

I

OL

5

80 I 6ZL'Z 6

68

L% 1

LZS

8 LS

t'9 I

8 E 01

E

1

YLZ

E

Z

9 I

95

51

81

IZ

Ll

86E

I

Pb

Z

LEI

os I' 1-002

oVE'I*l 009'1-002 051' l-02Z OS1'1-58 051' 1-008 OOL1X)Z

nsi ' 1-002

009-002 OOZ'1-052 009'1-009

OOZ'I-S8

os1a 1-009

ooZ'1-58

nsz-01

08L'I-OEZ OPE' I -002

nou-ooz

OOZ'1-01

4

000'1-002 OSSQOZ

os8-58 002'1-58

001 * I*ZZ 0S1'1-0SE OXL'I-OEZ 002'1-58

h,

+.

W

008-00L

021' 1 5 8 007,' 1-58

OSWI 001'1-00E 009'll)S6 008-06

OSI'I1X)Z

Y

m

TABLE B IO(2) (conr ) Seasonal Occurrence (number of samples)

Species

Feb (IO

Mar 10

a

3

36. C . knighri 37. H . cambeforti 42.Aphodius sp.5 43. Aphodius sp. 6

Apr 10

May 5

6

2

Jun 2

Aug

JUl

Sep

3

3

Oct

3

Not,

3)

3

3

3

4

2

108

*

3 3 66

6 86

cv

I

*.< 310

*

3

210

I 169 26 50 49 . 63 4 4 B . celebensis 109 20 21 18 33 N o m : Results are given separately for Februaty to November (lune Simple was collected 6-13 July, September sdmple 2-9 October). Number of samples is the nurnher of weekly FIT samples. The figurer given are averages per sample mulliplied by IO. The Inst two Columns pivs the mean and the coefficient of 5 65

variation (SDimcan) across the 10 months. * Average is leis than 1.

B. I l(11 ist of Scarabaeidae dung beetles callected in Tay forest, 1980-81

ABLE

Sens0,znl Orcllrrencr

necier I.Gorrero d&ir (Waterhouse) 2. Nrosinphus ongdicollrr (Felschel 3 . Neosiqphus i d Carnhrfon

4. SisTphui eburneer Carnbefon 5 . Sisyphur larur Boucornont 6 . Carharsius niner Gillet 7. Copris rrrnabilis Kolhe S. Coprir camerunu~Felsche 9. Coprisphylar Gillet 0 . Coprir widens Felsche 1. Copris truncaius Felsche

2. Pseudopedarin grosrn (Thornson) 3. Heliocopris diunoe Hope 4. Porophyius bechynei (Balthasar) 5 . Pnmph,iur rancyi Pauliiln 6 . P a r o p h p s rai Cambefan 7. Alioniiis nasuiui (Felschel 8 . Lophodoniris corinarus (Felsche) 9. Onirir nemoralis Gillet !O. Oniris subcrenuius Kolbe !I. Dreponocerur st~ipaius !2. Drepanoplorynus gillrri Boucomunt 13. Euoniiicellur iai Cambefan !4. Liorongus sjostedti (Felschel ! 5 . Oniricellur pseudoplanarus Balthasar !6. Tiniocellus ponrhera (Boucornont) L7. Amierina eburnea Carnbefon

HU

2 69 142 10

MI

BU

EL

1

6

9 6

2 20

VE

1

LF I

2

2

1

7

CA

9

20

4

5

70 2

1

2

5

16

FLVr

350

SO 76 10 15 255

D D D D

D N

I

/I

9 4 16

12 3 58 7 I

7

101 442 860

N

353 917

N

I 7

N

3

230

N N

2

3,110

9

DIN

N N

2

Ill

IV

V

VI

I0

2 23

23

2

L

50 21 4

1

13

5

3

3

24 7

18

22 1 3

32 204

1

346 I1

61

13

16

2

4

2

s

I

7

I

1 12 41 6

3 5 1 41

5 II

21

2

1 24

1

2

13 2

14

1

514 370 441 506 4 49

N N N N D

10 63

D

72 70 4

D D D

D D

I

I

3

I

6 21 35

2 6 38

1

14 1

8

IS

2

I

181

6 46 I

104 6

8 21

10 97

101

2

4 1

2 2

40

ABLE

B.II(1) (conr.) Seosonal Occurrencr

HU

7ecies 8. Caccobius cribrmier Boucornont

9. Caccobius &oris Cambefon 3. Cnrcnbius elephantinus Balthvrar 1. Caccobius rai Cambeion

2 . Diasrellopalpus conrndri d'Orbigny 3 . Dinstellopolpus lnevibibods d'Orbigny 1. Diasreliopalpus n o d s (Thornson) 5 . Diastellopnlpus tridens (Fabricius) 5 . Milichus inoequolis Boucomoni 7 . Milichus merzi Cambefon 3. Mimonrhophagus apicehirras (d'Orb.) 3 . Omhophagus andropnus d'Orbigny 1. Onrhophagus otronirider d'Orbieny

BU

EL

1

83 12 380 43

MI

I

VE

LF

I

9 6 5 277 447 256 380 25 57

10 1

3

25 24 3

20 2 6 I 33 6

1

110

1

165

15

I

2

23 49 21 30

35 I 1

87 26 49 I

7 2 4 298 97 14 5 1

FWr

1

29

1 1

2

2

2 6 23

I

8 3

3

1

5

DIN

10

I.Onrhophages bnrrosi Baltharar

2 . Onrhuphnges cephaiophi Cambefon 3. Onrhophngns c u r ~ f r m d'Orbigny s 4. Olrrhophogrrr densipilis d'Orbigny 5. Onrhophogics denticulorus d'Orbigny i. Onrhuphagrcs denudanis d'Orbigny I . Oarhophagas depilir d'Orbigny 1. Onrhophogsr deplnnnrirr Lanrberge 3. Onrlrvphrrgasf e d dOrbipny I. O~!rl~uphogrrs foelliorrri Cambefon 1 . 0,lrhophogrrrfi'rcorsr d'orbigny !. 0 , r t h o p h o g a s f i ' r c i d ~ ~d'Orbigny ~i.~ I . Onrhopho,qicrgmrori d'Orbigny I . Onrhuphrrgerhiloridis Cambefan i. Onrhophagrn hilnrir d'Orbipny

CA

20

10

28 23 69

71

~

I

I1

D N

26

19

D N N N D N N N N

12 19

98 25

D

D N N

II

VI

1

4

26

9

99 4

18 1

6

147 5 I 3 1 0 9 2 7 2 1 1 I I 2 20 I 33 1 2 1 1 3

1 6 5

I

1

1

6 53 3 7 I 2 3 2 9

14

N D

6

N N

3 2 1

D N

v

Iv

Ill

6 23

4

40 25

42 22 4 1

3

D

28 51 38 27 6 9

N

10

N D D

3

17 4

1

1

13

D

16

21

7 8

I

2 1

4

1

N

34

1

8

84 23 2

102 1

3

17 0 5 10

4 82 20

9 I

I

6 .

5 . Onrhophnjiar i d Cambefon .~

7. 0,lrhophagar irlfausrar Cambefort 8 . 0,irhophagas kindinnus Frey 9.0,zrlwphogas Iaevicepr d'Orbigny 0. Onthophngus lominmer d-Orbigny I,Onrhophngus liberianur Van Lanrberec 2. Onrhophugus marof Cambefon 3. Onrhophng!'r orrhoremr Thornson 4. Onrhophups pleurogontts d'Orbigny 5. Onrhnphagar rrcrorispnslinni Cambrfor 6 . Onrhophngus rufopygitr Frey ,7. Onrhophagus semii.iridis d'Orbigny 8 0,drophogur srricreririnrrrr d'Orbigny ,9, Onrhophogus rynceri Cambefort '0. Onrhophngus roirnrir Cambefon 1 1 . Onrhophngus renuisrrinrur d'Orbigny 12. Onrhophogus veranur Balthasar 13. prongodrrus rirsemoi Van Lansberge 14. Srrondiur rigrinus (d'Orbigny1 IS. Tomogonur crassu-~d'Orbigny

Vumber of individuals Number of species

%umber of species in a sample of 78

19

4

I

1 10

I I4

4 67

I3

2

I

2

I

2 4 123 44 32 I 3 26 7

3

4

I

63

8 5 1

2

-I

67 15 33 N 20 39 25 II

80 67 58 48 12 62 13 159 171 35

16

3

1

58 1

17 II

1,506

146

106

120

78

32

50

43 20

44

ll

18

IO

23 19

9 9

3 -

-

N

_I

I

1

D N

3

7 3

4

4

18 1

N

N N D N

D N N D N D D N N

..

