Ecological Entomology (2002) 27, 257±270

Dung in a Central Amazonian rainforest and their ecological role as secondary seed dispersers

ELLEN ANDRESEN Departamento de Ecologõ a de los Recursos Naturales, Instituto de Ecologõ a, Universidad Nacional Auto noma de Me xico

Abstract. 1.The role of several factors that affect the composition of the dung assemblages in an Amazonian rainforest was quantified, together with the effect of these factors on the role that dung beetles play as secondary seed dispersers. 2.A total of 61 dung beetle species was captured during 3360 h of trapping. During nocturnal trapping periods, more dung beetles, of larger mean size, and more species were captured per trap than during diurnal trapping periods. 3.During the rainy season, more dung beetle species were captured per trap than during the dry season, but the number of individuals and their mean size did not vary between seasons. 4.Bait size had a significant effect on the mean number of beetles and mean number of species but not on mean beetle size.As bait size increased from 5, 10, 25, to 50 g, more beetles and more species were captured per trap. 5.Between 6 and 73 % of plastic beads, used as seed mimics, were buried by dung beetles at depths that ranged from 0.5 to 7 cm. Both the proportion of beads buried and burial depth decreased with increasing bead size, and increased with increasing amounts of dung surrounding each bead (5, 10, and 25 g). 6.The proportion of buried seeds for three species varying in size between 5 and 27 mm, increased with increasing dung beetle size, using beetles of seven sizes, varying between 10 and 25 mm. 7.Seeds surrounded by dung were buried more often and more deeply when placed on the forest floor during the late afternoon than when placed during the early morning.Seeds were also buried more often when placed on the forest floor during the rainy season than when placed during the dry season, but season had no effect on burial depth. 8.Forests in Central Amazonia hold a rich dung beetle community that plays an active role in secondary seed dispersal, and consequently in plant regeneration. The interaction between seeds and beetles is complex because it is affected by many factors. Key words. Dung beetles, plant± interaction, , secondary seed dispersal, seed fate, tropical rainforest.

Introduction

Dung beetles (Coleoptera) are members of the Scara- baeidae, Geotrupidae, and Aphodiidae families (following the classification used by Hanski and Cambefort, 1991a), Correspondence: Ellen Andresen, DERN ± UNAM, Apartado the adults and larvae of which feed on faeces.After locating Postal 27±3 (Xangari), Morelia, Michoaca n, C.P. 58089, Me xico. a source of dung, the adults of many species rapidly relocate E-mail: [email protected] a portion of it, either for feeding or for ovipositing (Halffter

# 2002 Royal Entomological Society 257 258 Ellen Andresen

& Edmonds, 1982; Hanski & Cambefort, 1991a).Reloca- the dry season (Hanski, 1980; Janzen, 1983; Estrada & Coates- tion of dung occurs mostly by burying it under the soil Estrada, 1991; Gill, 1991; Andresen, 1999); time of day À the surface.Ecological consequences of this behaviour include nocturnal guild often dominates in terms of biomass (Hanski & soil fertilisation and aeration (Mittal, 1993), an increase in Cambefort, 1991b); and amount of dung À larger amounts of the rate of nutrient cycling (Nealis, 1977), and a reduced dung seem to attract beetles of larger average size than do transmission of some parasites (Bergstrom et al., 1976). smaller amounts of dung (Peck & Howden, 1984). Horizontal and=or vertical movement of seeds present in The main objectives of this study were to identify some of the dung, i.e. seed dispersal, also occurs but this eco- the factors that affect the composition of the dung beetle logical role of dung beetle activity and its effects on assemblages in a rainforest in Central Amazonia, and plant reproduction are less well understood. to determine whether these factors affect the outcome of the Seed dispersal is advantageous for plants because seeds beetle±seed interaction.Specific objectives were to assess may be deposited in sites in which conditions are appro- the effects of season, time of day, and amount of dung on priate for seed survival and=or seedling establishment the composition of the dung beetle assemblages, and to (Howe & Smallwood, 1982).After initial deposition of seeds assess whether and how these factors, together with seed by a primary dispersal agent (e.g. wind, water, fruit-eating size and beetle size, affect secondary seed dispersal by vertebrates), seeds may be moved to a different site by a dung beetles. secondary dispersal agent (e.g. rain, ants, rodents). Secondary dispersal has received less attention than primary dispersal, but as evidence accumulates, it appears that Materials and methods secondary dispersal is common in many systems and may play a very important role in plant regeneration (Forget & Study site Milleron, 1991; Levey & Byrne, 1993; Hoshizaki et al., 1997; BoÈ hning-Gaese et al., 1999; Andresen, 2001). The study was conducted in an 800 ha forest reserve Several recent studies have shown that in tropical rain- embedded in an expanse of continuous primary forest forests, dung beetles of the family Scarabaeidae can act as >10 000 ha in area.The reserve is part of the Biological secondary dispersers of seeds, the primary dispersal of Dynamics of Forest Fragments Project, located 90 km  0  which has been achieved through defecation by mammals north of Manaus (2 30 S, 60 W), Brazil.The study site is (Estrada & Coates-Estrada, 1991; Shepherd & Chapman, covered mainly by primary terra firme forest (not seasonally 1998; Andresen, 1999, 2001; Feer, 1999; Vulinec, 2000). flooded), with a very rich flora.Mean annual temperature  Secondary dispersal by dung beetles can affect the survival in Manaus is 26.7 C and mean annual rainfall is 2186 mm probability of seeds and seedlings in several ways.For (Lovejoy & Bierregaard, 1990), with a drier season between example, buried seeds are more likely to avoid detection June and October.For a more detailed description of the by seed predators than are seeds on the surface (Johnson & study site, see Lovejoy and Bierregaard (1990). Jorgensen, 1981; Estrada & Coates-Estrada, 1991; Crawley, 1992; Shepherd & Chapman, 1998; Andresen, 1999, 2001; Feer, 1999).Buried seeds also encounter a more humid The dung beetle community environment than seeds on the surface, which may promote seed survival and germination in some cases or pathogen Dung beetles were sampled using pitfall traps, which were attack in others (Price & Jenkins, 1986; Chambers & plastic containers 15 cm tall and 10 cm in diameter.Traps MacMahon, 1994).Seed burial may also hinder seedling were filled to two-thirds of their capacity with odourless emergence in some plant species (Andresen, 2000, 2001). soapy water and buried to ground level.A bag of plastic On the other hand, through the horizontal movement of mosquito netting, containing fresh monkey dung, was sus- seeds, dung beetles may decrease the negative effects of seed pended 5 cm above the trap (see below for bait sizes used). clumping and seedling competition (Howe, 1989). Traps were placed under intact canopy,  50 m from tree-fall What determines whether or not a seed is dispersed by gaps, because many dung beetles in this forest avoid gaps dung beetles? In part, it depends on seed size, because seeds (E.Andresen, pers.obs.).Trapswere located along constitute dung contaminants from the dung beetles' trails,  1 m into the forest and 30 m between traps. perspective.Thus, larger seeds should be separated more When it rained heavily for more than 2 h of the trapping frequently from the dung by the beetles, and consequently period, the trapping was cancelled. dispersed less often than smaller seeds (Estrada & Coates- Collected dung beetles were sorted by morphospecies. Estrada, 1991; Shepherd & Chapman, 1998; Andresen, Samples of each morphospecies were pinned, dried, and 1999; Feer, 1999).On the other hand, the species and measured (body length to the nearest 0.1 mm). The mean number of dung beetles attracted to a dung pile will also affect size of beetles was calculated for each trapping period by whether a seed is dispersed.Consequently, variables that adding the number of beetles in each morphospecies multi- affect the composition of dung beetle assemblages are plied by its mean length, and dividing by the total number also likely to affect the fate of seeds present in dung indirectly. of beetles caught (Peck & Howden, 1984). In tropical forests, such variables include: season À beetles are Dung beetles were classified according to their dung- often more abundant during the rainy season than during processing behaviour into tunnellers, rollers, and dwellers.