3

1

-

U N

,

I 4

4 4j

3.1

20

I 2

I

1

6 7 3 3

I5

2

3 4 1

2 5 1 1 1

4 8 7 2 3

315

730

2 I?

2 2

3 1

1 51 I

13 24 4

4 44 21 22

48 6 I

2 I

I

8

7

3 14 34

2

3

14 7

502

1,050

642

149

10

Norer: Food selecti~ngiven as the numbem of individuals caught with the followingbaits: HU,human dung: EL, elephant dung; B Y , buffalo dung; MI, missellaneour dung; CA, carrion; VE. vegetable stuffs; Lf, specimens found sitting on ICBYCS. Also included are numbers of specimens collecled in six bimonthly periods ( I = Febmary-March, etc.). individual fresh weighl, and diel activily.

,

.. -

408

'

Appendix B

AppendixB

8.1 l(2) List of Scarabaeidae dung beetles collected in Makokou, 1Y81-83. TABLE

HU

Species I . Garrera ebenus Janssens 2. Sisyphus arboreus Walter 3. Neosisyphus angulicollis (Felsche) 4. Neosisyphus barilewskyi (Balthasar) 5. Carharsius gorilla Thornson 6. Carharsius gorilloides Felsche 7 . Catharsius lycaon Kolbe 8. Calharsius ninus Gillet 9. Copris amabilis Kolbe 10. Copris colmanri Gillet 1I . Copris jahi Nguyen & Cambefon 12. Pseudopedaria grossa (Thornson) 13. Pseudopedaria villiersi Walter 14. Heliocopris corona~usFelsche 15. Heliocopris murobilis Kolbe 16. Paraphyrus ophodioides Boucomonl 17. Paraphyrus bechynei (Ballhasar) 18. Pedaria ovala Boucomonl 19. Oniris androcles Janssens 20. Oniris arluosus Gillet 21. Onitis subcrenarus Kolbe 22. Lophodonitis carinorus (Felsche) 23. Liarongus sjosredri (Felsche) 24. Onilicellus pseudoplanatus Balthasar 2.. Tiniocellus panthera (Boucornont) 26. Arnietina larrochei Carnkfon 27. Coccobius elephantinus Balthasar 28. Diastellopalpus anrhonyi Walter 29. Diasrellopalpus conrodri d'Orbigny 30. Diasrellopalpw gilleti d'Orbigny 31, Diaslellopalpus laevibusis d'Orbigny 32. Diast~llopalpusrnurrayi (Harold) 33. Diasrellopalpus sulciger Kolbe 34. Hereroclitopuspunctularus Boucornonl 35. Mimonrhophugus apicehirtus (d'orbigny) 36. Onrhophagus ahenomicons d'Orbigny 37. Onrhophagur belingo Waller 38. Onrhophagus biplagiatus Thomson 39. Onrhophagus densipilir d'Orbigny 40. Onrhophugus denudarw d'Orbigny 41. Onrhophagus depilis d'Orbigny 42. Onrhophagus erectinasus d'Orbigny '

'

EL

3 109 13 I 14

MI

5

1

I

I

CA

VI<

LJ

LF

10

21 I 2

2

2

2

6 2

I

I1

I

1

2 1

2 3

II

8 '

I

3

2 I 2 3 2

I

4

I

I

I

4

1 I1

I

I

35

2 2 1

3

I

1

8 13

2 1

18

15 I 2 90

7 3

8

3

1

1

3

2 10

5

2

.

409

I 1

.

410

'

AppendixB

TABLEB. I I(3) Numbers of Aphodiinae collected in Tar (top) and in Makokou (bottom). I . Aphodius formosus Paulian 2. Aphodius cambeforri Dellacasa 3. Aphodius heleninae Dellacasa

19

21 7

4. Aphodius kumasianus Endrddi 5 . Aphodius moroensis Endrddi 6 . Aphodius egregius Petmvitz 7 . Aphodius principalis Harold 8. Aphoidus renaurli ClCment 9. Aphodius harrwigi Petrovilz IO. Aphodius unrhrar Gerslaeckcr 1 1 . Aphodius n. sp. 12. Aphodius aequororiulis Petrovitz 13. Aphodius maldesi Bordat 14. Aphodius schouredeni Boucomont

49 31

2 1 4 I

2 43 I13 2

15. Lordiromueus cambeforri Bordar

1. Aphudius wirrei Paulian

2. Aphodiuspiicarus Endriidi 3. Aphodius gi/ieri Schmidt 4. Aphodius cf. morocnsis Endrddi 5. Aphodius principalis Harold 6. Aphodius siekessyi Endrikii 7. Aphudius asracus Boucomonl 8. Aphodius rnoroi Paulian 9. Aphodius n. sp. 10. Aphodius n. sp. I I . Aphodius oequurorialir Petrovitz 12. Aphodius humaror Endrodi 13. Aphodius mulrirarinarus Endrddi 14. Aphodius sp. I 15. A p h o d i u sp. 2

16. Aphodius schouredeni Boucomont 17. Aphodius bdoghi Endr6di

-

21 3

I

7 27 I 13

~

I

8

4

I1

, ,

111 :

23 14 4 I 1

2 I

s

I -

* - m 0 - 0 0 0 0 0 0 'D m - 0 0 ~ N 0 0 ~ 0 0 O N'

TABLE B 12 ( m i i f

)

Specrer

DWr

24. Copris lugubris Boheman 25. Coprophanaeus'relamon coryrhus (Harold) 26. Delforhiiumpseudoparile Paulian 27. Delrochilron vnlgicm acropyge Bates 28. Dichotomias ngenor (Harold) 29. Dichoromius femornrus H.& Y. 30. Dichoromius samnas (Harold) 3 I . Eurysteriius caribaeus (Herbst) 32. Eurysrernus foedus Guerin-Meneville 33. Earysrernesplebejus Harold 34. Onrherus brevipenais Harold 35. Onrherrcs srrirrs H.& Y . 36. 0,zrhocharir panumc,uis Paulian 37. Onrhophagui anminutus Harold 38. Onrhophogus cosci,ieas Bales 39. Omhophugus crinirus panomensis Bates 40. Onrhophagrcs dicranias Bates 41. Onrhophagrru lebasi Boucomont 42. Onrhophagus praecellens Bales 43. Omhophugus shnrpi Harold 44.Oiirhophagtrs stockwelli H.& Y . 45. O.qsrerno,i rilenas Carklnau 46. Pedaridiem bo~ritnerit<.&Y .

I86 525 47 70 235 103 267 105 158 12 75 ? 2 8 2 32 6 8 17 12 24 130 2

16 23

47. Peduridiam brn.iserost~ttt H.& Y . 48. Pedaridiuaz pilosum (Robinson) 49. Phaiiaeas hoa,detti Arnaud 50. Phaiiaeirrpyroir Bates 5 I . Scarimrrr o~'11rus Harold 52. Sulcophanrreus cupriroilis (Nevinson) 53. Uron.sgarene,,sir H.& Y. 54. urO.r?S gorgon Alrow 55. Uro,rys macrocuiuris H.& Y . 56. Urorys meragorgon H.& Y. 57. Uro.rvr microcdaris H.& Y . 58. Uro.ryj micros Bates 59. Uro.ryjplaqpyga H.& Y.

2 2 298 192 7 192

3.5 3.5 16

~

10

46 3 14 3

3 3

LE

SDT 0 0

12

0

12 17

0

14

20

16 16

9

13 I4 4 6 35 9 5.5 5 6 7.5 8 16 35

Ij

6 19 5 IO 3 7 3.5 4 4

0 0 20 2 I 12 0 0 0 67 38 5 0 294

LDT 1 0 0 0 0 0 79 4 13 40 0 0 0 I27 65 23 0 17 I2

FIT

Toral

0 0

0 1

0

0

1 21 I2 6 I24 0 0 65 453 796 81 323 19 134 I64 115 0

0

0 U

0 34 48

0

0 I1 0 0

U 0

I

0 I I O 2

120 19 20 180 23 0 65 656 913 110 323 42 175 170

NID

N CIN

CIN N? N

T

D

T

N7 N? D

? ? ?

D D D

0

N'

0

0

I4

6 66 394 33 21

0 20 66 418 I68 27

0

87 0 0

0 2

0

0 1

I

0 0 58 13

0 0 101 8

29 0 0

594 374

0

15 56 2 0 789 464

TIK T T

D

0

141

T

AIC

I

2

R

R?

AVC7

D D D D D

15

T T

T? T '1'

N

N

"?

N D D N

D N N

?

T T

T T

D CID CID ? D D DiC

D D

D

Ant nests ?

7

DIC D DIC DiF 7

DICIF DICIF D D

'?

Phoretic7

?

Phoretic? D D

K TI0 TI0 TIK TI0

DIC

DIC D

?

N

N

1

N

?

N

TIK? ?

N

Food Prefereure

Relocunou T~clriiiqae

Sloth dung D? Sloth dung D?

D

D?

Nom: Nornenclaiure follows Howden & Youne [ 198 I ) and Hawden & Gill (1987). Dry weights and lengths are averages for samples of 40 specimens (or less if fewer than 40 specimens were available).SDT. number of beetles collected in small dung traps ( b a i l 2 cm'. total sampling effort I18 trap-nights); LDT. number of beetles collected in lnrge dung traps (bail 200 Em'. total sampling effon 18 trap-niehts);FIT,numbers of beetles collected with Right interception traps (total sampling effon 152 trapnights); To0181. numbers of beetles collected by 811 methods. Diel activity: A , auroral,C, c-repuscular:D, diurnal: N , nocam~l.Food relmation techniques (see texl for details): K , kleptopararite: C , pellet roller, 0.dung pusher: T, tunneler; R, roller. Food preference: C . carrion; D. dung; F, fruit. See Halffteret al. (1980) for details on Euqrrerner behavior.

1

E

I aL

z

" LP

zsz I

I

9 08

PP 8E Z8E 829

6 9 5 I

L

OE I8

OIP OS')

LSI

zr

El LP

I E LI I

5P 1

Z

9 Z PI L

I ll

I

OhP

6 RR

6RP

I IZ

9 E

L

01

6 Z

LO I EZ

.

*

.

..

~ , .

418

i I

,

,

TABLE 8.14

.

AppendixB

'I1~w.i. 13.14

(cont.)

i !

! i

I

3

2

1

Month

Species

4

SilC

7

6

5

Jun

3,670 45

112 34

1 5x

214

Aug Sep

43

I

I

16

Jun Jul

10 58 376 20

Jul

16

xs

I

II

65

1.

I I

16. Aphodius rufrpes (L.)

!

L E 11-13:DWt: 198 c. ha: CO

Aug SCP

P

I

<M

316

12

x

Y

153

49

2

12

IY

28

4 2 I 564

2

1

I

J""

Jul I 15

Aug

Sep

18. Aphodiusfmelarius

L E 5-8; DWI: 99 c, ha. s; CO. de

Jun

7

146

xx

2

48

7

28

I

I

5

I

5

6

71 'i45

I

1 55

13

4

147

531

8

I0

4 20

I83 272

26 137

20

Y

279

166

34

II

102

Y8

6 I

17

4

324

44

I02

173 777

I58

Aug

641

SeP

6

7 79 32

21

68

I04 20

Jun

I

1.055 1,581 82

440

I

206 I92

6 4

Jul

Aug SeP

'

I

3

19. Aphodiur haemorrhoidalis (L.) L E 4-5; DWt: 40 c , s, ho; CO

P

Jun Jul Aug Sep

,

.'

.

I

20. Aphodius alpinus (Scop.)

L E 5-7; DWt: 34 c , m, s, ha; M

P

Jun Jul

I 257 397 47

51 1 26

21. Aphodius soryrus Reitter

L E 5 6 . 5 ; DWt: s, c, rn; CO P.

f

45.5

LE: 6.5-8.5; DWI: 60

J""

U. 111, 5 , 11": C"

JUI

D; p

5

42

I

2

AUE Sep

4

5

6

I

2

1

I I

1 I6 2

I

969 79 13

I

139 6

I

23. Aplwdim d d o m i u d i . ~Bonclli ( = A. ,rri.irrrs A . & G.B. Villa) LE: 5-6.5: DWt: 17 de I): 1'

LE: 6-8: UW1:

(L.)

P

3

2

1

Jim

Jul

I

5

17

73

A"g

2

scp

I

24. Aplroditrs oD.wwrrs (Fabr.)

L E G 5 ; DWI: 16.5 c , s; CO

P

I

22. Aplrodiu ge,-n!um/i Niculas & Ribouler

U. 5 :

17. Aphodiur tenellus Say !

hiorrtl,

Sl"'iC.S

15. Aphodiro depressus (Kugel.)

LE: 6-9; DWt: 65.5 c, s, h. m; CO D P, f

419

coni,^

sire

1 i

.

Appendix B

Jul

'4%

Sep

2

10

3

27

I

I

15

I

92 279

8

c . ini. I): 1,

\,

ho;

CO

so

J",, Jul

56

AUf

562 Y7 201

586 381 YSY

670 91

2 814

XI3

1.545 1.497

12.174 4.298

scp

13

193

74

15

39

1,202

3.3

1.5 7

N o m Sludy 9 1 1 ~ s :I. Bcssilns Cillritudc 1.750 ml; 2 . Bonneval (1960 mi; 3. Lo Ram;~sac(2.000m):4. G I'lm (2.230 111): 5 . P m d" Manic1 (2.410 ~nd:h. L e s Roches (2.440 ml: 7 . Balcun du Montci (2.760 m i . U lypc preScieiiuc%(iitlulc bcerlcri: c. CILLIC; 11. human: LO. hone: 811. ~~vilcn~ul: I . sheep. Larval h o d 1n;sbils cuproplugous: de. rlclrztivuruus. Hobilrl sclrdun: p. ponurr: f. furest.

420

,

AppendixB

References

T h ~ ~ 8 . 1 5 Dung beeller of Badgingarra National Park.

Species I.OnthophagurJerox Harold 2 . Oiirhophops rupiraprrr Waterhouse 3. Onihophvgur evanidus Harold 4. L;rtonirir.ellus internwdiur (Reichel 5. Aphodiursp. 8lLl68 6. Aphudius sp. 81-16')

7. Apirodiur sp. 86-UW 8. Apkudiarsp. 86-0310 9. Aphodiur pseudolividus Baltharar 10. Aphodiusfrenrhi Blackbum I I.Anhrwliur ~'runonur (L.1 12. Procrophoner 1?J srulp1u.s Hope

Nil)

LE

-

~

Huh

PHF

16 7 4 9

N

3

3

'I

5 4 5 4

!'

H

!'

H

7 5

'! U

H

U

P

!'

111: 1111

U

6

..**...

CIF

P

?

P

1

PH

PI1

park i s irmb heath mosaic on laceritis landplain. Sampling was crmed out with live dung~baivdp8Lfall traps 10 m apan in a line Trap pailions were pennrnenl and traps were ret for a m week every month. November l982-Octeher 1984. In each trap 7 cm1 0 1 frcsh human dung was used as bail. placed on w d e n skewers over a waxed p a p ' cup 7U I XU mm. sunk so that the rim was l c v d wilh she mil surface. E(hy1cne glycul was plnccrl in himm or each trap as an udorlerr prrsenalive. Trap +ala fmm Riddill-Smith & H a l l (1YWbl. ltrhildl p"rferenceda~rarefrumacompariionolvappingrrrulsinpraure1PI. hcnhIHIandupenjunzih furer, IF); none 01 dung beetle species Irappcd I I Badgingarra showed a prefcrcncc four cloxd kani Brcrf 1Ridadill-Smithet al. 19R3: Mallhcwa 19721. A l l bpccier prelcmd human dung OYCI canion bails IRidrdlllMmilh e l al. 19831. bur we_ trapped II both human- m d callle~dungbaits. Spec~csc d e numbers arc AustralianNalvmal Insect C o k t i o n voucher numkrr. N. 1 0 ( 3 nuinher of individuals collectcd. Dots (.I and asterisks (11 under " S ~ ~ ~ ~ w i l lqi lmys' 'e n l ab5ence (I prescnce of the species in xampler from March through Seplcmbrr. Norm: Vegetation tn

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Index of the Genera in3carabaeidae

For each genus is given: the author's name, the year of publication, the tribe (CA, Canthonini; CO, Coprini; DI, Dichotomiini; EC, Eucraniini; ER, Eulystemini; GY, Gymnapleurink OC, Oniticellini; OP, Onthophagini; OT, Onitini; PH, Phanaeini; SC, Scarabaeini; SI, Sisyphini), the number of described species, and the page numbers where the genus is mentioned in this book. This information gives a visual impression of our ecological knowledge ofthe genera.