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 Dung beetles as seed dispersers 259

Rollers make dung balls and move them away from the period.For the response variables consisting of counts source before burying them.In contrast, tunnellers make a (number of individuals and number of species), the error burrow close to the dung source then start provisioning their structure was defined as having a Poisson distribution, the tunnel (Halffter & Edmonds, 1982; Cambefort & Hanski, log link function was used, and the 2 statistic was used 1991).Finally, dwellers process the dung immediately to test for significant changes in deviance (Crawley, 1993). below the dung pat or inside it (Halffter & Edmonds, 1982). When the residual term of the model was inflated due to At the end of the study period, the dung beetle collection overdispersion, the data were rescaled as indicated by was donated to the entomological collection of INPA Crawley (1993), making the tests more conservative.For (National Institute for Research in Amazonia), Manaus, the continuous response variable, mean beetle size, the error Brazil.Other specimens were sent for identification to Fer- structure was defined as normal, the identity link was used, nando Z.Vaz-de-Mello (Setor de Ecologia, Departamento and the F statistic was used to test for significant changes in de Biologia Geral, Universidade Federal de VicË osa, VicË osa, deviance.The response variable was ln-transformed to obtain Minas Gerais, Brazil). constant variance (Crawley, 1993; Sokal & Rohlf, 1995). Large amounts of fresh dung were needed, therefore the To test for central tendency differences between the full dung of howler monkeys Alouatta seniculus was used size distribution of dung beetles in day vs.night samples, throughout the study.Howler monkeys are abundant at two-sample Kolmogorov-Smirnov tests were used, one for the study site, and it was relatively easy to find large quan- number of individuals and one for number of species.Tests tities of fresh dung.All seeds >3 mm in the dung were were one-tailed, which according to Siegel and Castellan removed to avoid interference with experimental seeds (1988) is appropriate when the objective is to test whether and=or beads in the experiments described below.Seeds the values obtained from one population are larger than the 3 mm were not common in dung, their removal was values obtained from another population, rather than to not practical, and they were considered unlikely to affect test whether populations differ in their overall distributions. the interaction between dung beetles and experimental seeds=beads.Dung was stored in plastic bags and either kept in the shade and used on the same day or kept refriger- Effect of dung amount ated and used on the following day. Dung beetles were trapped four times with 5, 10, and 25 g of bait and twice with 50 g of bait.These sizes were based on Effects of season and time of day the defecation sizes observed for howler monkeys (Andre- sen, in press).In three of the trapping periods (including Dung beetles were trapped 14 times between August 1996 those with the 50 g treatment), three traps were used per and January 1998, with 1 month between trapping dung treatment, and in the other trapping period, two traps periods.Eight of the trapping periods were conducted during were used per treatment.Baits of all sizes were used on the dry months (June±October) and six were conducted during same day.In each of the four trapping periods, dung treat- wet months (November±May).During each trapping period, ments were assigned to different trap locations in the forest. 10 diurnal traps and 10 nocturnal traps were set out, each Two of the trapping periods were 24 h in duration, the other baited with 25 g of dung.Diurnal traps were baited at two trapping periods were 16 h in duration; two were dawn and dung beetles were collected at dusk.For the performed during the 1996 dry season and two during the nocturnal sampling, fresh dung was placed at dusk and 1998 wet season. dung beetles were collected at dawn.The 10 trap loca- For each trap, the number of individuals and the number tions were the same for diurnal and nocturnal traps, and of species captured were recorded, and the mean dung were the same in all trapping periods. beetle size was calculated.Data were analysed using gener- For each diurnal and nocturnal trapping period, the total alised linear models with block design, with the factor of numbers of dung beetles and species were counted for each interest being dung amount and with trapping periods con- trap.To determine the effects of year (2 years), season (dry, sidered as blocks.The response variables and specifications wet), trapping period (eight during dry months, six during for the analyses were the same as above: number of individ- wet months), and time of day (diurnal and nocturnal uals (Poisson error and log link), number of species samplings) on the number of beetles captured, number of (Poisson error and long link), and mean beetle size (normal species captured, and mean beetle size, data were analysed error and identity link; transformation of the response using generalised linear models, using the GLIM statistical variable was not necessary to meet the assumptions of the package (Francis et al., 1993). In generalised linear models, analysis). the deviance is a measure of the discrepancy between the observed data and the fitted values, so the significance of each term in a model can be tested through the deviance Secondary seed dispersal by dung beetles that the removal of the term adds to the model (Crawley, 1993).The factors analysed were nested in the following Experiment 1: effects of seed size and dung amount. In manner: season nested within year, trapping period nested this experiment, single beads (used as seed mimics) of nine within season, and time of day nested within trapping different types (Table 1) were put inside dung piles of three