No.

GenudAuthor

Year

Tribe

Acanthonitb Janssens Agmopus Bates Aleiantus Olsoufieff Allogymnopleurus Janssens

1937 1887 I947 1940

OT CA CA GY

Allonitis Janssens Alloscelus Boucomont Amidno Cambefort Amphislomw Lanskrge Anachalcos Hope

1936 1923 1981 1871 1837

OT OP

Anisocanrhon Man. &Per. Anoctus Sharp Anomiopsoidcs Blackwelder Anomiopur Wcslwoad Anonthobium Paulian Anonychoniris Janssens Anoplodrepanus Sirnonis Aphengium Harold Aphengoecur Piringuey Apololomprus Olsoufieff Aptenocanthon MaIthews Aptychonitis Janssens Arachnodes Weslwwd Ateuckus Weber

1956 I875 1944 I842 1984 1950 1981 1868 1901 1947 1974 1937 1837 1801

CA DI

1859 1986

CA CA

Aulacopris While Baloghonthobium Paulian

I

OP CA CA CA OP EC DI

CA OT

oc DI CA CA CA

OT

Pg. No.

Species 1 4

20 19

I

4 4 21 8 4 5 8 29 6

216 142, 144,14&47,256,

277, 307,320,383, 388,394 66,200,405

200, 203,205,405,408

182, 189,256,258 64,147, 155, 163,320, 383,388,394

21 5 , 2 2 I , 4 I2

1

2 2

2 8 3 3 . 69 79 3 1

60

256,258 205-206 58, 118, 129,2l1.21& 18, 223,228,286. 289.411 25658

I'

466

'

IndexofGenera

IndexofGenera

Bdelyropsis Per. Vulc. MaR. Bdelyrus Harold Bohepilissus Paulian Boibires Harold Bolefoxapter Matthews Bubos Mulsant

1960 1869 1975 1868 1974 1842

DI DI CA PH CA OT

3 2 I 2 3

Byrrhidiwn Hamld Caccobius Thomson

1869 1859

CA OP

3 88

3

Caeconrhobiwn Paulian Cambeforranrus Paulian Cambeforrius Branco Coruhidium Erichson

1984 1986 1989 I847

CA CA OP DI

I 9 153

Conrhochilwn Chapin Canchon Hoffmannsegg

1934 1817

CA CA

13 146

Canrhonella Chapin Canrhonidia Paulian Canrhonosoma MacLeay Coruhorrypes Paulian Cassolus Sharp Corharsius Hope

1930 1939 1871 1939 1875 1837

CA CA CA CA OP CO

Cephalodesmius Westwood Chalcocopris Burmeister Cheironiris Van Lansberge Circellium Latreille Cleprocaccobius Camtefon Copridaspidus Boucomont Copris Muller

1841 1846 1875 1825 1984 1920 1764

CA DI OT CA OP CO CO

I

II 2 3 1 7 90

3 I IO 1 24 1 I85

26.58 26, 58, 216

256,258 101-102, 104-106, 1 1 0 13,254,269, 271 102, 107, 165, 245, 332, 334, 381. 386, 390. 397,406,408,414

390,397 30,58, 118, 21 I , 21417,220-23. 225-26, 228.307-308.41 1 214 4345. 57,118, 121, 129, 132, 21617, 22fL22. 225-28, 256,291, 307-310,3l&20,323. 356,4l I 214. 216

Coproecus Reiche Coprophonaeus Olsoufieff

1841 1924

CA PH

Coprodacfyla Burmeister Coptorkina Hope Cryprocanrhon Balthasar Cyobius Sharp Cyprochirus Lssne Delopleurus Erichson Delrepilissus Pereira Delrochilurn Eschschnltz Delrorhinum Harold Demarziella Balthasar Dendropoemon Perty 1. Diabrocris Gistel i Diasrellopalp~sVan Lansb. Dichoromius Hope

1846 1830 1942 1875 1900 1847 1949 1822 1867 1961 1830 1857 1886 1838

CO DI CA OP OC DI CA CA

DI DI PH PH OP DI

1 4 6 2 81 I 14 25 3 23 148

Digironrhophagus Balthasar

1959

OP

18

Diorygopyx Matthews Disphysema Harold Dorbignyolus Branco Drepanocerus Kirby

1974 1873 1989 1828

CA OP OP OC

8

Dreponoplarynw Boucomont Drepanopodus Janssens Endroedyolus Scholtz Hoyden Ennearabdus Van Lansherge Epacroides Olsoufieff Epilissus Reiche Epirinur Reiche Eucronium Blullt

1921 1940 1987 1874 1947

OC SC CA EC CA CA CA EC

I 28 13 18 I2

256.258 54. 66, 142, 144, 148, 153. 155, 16849, 175, 181-82, 187-88, 193, 207, 289, 323, 353, 384,388, 395,405, 408 29-30,49,62, 256,258 66, 101, 245, 256 41,43,45, 316 48, 164,332. 390,397 41, 43. 49.58, 61-62, 64,66, 81, 100-102, 107-108, 110, 118. 127-29, 142, 151, 154, 168-69. 172, 175,182, 185, 187, 18&89, 208, 213,21617,224-25.

I

1841

1841 1834

'

467

244-45, 25657, 2 7 6 77, 289, 308, 310-11, 317-18.323-24.35354,381, 384,388, 395,401,403,405, 408,411-12 25657 126,213,216. 219-20, 307,336,412 62,25657 64,167, 388, 395 118,214,219 183, 185-86,401,404 164, 384,388,396 64,167,395 118, 214. 216. 227, 412 62,25657 318 166. 200,397.406.408 30,54,58, 118, 121, 127, 129, 132,213, 215-18, 220,223-25, 227,382,412 41, 67. 95, 131, 143, 147, 152-53, 166, 168, 237-38, 240,263-68, 272-74,277,286. 29495. 297, 298, 300-301, 303,368, 390, 397,414 256,258

1

1 25

1

2 1 1

2 I 23 7

143, 164-65, 16748, 386,390,396,405, 414 200,405

468

.

IndexofGenera

1840 1953

Eudinopus Burmeisfer Euoniricellus Janssens

CA OC

1

17

Euonrhophagus Balthasar

1959

OP

33

Eurysternu~Dalrnan

1824

ER

26

Eusaproecius Branco Falcidiur Branco Falsignambia Paulian Garrera Janssens

1989 1989 1987

OP OP

7 I

CA

1940

GY

20

Gillerelius Janssens Glyphoderus Westwood Cromphar BmllC Gymnopleurus Illiger

1937 1837 1834

OT

2 3 4

1803

Gyronotus Van Lansberge H a m m o n d a m s Cambefon Hansreia Halffter & Martinez Haroldius Boucomont Helicropleuncr d’Orbigny Heliocopris Hope I

Hereroclimpus Peringuey Heteroniris Gillet Hererosypkus Paulian Holocanrkon Mart. & Pereira Holocepkalur Hope Homdorarsus Janssens Hyalonrhopkagur Palestrini

1874 I978 1977 1414 1915 1837

1901 1911 1975 1956 1838 1932 1989

EC

PH GY

CA CA CA CA OC

D1

1

52

5 1 1 15

53 49

OT

8 5

CA

1 1

OP

OC DI PH OP

31,33,41,66, 102,107, I 10. 147, 152-53. 168, 237-40,245,246, 25&57, 263-70,27275,277,286,297, 300-303, 310,381, 384, 386,390,396, 397,405,414,420 102, 107-108, 144. 245, 381,390,397 ll8.214,2l7,221-22, 412

166,291,320,339,383. 388,394,405,408

42,44, 105, 107, 147. 164,166, 168-70. 172, 180.245.307-308, 310,320,339-41.383, 388,394 101

182, 194,401-402,404

8. 10,41,48-49,64,65, 148, 151-53. 164. 16748, 175-76,201. 206,208,289,295, 307,310.316,319, 323,332,334,336, 340,353,368,370, 384,388,395,405, 408 408 167. 176,295,353,396

3

I

9

48,166,397

Hypocanrhidium Balthasar lgnambio Heller Isocopris Pereira &Man. Janssensanrus Paulian Janssenseilus Cambefort Kheper Janssens

__

1938 1916 1960 1976 1976 1940

IndexofGenera

DI CA

DI

I

3 2

sc

22

OT OP

1 1

1

Kolbeellus Jacobson Krikkcnius Branco Labrom Sharp Lepanw Balthasar Liarongus Reitter

1906 1989 1873 I966 1893

CA CA OC

3 26 38

Lirocopris Waterhouse Lophodonitis Janssens Macrodcres Westwood Madapkacosorna Paulian Madareuchus Paulian Malogoniella Martinez Megaloniris Janssens Megaponerophilus Janssens Megathamis Waterhouse Megarhopa Eschscholtz Megathoposoma Balthasar Melonoconrhon Halffter Menrophilus Lapolte de Cast Metocathamius Paulian

1891

CO

4 1 13 3

Milichus Ptringuey Mimomhophagus Balthasar Mnemaridium Ritsema Mnemarium MacLeay Monoplisres Van Lansberge Namakwanus Scholtz & Howden Nanos Westwood Nenreuckw Gillet Neomnemarium Janssens Neoniris Peringuey Ncosaproecius Branco Neosisyphus Muller

1938

1876 1975 1953 1961 1937 1949 1891 1822 1939 1958 1840 1939

OT DI

CA SC CA

OT OP PH

1

9 2 1

2 4 2 61

1901

OP OP

8 2

1883 1821

SC

1874 1987 1837 1911 1938 1901 1989 1942

I

1

sc

4

SC SC OT

1 I2 1 1 2 2 24

CA CA CA

OP

SI

7,41,43-45, 1 4 4 4 5 . 147. 149-53, 155, 163 290-91,295,302,307 308,316,319-20, 323-24. 327, 332,339 368,370,383,394

25657 256,258 41, 118, 143, 152, 182, 256,26468,277,286 289,303,309,384. 397,405.408 175,388,395 66,200,405,408

214,216

1

CA CA CA CA CO

1963

469

I

CA

OT

’

6

51.57 44, 128,219,339 57, 118 25&57 66,168-70, 175,323, 384.388, 395,414 166, 384,390,397,406 20&201,406,408 65 256-57

41,45,48,66,143, 15253, 163-64, 166, 170,

470

.

IndexofGenera 175-76, 205, 207, 256, 263-68.272-74, 27677,2n6,30a-301,303, 307-30~,315.317-1n, 320,323-25,332, 340, 342, 388, 394,405,

Nesosisyphus Vinson Nesovinsonia Marl.& Pereira Odontoloma Baheman Ofrcanthon Paulian OniticeNus Lep.Au&Serv.

Oniris Fabricius

1946 1959 I857 1985 1828

1798

SI CA CA CA OC

OT

4 1 20

408 60, 66

383,394

I

9

153

Ontherus Erichson

1847

DI

36

Onthobium Reiche Onthophagus Latreille

18M) 1802

CA OP

13 1765

4 , m , 38-39,41,43,47, 137, 148, 153, 164, 167~jn.202,238,7.98, 305.306,3l2-l3.322, 324,387,390,397, 405,408,414 41,48,65, 101.14n-xj. 152-55, 166, 172, 193, ZOI,208,23740. 25657, 26348, 27175, 277, 300-301, 311, 313,317,323-24.368, 385,388,396,405. 408 58, 118,214.216,225, 412 1 9 , 3 2 , 4 w i , 44.48, 51,58,61-62. 64, 81, 95. 100-103,105-114, 118. 129-32, 143. 148, 165-67. 169, 171, 177, 1 8 ~ 2184-87.189, , 190-91, 193-95, 201. 204-206,208, 213, 215-23.22628.24346,248-49.253.25659,264-72, 274-75, 277,286,291-92, 29695,297799, 302303,309-10,316,324, 328,339,351,359, 368, 381, 382, 385, 387,390,392.397401,403,40&409, 412,414,416, 420

Onychothecus Boucomont Oruscatuen Bates Outenikwanus Scholtz Howden Oxysternon Laporie de Cast.

1ndexofGenera

-191% 1870 1987 1840

DI PH CA PH

2 2 I 15

Pachylomera Hope

1832

SC

2

Pachysoma MacLeay Panelus Lewis Poracanrhon Balthssar Parachorius Harold Paragymnopleurus Shipp

1821 1895 1938 I873 1897

SC CA CA CA GY

II 19 4 4 13

Paraphytus Harold

1877

DI

13

Paraniticellus Balthasar Pnronrhobium Paulian Peckolus Scholtz and Howden Pedaria Lapone de Cast.

1963 1984 1987 1832

OC CA CA DI

1 I 2 34

Pedoridium Harold

1868

DI

II

Penalus Paulian Peyriermantu Paulian Phacosoma Boucomont Phacosomoides Mart. & Per. Phaedorrogus Paulian Pholops Erichson

1985 1976 1914 1959 1985 1847

CA CA CA CA CA OP

I 1 IO I 37

Phonaeus MacLeay

1819

PH

53

Pinacopodius Branco Pinacorarsur Harold Pioryoniris Janssens Plewoniris Van Lansberge Ponerorrogus Silvestri Pioagoderus Van hnsberge

1989 1875 1942 1875 1924 1883

OP OP OT OT CA OP

I 3

105

Pseudmachnodes Lebis Pseudignambia Paulian Pseudocanthan Bates Pseudochiranitis Krreira Pseudocopris Ferreira

1953. 1984 1887 1977 1960

CA CA CA OT CO

3 2 8 2 2

’

471

zi3,2i9,222,307,3on 310,323 30, 144, 147-48, 170, 308,383 133-34 53, 334,402

65,184.188-89,307, 308, 310, 355, 401, 403 26-27, 64, 200, 203, 405,408

48,64,165. 167-68, 207,332,385-86,381 39596, 408,414 214. 216,225, 227, 334 412-13 182.18~1

1

30, 166,386,392,400, 414 24,30,43,ni, i i 8 , 1 2 1 126, 127-29, 131-32, 213,21619,222. 225-26,228,307-309 335-36.382.413

3

3 1

66, 165-66.339 166,292,392,400,407, 409,414 256, 258 118,214

.

472

.

.

. ..

IndexofGenera

Pseudonthobium Paulian Pseudopedmia Felsche Pseudophacosom Paulian Pseudosaproecius Balthasar PseuduroEys Balthasar Pteronyx Van Lansbcrge Pycnopanelus Armw Saphobiamorpha Brookes Saphobius Sharp Sarophorus Erichson Sauvagesinella Paulian Scaptmmemis Eringuey Scarabaeus Linnaeus

Scarimus Erichson Scaronomus Erichson Sceliagcs Westwood Scybalocanthon Mariinez

Scybalophagus Maninez

Sikoranrus Paulian Simpisom0 Boucomont Siwdrepanus Simonis Sisyphus Latreille

1984 1904 1975 1941 1938 1874 I931 1944 1873 1847 1934 1901

1758

1847 1835 1837 1948 1953 1976 1928 1985 1807

Sphaerocanthon Olsoufieff Sriptocncmis Branco Sliplopodius Harold Stiptomrsus Branco Srrandius Ballhasar Srreblopus Van Lansberge Sulcophanaeus Olsoufieff

1947 1989 1871 1989 1935 1874 1924

Sylvicanthon Halffter Marf. Synapsis Bates

1977 1868

CA CO CA

OP DI DI CA CA CA

DI

CA

oc SC

DI DI

SC CA CA CA CA

OC SI

CA

OP OP OP OP CA

2 2 I I2

I

1 3 I 13 4

3 I 94

8 9 6 16 6

I I 6

30

2

PH

14

CA CO

12

5

Tanzanolus Scholtz & Howden TernnoplectronWestwood Tesserodon Hope Tetraechma Blanchard Tetramerein Klages Thyregis Blackbum Tiniocellus Peringuey

4w

Tornogonus d’Orbigoy Tragiscus Klug Frichillum Harold Tropidonitis lanssens Uroxys Westwood

144386 25657 31,33,3&.37, SI, 65, 101-103, 105, 107108,11CL11, 114. 14 163.245, 307,309, 320,323,339,381, 383,388,394 118,227,413

VulconoconrhonPer. &Mart. WalteranrusCambefort Xenocanrhon Maninez Xinidium Harold Zonocopris Arrow Total number of genera : 234 Total number of species: 4,940

167 214

4144,51,57-58.60, 66, 102, 105, 107-108, 1 1 1 , 114, 118, 14244. 148, 153, 162, 166, 168-70, 172, 175-76, 201,203205,207, 214,245,307-308. 310,319-20.324, 34142,368,381, 383-84, 388,394,405, 408

23 2 9 4 0 9 2 17

IndexofGenera

‘i

200,205-206,405,408

iI

I

392,4OQ,407 126,213,215. 226, 228, 413 66,353

!