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 260 Ellen Andresen

Table 1. Mass,length,andwidthofbeadsusedasseedmimicsto bucket, filled with forest soil up to 20 cm.On top of the soil, quantify the role of dung beetles as secondary seed dispersers.The a 10-g dung pile containing seeds was deposited, and the sample sizes used in expt.1 for the three dung treatments are also bucket was covered with a lid.The dung beetle species used given, where n is the number of individual bead-containing dung piles. in this experiment were Scybalocanthon sp.1 (10 Æ 0.2 mm, n ˆ 10, four or five beetles per bucket; here and elsewhere Mass Length Width n for n for n for Bead type (g) (mm) (mm) 5g 10 g 25 g means Æ1 SE are reported), Dichotomius lucasi (LuÈ der- waldt) (12 Æ 0.3 mm, n ˆ 9, two or three beetles per bucket), No. 1 0.03 4.0 3.8 36 44 ± Phanaeus chalcomelas Perty (14 Æ 0.3 mm, n ˆ 8, one or two No. 2 0.11 5.7 5.5 35 72 ± beetles per bucket), Dichotomius sp.1 (16 Æ 0.3 mm, n ˆ 7, No. 3 0.25 8.0 7.6 36 81 ± one beetle per bucket), Dichotomius subaeneus (Laporte) No. 4 0.23 12.1 5.3 37 40 ± No. 5 0.33 18.4 5.5 39 50 47 (17 Æ 0.5 mm, n ˆ 10, one beetle per bucket), Dichotomius No. 6 0.63 16.0 9.5 27 42 33 boreus (Oliv.) (small individuals: 19 Æ 0.9 mm, n ˆ 4, one No. 7 0.87 11.2 10.9 25 41 42 beetle per bucket; large individuals: 25 Æ 0.5 mm, n ˆ 10, No. 8 1.73 25.8 10.9 32 42 44 one beetle per bucket).Because quantifying seed burial No. 9 2.16 20.0 13.3 ± 34 33 only makes sense when all the dung has disappeared, rather than using the same number of beetles per bucket for each species, the number of individuals for each species that sizes: 5, 10, and 25 g.Bead-containing dung piles were would completely bury all the faecal matter within 1 or placed on the forest floor, along transects, one pile every 2 days was used.Thus, in terms of dung and seed burying 10 m.To find beads that were moved by beetles, a 50-cm capacity, several individuals of the smaller species were piece of thin white nylon thread was tied to each bead (the considered equivalent to one individual of the larger species, other end of the thread was loose).Because dung was limit- and it was not considered appropriate to estimate the ing during this study, all bead types could not be replicated number of seeds buried on a per beetle basis. with all dung treatments (Table 1).Ten to fifty dung piles Each beetle species was tested with three different seed were set out on any single day, between 15.00 and species: Helicostylis scabra (J.F.Macbr.)C.C.Berg, 18.00 hours during the dry season, to avoid having time of Moraceae (5 Æ 0.2 mm, n ˆ 10), Pourouma guianensis day and season as confounding factors.After 2 days, beads Aubl., Moraceae (11 Æ 0.8 mm, n ˆ 10), and Pouteria were recovered, and it was recorded whether they had been durlandii (Standl.) Baehni, Sapotaceae (27 Æ 0.7 mm, n ˆ 10). buried by dung beetles, the depth of burial to the nearest In each dung pile, seeds of a single species were included, 1 cm (for beads covered slightly by soil, a burial depth of using eight seeds of H. scabra, four seeds of P. guianensis,or 0.5 cm was assigned), and the horizontal distance to the two seeds of P. durlandii.When all dung had been buried nearest 5 cm. by beetles (1 or 2 days), the number of seeds remaining To analyse the effects of bead size (using bead mass as the on the surface was counted.The experiment was repeated best indicator of size, because beads were of different five times per seed species for D. subaeneus, D. sp.1, and shapes) and amount of dung on bead burial and horizontal P. chalcomelas,seventimesforS. sp.1, D. clypeatus,andsmall movement of beads, four generalised linear models were D. boreus, and 11 times for large D. boreus.Individual dung used following the ANCOVA design.The factor was amount beetles were re-used up to three times.Because seeds are of dung, the covariate was bead mass, and the dependent simply considered as dung contaminants by dung beetles, variables were proportion of beads buried, proportion of in terms of seed burial, each trial conducted with the same beads moved horizontally, depth of burial, and horizontal individual can be considered as statistically independent, distance moved.For the first two variables, a binomial as long as all dung disappeared from the surface. error structure was defined, with a logit link function.For Data were analysed using a generalised linear model with proportion of beads buried, the significance of changes in an ANCOVA design.The factor was seed species, the covari- deviance was tested using the 2 statistic.For the propor- ate was beetle size, and the response variable was the tion of beads moved horizontally, a slight overdispersion of proportion of seeds buried.The binomial error structure the residual term was corrected through rescaling, and as a with logit link function was used; rescaling was necessary consequence the F statistic was used for testing the signifi- to correct for a slight overdispersion of the residual term. cance of changes in deviance (Crawley, 1993).For the two Experiment 3: effect of time of day. To determine continuous variables, a normal error structure and an iden- whether seed burial varies depending on whether seeds are tity link were used, with no transformation of the response defecated in the morning or in the late afternoon, the same variables being necessary. set-up described in expt 1 was followed, but placing dung Experiment 2: effect of dung beetle size. In this experi- piles both in the morning (06.00±07.00 hours) and in the late ment, individual dung beetle species of different sizes were afternoon (17.00±18.00 hours). Number of seeds buried and tested using three seed species.Individuals of six dung beetle burial depths were recorded after 2 days.This experiment species in seven size categories (one species was strongly was conducted for bead type no.3 (diameter 8 mm) with dimorphic in terms of size, so small and large individuals 5 g dung piles (n ˆ 33 and 36 for morning and afternoon were tested separately) were captured and tested separately respectively) and 10 g dung piles (n ˆ 76 and 81 for morn- for seed burial by putting them in a 25-cm diameter plastic ing and afternoon respectively), and for the seeds of

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 Dung beetles as seed dispersers 261

Byrsonima crispa A.Juss.,Malpighiaceae (diameter ˆ of Minquartia guianensis Aubl., Olacaceae (length: 8 Æ 0.2 mm, n ˆ 15) with 10 g dung piles (n ˆ 120 and 152 22 Æ 0.5 mm, width: 12 Æ 0.6 mm, thickness: 12 Æ 0.6 mm, for morning and afternoon respectively) and 25 g dung piles n ˆ 10) in the dry season; Buchenavia grandis, large seeds (n ˆ 80 and 120 for morning and afternoon respectively). (length: 30 Æ 0.4 mm, width: 13 Æ 0.3 mm, thickness: Dung removal rates were also assessed, by recording 12 Æ 0.3 mm, n ˆ 10) in the wet season paired with bead whether some dung remained in each dung pile after 12 type no.8 (length: 26 mm, width: 11 mm, thickness: and 24 h.To collect these data, dung piles used in experi- 11 mm) in the dry season, used with 10 g dung piles; large ments described elsewhere were monitored (Andresen, Buchenavia grandis seeds in the wet season paired with bead 2001), in addition to those used to assess seed=bead burial type no.8, used with 25 g dung piles. at day vs.night.All data were gathered during dry seasons. Dung removal rates after 24 h in dry vs.wet season were To test for the effects of time of day and amount of dung assessed for 10-g dung piles placed in the afternoon.For the on the proportion of seed=beads buried, data were analysed dry season, data for the 10-g dung piles placed in the after- using separate generalised linear models for seeds and noon in expt 3 (n ˆ 179) were used, and for the wet season, beads, with two factors, binomial error structure, and logit 298 additional 10-g dung piles were monitored. link.To test the effect on burial depth, two-way ANOVAs Data on the proportion of seeds buried were analysed were performed for beads and seeds on square-root-trans- using a generalised linear model with binomial error formed data.Finally, to analyse the data on dung removal, structure and logit link with a block design.Season was a generalised linear model was used, with the same factors the main factor, and each matched pair of seeds or used above: time of day and amount of dung, and an add- beads=seeds was used as a block.Data on burial depth itional factor: hours since set-up (12 h vs.24 h).The response were analysed using a generalised linear model with variable was the proportion of dung piles that still had some similar design, but model specifications were normal error dung remaining.Binomial error structure and logit link structure and identity link.Data on dung removal were were used, and rescaling was necessary to correct for over- analysed using a Pearson 2 test. dispersion. Experiment 4: effect of season. Five paired comparisons in the wet and dry seasons were performed.Data were Results available for the same seed species in both seasons for only one comparison; for the other four comparisons, dif- The dung beetle community ferent seed species, or seeds and beads with similar sizes and shapes, were paired.The five comparisons were: Pourouma Effects of season and time of day. A total of 8845 dung guianensis seeds (length: 11 Æ 0.8 mm, width: 7 Æ 0.3 mm, beetles of 61 species (59 species of Scarabaeidae and two thickness: 6 Æ 0.3 mm, n ˆ 10) in the wet season paired species of Aphodiidae) was captured in the 14 trapping with seeds of Ocotea percurrens Vicentini, Lauraceae periods.Twenty-two species were classified as nocturnal (length: 12 Æ 0.2 mm, width: 8 Æ 0.1 mm, thickness: species and 27 as diurnal; the other species were equally 7 Æ 0.1 mm, n ˆ 10) in the dry season; Micropholis guya- abundant in nocturnal and diurnal traps or too rare to allow nensis (A.DC.), Sapotaceae, seeds (length: 18 Æ 0.3 mm, classification (see Appendix).Thirty-two species were tunnel- width: 9 Æ 0.2 mm, thickness: 6 Æ 0.2 mm, n ˆ 20) in both lers, 11 were rollers, two were dwellers, three species were of seasons; Buchenavia grandis Ducke, Combretaceae, small the genus Eurysternus (this genus has a dung-processing seeds (length: 21 Æ 0.3 mm, width: 10 Æ 0.1 mm, thickness: behaviour in which dung balls are only covered shallowly 10 Æ 0.1 mm, n ˆ 10) in the wet season paired with seeds by soil; Halffter & Edmonds, 1982), and 13 unidentified

Table 2. Nested analyses of deviance for the effects of year (Y), season (S), trapping period (TP), and time of day (TD) on number of beetles captured, number of species captured, and mean beetle size.

Number of beetles Number of species Mean beetle size

Deviance Deviance Factor d.f. ( 2 approx.)z ( 2 approx.) F-value

Y 1 8.48** 15.23*** 0.451,2 NS Y=Sy 2 0.81 NS 12.90** 2.192,10 NS Y=S=TP 10 103.50*** 42.98*** 0.7210,14 NS Y=S=TP=TD 14 124.30*** 27.29* 11.3214,252** Error 252 227.11 164.72 13.79§ Total 279 463.37 263.11 29.29§ ySlash indicates nested within. zNS P > 0.05, *P < 0.05, **P < 0.01, ***P < 0.001. §These values are sum of squares.

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 262 Ellen Andresen

In terms of the overall size distribution of all dung beetles captured during the 2 years, larger beetles, both in terms of individuals and species, were more abundant in nocturnal than in diurnal trapping periods (one-tailed Kolmogorov- Smirnov tests: for individuals, D ˆ 0.278, P < 0.01; for species, D ˆ 0.365, P < 0.05; Fig. 3). Effect of dung amount. There were significant differences among the bait-size treatments in mean number of indi- viduals captured per trap ( 2 ˆ 78.17, d.f. ˆ 3, P < 0.01) and mean number of species per trap ( 2 ˆ 25.92, d.f. ˆ 3, P < 0.01), with both variables increasing with increasing bait size (Fig.4). In both cases, a significant amount of the deviance was due to the block effects (trapping periods with different trapping regimes; for individuals: 2 ˆ 60.92, d.f. ˆ 3, P < 0.01; for species: 2 ˆ 13.82, d.f. ˆ 3, P < 0.01). No differences were found among dung treatments in terms of mean size of beetles, which was 5 mm for the 5- and 50-g treatments, and 6 mm for the 10- and 25-g

treatments (F3,35 ˆ 0.43, P ˆ NS).The block effect was again highly significant (F3,32 ˆ 11.18, P < 0.01).