1987 1841 1837 1843 1907

1904

1901

1904

1855

1868 1937 1842 1960 1977 1952 1869 1932

..

CA CA CA CA

PH

1

15 13 2 1

CO

4 6

OP

2 1 19

oc

oc

DI OT DI

CA

1

55

1

CA

1 3

DI

CA

1

. 473

189. 256,258 182, 189.194,256-57 62,25657 168, 182,201,387,390 397,405,408 200-201,407,409 58, 21&-15,218, 334

58. 118,211,214-15, 218,225,228,334, 413

1

OP

.

32,57,215

abundance, 5.95. 1 6 W , 16S70, 267-68, 271-72; complementay changes in, IS& 89: distnbution, 72.91, 187-88, 251-53, 295-96.363; of introduced species, 264; seasonal, 263-65.269-71; andsize. 17677

activity, 263. 266, 269-71; diel, 15.46. 54, 72, 86.90, 128, 148-49. 170,203.221, 225,290,322, 336,33a39,345,355; sea ronal. 203-204,259,296 adaptive: nesting behavior, 237-39; radiation, 54 Aegiolio, 51 Africa, 5.63-67, Ch. 9, Ch. 11. Ch. 16, Ch. 17. Ch. 18.352-57,359-64,370-71.374, 376, 378.379, 383-87.414

Afmdiiopternn, 200

aggregation. 12, 128; aggregated distribution. sec distribution: causes of. 289; conequenca of. 291; correlated lraill, 287; density dependencc of. 285; interspecific. 90, 284. 289-90, 335: inmpccific, 172-73, 284. 286; measurement of. 284; spatial, 72 Agoliinus, 243 Agoiius. 243 Agrilinus. 243

Almcharinae, 233 Alountta, 221 Amides. 213

ancertal: Coleoptera. 22; habits, ZZ; strocuues, 22 Anoplowupcs, 246, 249 Anorylus, 191

Anrhicidae, 233 ants, 32.67. 121, 180,216, 225,236 Aphdiidae, 6.22-23.29.39, ch.5.98, 100, 108, 110, 114, 123. 133, 1-9, 200. 211,213, 233, 235-37, 240. 246, 258. 352,401~02,410,414 Aphodiinae, 6.27.29. Ch. 3,51-52.63, 16041.200,208.322 Aphodiires. 51 Apiomerus, 223 A p M i u s , 6, 27; 29-30, 38-41.51, Ch. 5, Cb. 6, 13LL32; 185. 197,213. Ch. 14,

294-97, Ch. 17. 335,33~0.34243.35~~51,356,35a 59.362. 380,401, 404,410,41620 aptcry.42.45, 133 arboreal foraging, 184. 196, 334; species, 259,27C-71,289,291.

57,204 Argiope, 223 Artemisia, 106 Asia. Sce South-East Asia Ammius. 213 Atlo, 216, 225

Aulonocnsmidae, 23.26

Australia. 6 1 4 3 , 135,Ch. 15, Ch, 16, 313, 315, 321, 325, 332, 334, 340, 354, 3 5 6

57,359-61, 367, 317. 379

bacteria. 28, 31 bark and ambrosia beetles, 333 bats, 220, 223-24 beetle: microphagous, 23; microtypal, 52.54 behaviol: breeding, 36, 72, 83; foraging, 72. 290:population dynamic consequences, 314

biogeography, 5147,72,78; ofdung beetles. 181;island, 193 b d y size, See size Bolbocsmtinae. 23, 52 Bolboceratini, 256 Bolboccrm, 51 Bolbocemmnur, 186 Bolbachromus, 185-86,402,404

Bomeo, 182, 187-90. 193,353,355

Brachypodium, 104, 114 Braconidas. 121 b e d i n g . Sec behavior breeding

bromeliads, 26,216 brood. See dung ball buffalo fly, 137,260,299,358 burying b n l c . See Nieropholus bush fly, 299.358 csecotrophy, 28

Colnpltwlus, 415 Calliphoridae, 8, 123, 128. 180. 191.202. 291

476

.

Index

C m p s i u r q 7.02 Canthonini, 44-45, Ch. 4. 161. 163,210, 214,256-58.336.355, 360, 362 Carabidae, 236 ca+ohydrateJ, 26.42 carrion inscn community, 123 cattle. I W I O I , I59,23141,255;dung, 18, 356; dung bufial, 112113,268,278; dung production. 232-33; dung quality, 274-75 caviomorphs. 57.59 Cebus, 228 cellulosobionl, 31

Cernlolnrpcs, 132, 244 Cerqwn. 90, 129

Cetoniidac, 6, 183, 202 Chaerodur. 213

Chimnidae, 6 , U-23 Chriwdpha, 402 closuidia, 28, 31

caxistcnce, 5. 12. 284.342, 371: bascdon resoura pMitioning. 330: of competitors, 9. 173, 291; facilitated by aggregation, 11; mechanism. 330: model, 326: regional, 9, 15: and size differences. 334: trade-off. 328 Coilde8, 213 Colobopuridiw, 200 colonization of resource patches, 12 community: cmuihgal smcture. 348: differences among continents. 359; imp-ished, 131: island, 193; mnrandom m i c Nre.346:strurmre. 12. 14. 114, 123, 171.

26&67,271.358.367;tempralslability. ..

37 1. Sec olro dung beetle

compelition. 37-38.44.48,52,59,62,61, 66, 188.284,305, 366; ability. 324; asymmchic, IS. 20, 154,321,356: and body sire, 289; coefficient. 291; Cocxistc-, 173; in dwellen. 312: exclusion. 5, 195: expaimcnt, 31 I; for fmd. 29,37-38,45, 138, 154,306,312: hierarchy, 309.321. 323: inlase. 15% interference, 72, 305306,309,367; intcrspcific, 11-12. 128, 152-53, 1 7 f 7 4 , 274.276.303. 308; intraspecific. 11-12, 15253,27%74, 307; intmduced species. 276: in larvae. 37-38, 306: lottery. 315; model, IO, 325; moderate. 48; and nesting type. 45: pmmptive, 310: resou~cc.72, 197,305,310, 367; in rollers, 114. 169, 171; 306;scmmble. 314; seasonal, 172; severe, 44,forapace, 37-38; t h q . 14: p.de-off. 324,327; in lropical

Index forests,322; in mnnelers. 114, 172,312, weak, 210 compelitor: inferior, 169.202: superior. 172; unsuccessful. 213

Coprini, 45-46, 48, 53.55, -1.

114, 161, 175-76. 180, 187, 203,213,25657, 287, 289, 313,316,332,336,339 laxonomy. 34

copmbiont. 31 copmphagy. Ch. 2 copulation, 4 3 4 5 c m species. 9 6 9 5 comiation, spatial. 90 Corsica, 309 Cuba. 297 Daseilloidcs. 51 Dmyprocra, 228 density compensation, 31S-14 Dumaptcra.36 desen. 121 developmmtal lime. 8.49. 82,300 Diomcsrw, 402 diapause. 341 Dicholmiini, 46-48, SI, 53.55. S7-59, 62, 65. 164,203, 206, 210,21%14.336. 360, 362

diel. Sec activity diel. See dung beetle digestion, larval, 49 dinosaun, 51 dispersal, 54. 61. 222-23, 29495 dishibution. 54. 100; aggregated. 89, 283. 36% changes in. 94; clevstional. 15, 72. 188-91,249;excludve. 86. 189, 195-96.