Secondary seed dispersal by dung beetles

Experiment 1: effects of seed size and dung amount. Between 6 and 73% of beads were buried by beetles, depending on both bead mass and amount of dung (Fig.5a). The proportion of beads buried decreased with increasing bead mass ( 2 ˆ 50.87, d.f. ˆ 1, P < 0.01) and increased with increasing amounts of dung ( 2 ˆ 28.49, d.f. ˆ 2, P < 0.01). There was no significant interaction between the factor (dung) and the covariate (bead size) ( 2 ˆ 5.24, d.f. ˆ 2, P ˆ NS). Mean burial depths varied between 0.5 and 7 cm (Fig. 5b). The results paralleled those obtained for the proportion of beads buried, with burial depth also decreasing with increas- Fig. 1. (a) Average number of dung beetles, (b) average number of ing bead mass (F1,18 ˆ 24.55, P < 0.001) and increasing with species, and (c) mean beetle size, per trap, for beetles captured increasing amounts of dung (F2,19 ˆ 7.34, P < 0.01). There during the day (&) and night (&), in two seasons (dry and wet). was no significant interaction between dung amount and Bars indicate ‡1 SE. bead size (F2,16 ˆ 0.027, P ˆ NS).The linear relationships between burial depth and bead mass yielded the best fits for species were not classified according to their dung-processing the observed data, however it is important to realise that once behaviour.Size of dung beetle species ranged from 2 to the level of no burial, i.e. 0 cm burial depth, is reached, it will 40 mm. remain the same for larger beads. Time of day had a significant effect on the three response Between 5 and 44% of beads were moved horizontally by variables examined: number of beetles, number of species, dung beetles (including beads buried by beetles and those and mean beetle size (Table 2).More dung beetles and more remaining on the surface).The proportion of seeds moved species were captured during nocturnal periods than diurnal horizontally decreased significantly with increasing bead periods, and beetles were of mean larger sizes during mass (F1,20 ˆ 14.70, P < 0.01) but was affected neither by nocturnal periods, but only during the dry season (Fig.1). amount of dung (F2,18 ˆ 2.26, P ˆ NS) nor an interaction Season of the year had a significant effect only on number between bead mass and amount of dung (F2,16 ˆ 0.72, of species, with more species being captured during the wet P ˆ NS).Mean horizontal distances varied between 6 and season (Table 2, Fig.1). 17 cm, with a maximum distance of 60 cm.The horizontal

There was a significant amount of added variance in the distances increased with increasing bead mass (F1,18 ˆ 7.30, number of beetles and species captured due to variability P < 0.05). The main effect of dung amount was not signifi- among years and among trapping periods within seasons; cant (F2,19 ˆ 1.57, P ˆ NS) but there was a significant inter- monthly rainfall also showed great variability within action between bead mass and dung amount (F2,16 ˆ 7.57, seasons and among years (Table 2, Fig.2). P < 0.01).

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 Dung beetles as seed dispersers 263

Fig. 2. Monthly rainfall (line) and number of beetles captured per 10 traps (bars).Months with no bars mean that no sampling of beetles was conducted during those months.

Fig. 3. Size distribution of dung beetles in terms of (a) total number of individuals and (b) total number of species, captured in 140 diurnal (&) and 140 nocturnal (&) traps.

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 264 Ellen Andresen

Fig. 4. Mean number of individuals (&) and species (&) captured per trap, using different bait sizes.Bars indicate ‡1 SE.

Experiment 2: effect of dung beetle size. Larger beetles buried a higher proportion of seeds for the three plant species than did smaller beetles (F1,137 ˆ 146.85, P < 0.001), and the proportions of buried seeds decreased with increasing seed size (F2,138 ˆ 11.37, P < 0.001). There was also a significant interaction between seed species and beetle size (F2,135 ˆ 3.22, P < 0.05), showing that for larger seeds, the increase in the proportion of seeds buried with increasing beetle size was less steep than for smaller seeds (Fig.6). Experiment 3: effect of time of day. The effect of time of day was significant for both beads and seeds: more Fig. 5. Relationship of bead mass to (a) the percentage of beads beads=seeds were buried when placed in the afternoon buried by dung beetles and (b) the depth of burial, for observed than when placed in the morning (beads 28 vs.53 %: values (symbols) and best-fit lines (lines).Beads were surrounded by three different amounts of dung: 5 g (Á, ÐÐ), 10 g (&, 2 ˆ 11.09, d.f. ˆ 1, P < 0.001; seeds 55 vs. 67%: 2 ˆ 6.12, - Ð - Ð), and 25 g (*, - - - -).Equations for best-fit lines for (a) d.f. ˆ 1, P < 0.05). For B. crispa seeds, there was also a are: 5 g: ln (p=1±p) ˆÀ0.191±1.044 X, where ln (p=1±p) is the significant effect of the dung treatment, with 53% of seeds logit of p and p is the proportion of seeds buried; 10 g: ln (p=1±p) being buried when surrounded by 10 g of dung, and 70% ˆ 0.199±1.044 X; 25 g: ln (p=1±p) ˆ 0.952±1.044 X. For the range of when surrounded by 25 g of dung ( 2 ˆ 14.77, d.f. ˆ 1, observed data, the best-fit lines for (b) are linear regressions: 5 g: P < 0.001), but there was no significant interaction between Y ˆ 2.96±1.55 X; 10 g: Y ˆ 4.38±1.55 X; 25 g: Y ˆ 7.02±1.55 X. time of day and dung treatments ( 2 ˆ 0.64, d.f. ˆ 1, P ˆ NS).For bead type no.3, neither the dung treatment surrounded by 10 g of dung (3.8 cm), but the interaction nor the interaction was significant (amount of dung: term was not significant (time of day: F1,172 ˆ 6.08, 2 2 ˆ 1.03, d.f. ˆ 1, P ˆ NS; interaction: ˆ 1.27, d.f. ˆ 1, P ˆ 0.01; amount of dung: F1,172 ˆ 6.91, P ˆ 0.01; interac- P ˆ NS). tion: F1,172 ˆ 1.97, P ˆ NS). In terms of burial depth, the results were analogous to Regarding dung removal rates, the effects of time of day those for proportion of beads=seeds buried.The two-way (morning vs.afternoon) and of hours until check-up (12 h ANOVA for bead type no.3 showed a significant effect of vs.24 h) were significant: more dung remained on the time, with beads buried more deeply when placed in the surface after the diurnal period of dung beetle activity afternoon (4.3 cm) than when placed in the morning (morning) than after the nocturnal period (afternoon; Fig.7) (2.3 cm); the effects of dung amount and the interaction and, logically, more dung was removed after 24 h than after term were not significant (time of day: F1,89 ˆ 3.97, 12 h (time of day: F1,7 ˆ 8.38, P < 0.05; hours until check-up: P < 0.05; amount of dung: F1,89 ˆ 0.09, P ˆ NS; interaction: F1,8 ˆ 5.73, P < 0.05). The interaction between these two F1,89 ˆ 2.07, P ˆ NS).For B. crispa, significant effects were factors was also significant (F1,2 ˆ 40.24, P < 0.05), due to found for both time of day and dung amount, with seeds the fact that the difference in dung removal after 12 and 24 h being buried more deeply when placed in the afternoon was much more pronounced for dung piles placed in the (5.6 cm) than when placed in the morning (3.8 cm), and morning than for dung piles placed in the afternoon (Fig.7). when surrounded by 25 g of dung (5.6 cm) than when The effect of amount of dung was not significant

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 Dung beetles as seed dispersers 265

P < 0.01). No differences were observed, however, in terms of burial depth between the dry and the wet seasons

(F1,8 ˆ 0.29, P ˆ NS); for this variable, the effect of blocks was not significant (F1,7 ˆ 2.59, P ˆ NS). Finally, in terms of dung removal in the wet vs.dry season, significantly more dung piles had some dung remaining on the surface after 24 h during dry months (18.99%) than during wet months (8.72%; 2 ˆ 10.73, d.f. ˆ 1, P ˆ 0.001).

Discussion

The dung beetle community

The nocturnal dung beetle assemblage consisted of 20% more individuals than the diurnal assemblage.Although the Fig. 6. Relationship between the average percentage of seeds buried species captured at night were mostly different from those and dung beetle size, for three species of seeds, for observed values captured during the day (see Appendix), the number of (symbols) and best-fit lines (lines): Helicostylis scabra (length: 5 mm, species was similar in both periods.Dung beetles captured &, ÐÐ, ln (p=1±p) ˆ ± 4.46 ‡ 0.367 X, where ln (p=1±p) is the logit at night were on average larger than beetles captured during of p and p is the proportion of seeds buried), Pourouma guianenesis the day.These results are consistent with other tropical (length: 11 mm, *,-Ð-Ð,ln(p=1±p) ˆ ±4.25‡ 0.308 (X), and forest dung beetle communities in terms of biomass and Pouteria durlandii (length: 27 mm, Á,----,ln(p=1±p ˆ ±3.99 ‡ 0.171 X). number of species (Hanski & Cambefort, 1991b, and refer- ences therein). More dung beetle species were captured in the rainy season than in the dry season.The number of individuals captured was 11% higher during the rainy season but this difference was not statistically significant, and there was no difference in the size of beetles in dry vs.wet seasons.In other neotropical forests with less pronounced seasons, researchers have also found little difference in dung beetle assemblages among seasons (Peck & Forsyth, 1982; Waage & Best, 1985).This contrasts with forests that show a more pronounced seasonality, in which dung beetles are much more abundant during the rainy season (Hanski, 1980; Janzen, 1983; Estrada & Coates-Estrada, 1991; Gill, 1991; Andresen, 1999).It is likely that in such forests, secondary dispersal by dung beetles will be less important or even absent during the dry months. Regarding the amount of dung, both the number of individuals and the number of species captured per trap Fig. 7. Percentage of 5-, 10-, and 25-g dung piles that still had some increased with increasing bait size.The number of indivi- dung remaining after 12 h (&) and 24 h (&).Dung piles were duals captured increased by 62% when comparing baits placed in the early morning (AM) or in the late afternoon (PM). of 50 g and of 5 g of dung, while the number of species Numbers above each bar indicate the number of individual dung increased by 36%, however no differences were found in piles monitored. the mean size of beetles.This means that both small and large dung piles attract large beetles, which are the most important in secondary seed dispersal (at least for seeds of (F2,9 ˆ 0.18, P ˆ NS), and neither were the interactions of the size considered here).This result was not expected.It is dung with time of day (F2,3 ˆ 0.70, P ˆ NS), and dung with known that larger beetles require and use larger amounts of hours until check-up (F2,5 ˆ 0.14, P ˆ NS). dung (Doube, 1990; Hanski & Cambefort, 1991b,c) and Experiment 4: effect of season. A test taking each of the thus it was expected that larger baits would attract a five matched pairs of seeds or seeds and beads as blocks, higher proportion of large beetles than would smaller showed that the effect of season was significant, with 39% baits.Researchers working in a Panamanian rainforest of beads=seeds buried during the wet season and 32% found that the mean size of dung beetles caught with buried during the dry season ( 2 ˆ 9.98, d.f. ˆ 1, P < 0.01); large baits was nearly twice that of beetles caught with the effect of blocks was also significant ( 2 ˆ 7.43, d.f. ˆ 1, small baits (Peck & Howden, 1984).In that study, the