286: geographical, 75, 182; paltcm. 118; random. 286; relict. 360; small-sale. 83; venical in forest, 20%206 diurnal. Sec activity diversity. See species diversity dormancy, 2-31 Drosophila, 292 Dryomyza, 8 dung: amounl buried, 317; ofbirds, 162,215; ofbison.81; burial. 127, 161.239:ofcarnivores. 162. 331: of cattle, 48; ofele. phant, see elephant: of herbivores. 42. 159, 201;insect community. 5, 16. 18. 72, 12w 21. 137, 15941,250, 356; of invertcbrates, 215; of mammals, 28-29, 136-37; ofmarsupials, 62-63; of monkeys, 226-27;

477

'

of nonherbivorss, 31: of omnivores. 42. 367; high, 47; lifetime, 39.41.43, 328; \ 159,201; pellets. 30.58, 104. quality. 16, 'IOW. 45-46.316 42,340; of reptiles, 162,215: of rumifeeding: mafllration, 32.40, 42,294 nants, 32: of small mammals,53; of toad. fernentation chamber, 31 162,215: types. 16,30. 106, 147, 159; flight, 42,21521 lype selection. sec food: of zebu. 231, 233 Right-oogenesis hypothesis, 294 dung ball, 29; for brood. 27-28.44-45, 47. fly: dung-breeding, 8, 15-17, 1%20, 12CL21, 49; burial, 45; competition for, 44,305128, 137, I61,202,223,23S,291,299, 306: conruuetian. 30, 61; fossil. 51: "up 356.35a59.3~ lid, 44; parasitized, 48; rate of COIISVUEfmd: malen. 28; relwalion, 226-27: sealion, 308, 319,323; rolling, 30,44,207, sonal shill in use. 332; selection, 72, 85, 228, 317; sire, 319, 321 16-67. 186,21416,259,331-32,335, dung beelle: biomass. 145; bumws, 27; clar345; web, 16-17, 19.78.235 sificalion, 368; clutch size, 39; density, 85, foraging: behavior, 184: modes, 21%22: opti92: diet. 23, 3&31; endothermy in, 44, mal, 84,283 flightless, 42, 45: fossil, 93; functional forert-savsnna comparison, 198,208-10 forest clearance, 77, 119 gmup. 137-40: intmduction of. sec inmfossil. 51 duction; type I. 367.371; type 11, 367,371; fungi, 7, 15, 28.32. 167 m s . 36 dweller, 36. 39. 139. 208 hmgivore, 8,292 dynamics: locally cornlaled, 294. 296; lottery, Ch. 1.85,292,314.362,369; me&gacnlions per year. 39,43, 162 papulation. 293; variance-covariance. Ch. genetical isolation, 54 I,85,292, 314,362.369

ectoparasite, 32. 57-58,63 egg size, 42 elephant,48, 136, 148. 159, 181.198-99. 201-202.339.353 Elephasromlct. 256 elevalion. See dishibution

emigration: density dependenl, 83, 89. 312, 314-15; experimental study, 83 endemic s p i e s , 182,258

Eacenc. 52

Eurystemini, 45, 51t59. 214.336 Eucraniini. 55,57-58, 214. 336 Eulissus, 223 Eupariinae, 26-27.52 Eurasia, 63-67, 362 Europe, Ch. 5,286-87,294,299,309,340, 34243. 354.357-59,364,373,376, 378. 379,380. 381 evolution. Ch. 4 excrement. Sec dung extinction, 101, 136, 156, 211-12. 260, 364: Plektoeene, 81,295,353

fast-burying tunnelers, 139 fecundity, 45-47, 54.82, 151-52, 300, 327,

G e o q e s , 27.46, 75.78. 82, 85. Ch. 6.

121, Ch. 14,256,351, 380. 381 Geompidae. 6,22,27,29,51,81, 84, 98, 100, 108. 114. 118, 133,244-46.256-57, 352,401-402

Oeampinm, 6,2530. C h 3.52.63, 84-85. 118 Gcowpini. 256 Gdndwanian. 52-54.57.61.64 grasslands. 53. 58; subtropical, 136, 143: mpical, Ch. 9 guildsofdungbeetlea. 138, 161. 292 Ouiman SBY-, 156-57 Gymnopleurini, 44-45.55.6445, 161, 163, 165-66. 176,210,289,315.336.339,

348

habitat: selection. 14.72.78, 80.86. 88, 145. 194,258-59.34142; specificity, 142 Haemarobio, U],260. 358 Hawaii. 297 Hmotherida, 57 Hcpmulacm, 24546, 249. 252-53 hibernation. 39, 82 Himalayas, 352 Histcr. 299 Histeridae, 120-23, 137, 160. 233-36. 358 Holamic, 53-55,57, 60.62, 66 howler monkey, 227

478

.

Index

human colonization, 259-60 humus, 23, 2 6 3 0 ; high quality, 31 Hybosoridae. 6. 22. 51. 118, 133,Ch. IO. 211, 213.258,312.352.401-402 Hydmphilidae, 6, 83, 120-23, 137, 160.202 233.250-52 Hydmlaeo, 8 Ichnsumonidae. 121 immigration, 322; density dependent, 287; rate, 310-11 Indo-Malaya, Ch. IO Indonesia. 341 introduction: to AusIdia. Ch. 15,260, 262, 275-78; dung beetle, 19.78-80.95.297302. 367; effect on native species, 278. 302: effect of fecundity. 302; failure of, 275-76; to No& America, 125L3I: success of. 275-76 Jamaica, 59-60 Japan, 309 Java, 182 Jurassic, 51 K-species. 80, 82. 151-52, 367 kleplopmsio, 38.48.64.82, 139. 16+65, 227, 240,322 Koshmmc-hibviur, 415

', ,

Lamellicomia, 23 Laparosticti. 2243.26, 51; list of taxa. 25 Lathridiidae, 233 Laurasia, 52 Leisralrophur, 223 Lcptodiridae, 123 Lethrinae. 29 lifehistory: paramtfns, 41,153; svategy, 151; trade-off.317 limiting similarity, 309 Liplorochrus. 189 longevity, 41 Lordilomaeus, 410,415 Louddia, 159 Lucilirr. 8 Luzon, 182 Macrochelidae, 17 Mmmpocoprir, 63 Macmpur. 63 Madagascar, 6446,297,360,363; uopical fonst in. 205-u16

Index Malaysia, peninsula, 182 mammalian: exunction, 136: paor fauna, 207, rich fauna. 206-207; megafauna, 65; size, 176 mammoth. 61 mandibles: biting, 22; filtering, 22-23, 30; intermediate, 23; hmertelic, 23 marsupial, 53.57.61; dung. 6 2 4 3 mate choice. 44 maternal care, 43.4648, 368 Mauritius, 60.66, 299 Mediterranean: climate, 134; region, Ch. 6 Megocephnln. 223 Megotelus, 414 Mcllivora, 49. 370 Melolonthidae, 26 Mesontoplays. 240.415 Mesozoic. 51 metapopulatian. 293. 295 Mexico, 116.373.378.382: m s i l i o n zone, 56. 118 micmorganism, 27. 31, 42 Middle East, 299 milliped, 167, 216 mimicry, 1 6 S 6 6 Mindanao, 182 Miocene. 5 I mile, 17. 20, 137, 235 modern taxa, 54.57.64 Moluccas, 182 montane: forest. 123: habitats, Ch. 14; insect communities. 252-54; species, 1 9 2 , 2 4 5 50

morphology: adapted to digging. 324; legs. 318; rollcn. 317: tunnelen. 317 mouthparts, 24,26,32 movement, denskydependent, 83 Musca, 19,260, 358 Muscidae. 17. 121.235 Muscino. 17 rnycetophagy, 63-64 Mydoea. 17 myrmecophily. 32, 61 Ncagolius, 243 necrophagy, 27. 32.42.45.59. 122, 167. 202,216,312. 333, 355 nematode. 15-16. 20 Neotherida, 57. 59 Neotropical. 211. 361 nest, 8, 27; architecture, 313. 342; building,

30: depth in roil. 84. 319; numberof. 316; primitive. 29.3% rate ofconsmction. 323 types, 4 6 4 7 nesting: alternativc behavior. 325; Aphodiur, 3 9 behavioral advantages. 27; behavior, 1 0 , 3 6 , 4 2 4 3 , 238-39 cost of. 40,expetimental, 5 9 pattern, 44.46; sequence, 45 New Caledonia, 62,297 New Guima, 62, 65, 182, 192, I 9 4 9 5 New Zealand. 62,367 Niaiur, 23637,240,415 nichc: complementary, 87; differences, 85, 88; ovcrdispened, 346, overlap. 87 Nicrophoncr, 7-8. IO, 15.27, 180, 185. 189, 191, 195, 402 Nitidulidae, 123 nitrogen, 32 nocturnal. SEEactivity North America, Ch. 5,297,303, 343.354, 357-58:subtropical, Ch. 7,335,373.378. 382 old taxa, 53-54, 57 Oligocene. 51, 57 Oniticellini. 4-8.55. 60. 161, 164. 166. 175-76,203,206,210,213,289. 332. 336. 339 Onitini. 4 6 4 8 , 55, 58-59. 65, 112, 164-65. 203,336,339 112, Onthophsgini, 4 6 4 7 , 5 3 , 5 5 , -62, 161, 164-66, 176,203,206,210. 213, 256-58,289,294,336 Orodolus. 237 Orphnidac, 23 ovary. 3940.42-43 uviparitian, 45; density-dependent, 83.312. 315 Oqomus, 107, 246 Oxytcllnae, 233

pair bond. 29.42

Palawan, 182 Panama.. 57.. 59.309.332.341.379 , . . . Pangaca, 52 parasite, 8 , 19, 121; of dung beetles, 137 parasitic dung beetle. See Weplopamsite panntal: care. 36,43, 328; care inhibits Rproduction, 43; investment. I S 1

Passalidae, 36. 203 patchy habitat, 6 7 , 2 8 3 Pccrinicornio. 23

~

.

479

perching on vegetation, 41, 72, 184, 186. 205-206,219-22.355 Phaeochmops, 191, 1 9 6 9 7 Phoeochrous, 184-85. 187. 1 5 9 7 , 4 0 2 Phanaeini. 46.55, 5 a 5 9 . 6 5 . 126.213, 219, 336 Phoraphdiur. 415 phenology, 247; dung beetle types, 169 pheromone, 4 2 4 3 , 4 6 , 9 0 , 2 9 0 Philippines, 183 Philonrhus, 191 phoresy, 215, ZZS. 259 Phoridae. 123 Plorydroeus, 161. 191 Plcislofene. See extinction Pleumplrodius, 414 Pleumdicti. 26 polwhw. 7 predation, 314, 358; by dung beetles, 32; on dung b e a k s , 72, 370; frequency-dependent, 11 predator, 120-21, 220,223-24, 250, 274, 359: of dung beetles, 137, 1-1. 165; generalist, 11

predatory: beetles. 17, 20, 35659, 366; flies, 17 Pr~Iophones.420 proteins, 26.28. 32 Psommodiur. 415 Psychalidae. 121 Ptemmalidse, 137 Pupit0 Rim, 297

r-species, 82, 151-52. 302, 367 rain fon81.2627, C h 10-12 rareapaies,91, 94, 181. 187.295, 335, 342 ratel, 49.370 recognition: mate, 44;sex. 42; species. 42, 189, 291 relicl. 45, 53, 60.62, 64 npmduetivc strategy, 272 resmrc~c:in excess. 202: multidimensional panitioning, 345: partitioning. 14, 72, 141, 186, 330; patch hetemgeneity, 290, selection in uopical forests. 333; spatial partitioning, 341: temporal panitioning, 3 3 6 utilization, 28. 227-28; roller. 36.43, 16163,207,227; campetilion in, 114. 169, 171; afdung pellets, 227; large, 139; papulation biology of. 370: amall, 139 spatial disuibution. 105

480

.

Index

sacred scarab. 37.65 Sahel region. Ch. 13,313,359.376 saprophagy. Ch. 2, 53,58,62,78.80,82,

86, 19697,248; hard, 22;soft, 22, 203 SqprosifEs,51 Sarawalr, 189-90,192, 196,355

Ssrcophagidas. 123 satcllilt species. 95 savmna, 136;Uopical. Ch. 9 Scarabaeidas, 6,22.23,81,9&1M), 108, 133. 18IL81. 183. 187, 191.2W.211. 3 5 2 , 3 8 a 8 9 , 3 9 4 , 4 0 1 . 4 ~ , 4 0 8414; , tu onomy. 34 Scarabaeinae, 45 Scamhaeini. 43.45.55, -5, 114,210, 289,315,336 Scatophaga, 8, 17. 283 Scatopsidae, 121 srawnal. See activity seasonality, l5,72,87-88. 109, t49, 16a 69. 183,216,218,234,339.345;differences due to competition. 87;lack of, 184, reversed. 110 sesegation. ecological, I97 Senobasir, 223 Sepsidae, 121,235 Se-, 194 sex ratio, 91 aex. eneountcr Of, 46 sexual: coopedon, 44.4748; display, 46 Silphidae, 8.27.44, 122, 180. 191,401402 Sisyphini, -5. 55. 6U+I.M, 16142,

',

..

164.203,206,214.287,289.315,328, 336,339 size: and abundance. 17677;eatcgory, 145; difference. 72.87-88, 1%. 334.348; 6s. Iribution, 33637. 345;ofdung ball, 320; ofdung beetle. 125-27. 167. 170, 176. 202,206,328,345,353;of dung pat. 167; effect on coexistence, 335;evolution, 353; limiting similarity. 309: ratio. 88;of tunnelsn, 316 slolh. 32,215, 218, 225. 334 small taxa, 54 snail, 32. 215 soil type. IM. 142, 144-47, 171-72.324, 327,34%44,368;selection by beetles, 72 South Africa, Ch. 8.286,292,313.317. 320.322.32627,%4142,344,351,3M,

37?-74.378.38%87

South America, 322.333-34.33637,341. 35%57,3M), tmpical forest, ch. I 2 Soulh-East Asia, 297,299,312,333,356 56,374,379;tmpieal forest, ch. 10 spalial: distribution of mllen, 105;large-scale distribution. 175:pattern, 88;p x c s s . 283; scale, 9,285 specialization: feeding, 7,334;f w d type, 332-33 s p i n t i o n , 63 species: M B N T V O . 193:dscline. 101;diversity, 67. 15,213,346 species composition: changes in. 95;compariSon among traps. 185; stability of, 94 species richness, 72.76.93-94. loo, 134. 189, 194.202,20&209,211. 250,350;altitudinal variation in, 352:in cattle dung. 357; and competition. 360: global, 362; habitat differnos. 352;latitudinal change9 in, 351-52: local, 362;mammalian, 352; mechanisms affecting. 360;and R S O U ~ C ~ partitioning. 364: and spatial aggregation, 362; and spatial heterogeneity, 369;in uopical forests. 354-55 Sphacridiwn,83. W. 129. I31 Sphaemeridae, 121. 123 spider, 121,223,250 stability: communities, 371; dung bectles. 9293;long-term. I n populations, 72 stable fly, 299 Staphylinidae. 6, 16. 12cL23. 137. 1-1, 18D-81. 191,223,232-36.250-52.356 58 stochasticity, 9 storage effect, 10 suidulation, 49 succession: in dung microhabitat, 15; seasonal, 39,340 Sudanese savanna, 157 Sulawesi, Ch. IO. 341. 35344,374,379, 401 Sumaua, 182. 19697 Sunda islands. 182 survival: of adult beetles, 46;of offspring. 15 I ~ y m p t r i cs p i e s , 12%?6 rauwarastiw, 52

monomy, 34 temporst patterns, 148 termite. 67, 121, 161,314

Index

-.

territorial behavior, 8. 49 themoregulatio", 222 Thorectcs. 101

m s e c t Uapping, 190-92 trap, Righl interception, 183 Trichophodius,415 Trogidae, 6,22. 133.211 tmpical forest, 41,53. 123: in Africa, Ch. 11; in America, Ch. 12; in Madagascar,20% 206; in Sou&-EaJt Asia. Ch. 10 Tiox. 44 Tlypocopris.246

.

481

tunneler. 36, 163-64,207,226:Aphodius, 208: competition in. 114,151-54, 172; fast-burying. 323,367:large. 45, IM, slow-burying, 139,323,367; small,45, 164 Typhneus. 8 5 , 105, 107 variance-mean regression. 89,284.288 vegetable matter. 134, 167,216-17 vegetationcover, 10&108, 141, 144 wallaby, 32,63