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 266 Ellen Andresen size difference between the two bait sizes used was 100-fold Chapman, 1998; Andresen, 1999; Feer, 1999).Conversely, (2 vs.200 ml), while in the present study the difference between seeds that are buried too deeply may not be able to emerge the largest and the smallest bait was only 10-fold, which as seedlings.Even small increments in depth, of <5 cm, can may not be enough to detect or cause differences in the size significantly decrease the probability of seedling emergence distribution of beetles. and successful establishment (Fenner, 1987; Shepherd & Chapman, 1998; Feer, 1999; Andresen, 2000, 2001). Thus, although more seeds are buried when defecated by Secondary seed dispersal by dung beetles mammals in the late afternoon, and are more likely to escape seed predation due to increased burial depths, more Larger dung beetles buried more seeds than did small of these seeds may fail to emerge as seedlings. beetles.This was primarily due to larger beetles using larger As seed size increases, the advantage of being handled by amounts of dung (Doube, 1990; Hanski & Cambefort, the nocturnal assemblage of dung beetles, rather than the 1991b).Because large beetles are more abundant at night, diurnal assemblage, probably also increases.This is because it was not surprising to find that in the day vs.night large seeds are mostly buried by large beetles, which are comparisons, seeds and beads were buried more often more abundant at night.In this study, seeds of Pourouma when placed in the late afternoon.The total number of guianensis (11 mm in length) and of Pouteria durlandii dung beetles was also higher at night, which may also con- (27 mm) were only buried by beetles >10 mm, while some tribute to the higher probability of seed burial at night. Helicostylis scabra seeds (5 mm) were also buried by smaller Dung does not always disappear in a single night or day. beetles.Smaller seeds, on the contrary, may benefit more Consequently, seeds present in mammal defecations will when handled by the diurnal assemblage of beetles, which often be subject to the activity of both diurnal and noctur- on average consists of smaller beetles that probably bury nal beetles.In expt 3, beads and seeds were left on the forest seeds less deeply.In accordance with the findings reported floor for 2 days.Still, the differences were significant in other studies (Estrada & Coates-Estrada, 1991; Shepherd between seeds placed in the morning vs.afternoon, suggest- & Chapman, 1998; Andresen, 1999; Feer, 1999), small ing that the first hours of dung beetle activity after dung beads were buried more often than large beads, but they deposition are probably most important in determining were also buried more deeply than large beads.Thus, whether a seed is buried.The results are probably due in a larger proportion of small seeds may be buried at depths part to the lower abundance and smaller size of beetles that hinder seedling emergence when handled by the noctur- during the day.Additionally, dung probably dries more nal beetles. quickly during the day, thus quickly losing its attractiveness Regarding the effect of season, the percentage of seeds= for most dung beetles (Howden & Nealis, 1975; Halffter & beads buried was higher in the rainy months.As mentioned Edmonds, 1982).This was corroborated by the fact that above, season of the year did not have a significant effect on differences in dung removal after 12 vs.24 h were more the number of beetles captured or on their mean size.Season pronounced for dung piles placed in the morning than for may affect seed burial by beetles in other ways.For example, piles placed in the afternoon, and by the fact that after 12 h, during the rainy season soils are probably softer, which diurnal dung piles were more likely to have some dung may facilitate dung and seed burial.It is well known that remaining than were nocturnal samples.The importance soil texture and hardness are important factors affecting of nocturnal dung beetles compared with diurnal beetles, the composition of local dung beetle communities and in terms of dung burial, has been noted in two other their dung-burying behaviour (Fincher, 1973; Hanski & neotropical forests (Estrada et al., 1993; Feer, 1999). Cambefort, 1991a; Giller & Doube, 1994; Osberg et al., Regarding burial depth, seeds=beads were buried more 1994; Davis, 1996). deeply when placed in the afternoon than when placed in With respect to amount of dung, seeds were buried more the morning.This result may also be due to the greater often when surrounded by more dung, probably because abundance of larger beetles during the night.Although larger amounts of dung attracted more beetles.Addition- there is great variation among dung beetle species with ally, beads surrounded by more dung were buried more respect to the depth at which they bury dung (Hanski & deeply than beads surrounded by less dung.Thus, as with Cambefort, 1991c), there is some evidence of larger beetles time of day (see above), from the perspective of plants there burying dung more deeply (Doube, 1990).Alternatively, may be a trade-off between the positive aspect of being deeper burial at night could be due to higher levels of surrounded by more dung (more seeds are buried and likely competition.Because more dung beetles were attracted to to avoid predation) and the negative aspect (seeds are dung during the night, it could be that in order to diminish buried more deeply and seedlings are less likely to emerge). competition for nesting sites, beetles may increase burial Dung beetles not only bury seeds but they can also move depths, thus partitioning the vertical space beneath the seeds horizontally, potentially diminishing the degree of dung source (Hanski & Cambefort, 1991c). seed clumping when several seeds are defecated together From the perspective of plants, depth is important (Andresen, 1999).The maximum distance recorded in this because seeds are more likely to escape detection by preda- study was 60 cm, with mean distances varying between 6 tors when buried more deeply (Johnson & Jorgensen, and 17 cm.Still, small distances such as these could have 1981; Estrada & Coates-Estrada, 1991; Shepherd & important implications for plant demography.Seedlings

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 Dung beetles as seed dispersers 267 germinating from seeds in a clump will compete with each Financial and logistic support was provided by University other, and only one seedling will usually survive (Howe, of Florida-Department of Zoology, University of Florida- 1989); however seedlings that establish from seeds that are College of Liberal Arts and Sciences, Biological Dynamics separated physically by even a few centimetres may survive of Forest Fragments Project (BDFFP), Instituto Nacional to the sapling stage.Thus, even short-distance horizontal de Pesquisas da AmazoÃnia (INPA), Smithsonian Institu- movement of seeds away from each other will increase the tion, Lincoln Park Zoo, and Wildlife Conservation Society. number of individuals available for recruitment into the This work was part of dissertation research while at the next age-class. Department of Zoology, University of Florida.This is Other studies have reported greater maximum horizontal contribution number 338 in the INPA-Smithsonian- distances than those reported here, for dung and=or seeds BDFFP technical series. moved by dung beetles in tropical forests, in particular by the roller dung beetles (Estrada & Coates-Estrada, 1991; Andresen, 1999).This is due to the dung-relocating behaviour of rollers, which make a dung ball and roll it References away from the source before burying it.Tunnellers, on the other hand, make a burrow close to the dung and make Andresen, E.(1999) Seed dispersal by monkeys and the fate of several trips to the dung source to provision their burrow dispersed seeds in a Peruvian rainforest. Biotropica, 31, 145±158. (Halffter & Edmonds, 1982). Andresen, E.(2000) The role of dung beetles in the regeneration Similar to other studies, it was found that tunneller dung of rainforest plants in Central Amazonia.PhD dissertation, University of Florida, Gainesville, U.S.A. beetles in neotropical forests are generally more abundant Andresen, E.(2001) Effects of dung presence, dung amount, and in terms of species and individuals (Peck & Howden, 1984; secondary dispersal by dung beetles on the fate of Micropholis Estrada & Coates-Estrada, 1991; Hanski & Cambefort, guyanensis (Sapotaceae) seeds in Central Amazonia. Journal of 1991d; Andresen, 1999) and are represented by species of Tropical Ecology, 17, 61±78. larger sizes than rollers (Estrada & Coates-Estrada, 1991). Andresen, E.(in press) Primary seed dispersal by red howler Additionally, tunnellers remove larger amounts of dung monkeys and the effect of defecation pattern on the fate of than roller dung beetles of equivalent size (Doube, 1990). dispersed seeds. Biotropica. Thus, in general, tunnellers are likely to be more important Bergstrom, B.C., Maki, L.R. & Werner, B.A. (1976) Small dung in secondary seed dispersal, in terms of the percentage of beetles as biological control agents: laboratory studies of beetle seeds they bury.Rollers, however, may be more important action on trichostrongylid eggs in sheep and cattle feces. Proceedings of the Helminthology Society of Washington, 43, when the advantage of reduced seed density achieved 171±174. through horizontal movement is higher relative to the BoÈ hning-Gaese, K., Gaese, B.H. & Rabemanantsoa, S.B. (1999) advantage of reduced predation achieved through seed Importance of primary and secondary seed dispersal in the burial. Malagasy tree Commiphora guillaumini. Ecology, 80, 821±832. Cambefort, Y.& Hanski, I.(1991) Dung beetle population biology. Dung Beetle Ecology (ed.by I.Hanski and Y.Cambefort), Concluding remarks pp.36±50.Princeton University Press, Princeton, New Jersey. Chambers, J.C. & MacMahon, J.A. (1994) A day in the life of a Most tree species in neotropical rainforests produce fruits seed: movements and fates of seeds and their implications for that are seemingly adapted for seed dispersal by frugivorous natural and managed systems. Annual Review of Ecology and Systematics, 25, 263±292. (Howe, 1990); also, most vertebrates in these forests Crawley, M.J. (1992) Seed predators and plant population include fruits in their diets (Terborgh, 1986).Because the dynamics. Seeds, the Ecology of Regeneration in Plant Com- dung of herbivorous vertebrates is the most important munities (ed.by M.Fenner), pp.157±191.CAB International, resource for dung beetles in most regions (Hanski & Cambe- Wallingford, U.K. fort, 1991a), it is almost certain that much of the dung used Crawley, M.J. (1993) GLIM for Ecologists.Blackwell Scientific by dung beetles in neotropical forests contains seeds.Conse- Publications, Oxford. quently, dung beetles in such forests have great potential to Davis, A.L. (1996) Community organization of dung beetles affect plant reproduction and thus forest regeneration, (Coleoptera: Scarabaeidae): differences in body size and func- through their role as secondary seed dispersers (Andresen, tional group structure between habitats. African Journal of 2001).As seen in this study, however, the relationship Ecology, 34, 258±275. between dung beetles and seeds is not simple and many Doube, B.M. (1990) A functional classification analysis of the structure of dung beetle assemblages. Ecological Entomology, 15, factors add complexity to this interaction. 371±383. Estrada, A.& Coates-Estrada, R.(1991) Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed Acknowledgements dispersal: ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology, 7, 459±474. I am grateful to R.Bodmer, J.Brockmann, C.Chapman, Estrada, A., Halffter, G., Coates-Estrada, R. & Meritt, D.A., Jr D.Levey, D.Pe  rez-Salicrup, F.Putz, and two anonymous (1993) Dung beetles attracted to mammalian herbivore (Alouatta reviewers for their useful comments on the manuscript. palliata) and omnivore (Nasua narica) dung in the tropical rain

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 268 Ellen Andresen

forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology, 9, Janzen, D.H. (1983) Seasonal change in abundance of large 45±54. nocturnal dung beetles (Scarabaeidae) in a Costa Rican Feer, F.(1999) Effects of dung beetles (Scarabaeidae) on seeds deciduous forest and adjacent horse pasture. Oikos, 41, 274±283. dispersed by howler monkeys (Alouatta seniculus) in the French Johnson, T.& Jorgensen, C.D.(1981) Ability of desert rodents to Guianan rain forest. Journal of Tropical Ecology, 15, 129±142. find buried seeds. Journal of Range Management, 34, 312±314. Fenner, M.(1987) Seedlings. New Phytologist, 106 (Suppl.), 35±47. Levey, D.J. & Byrne, M.M. (1993) Complex ant±plant interactions: Fincher, G.T. (1973) Nidification and reproduction of Phanaeus rain forest ants as secondary dispersers and post-dispersal seed spp.in three textural classes of soil (Coleoptera: Scarabaeidae). predators. Ecology, 74, 1802±1812. Coleopterists Bulletin, 27, 33±37. Lovejoy, T.E. & Bierregaard, R.O. (1990) Central Amazonian Forget, P.-M. & Milleron, T. (1991) Evidence for secondary seed forests and the Minimum Critical Size of Ecosystems Project. dispersal by rodents in Panama. Oecologia, 87, 596±599. Four Neotropical Rainforests (ed.by A.Gentry), pp.60±71.Yale Francis, B., Green, M. & Payne, C. (eds) (1993) The GLIM System: University Press, New Haven, Connecticut. Release 4 Manual.Clarendon Press, Oxford. Mittal, I.C. (1993) Natural manuring and soil conditioning by Gill, B.(1991) Dung beetles in tropical American forests. Dung dung beetles. Tropical Ecology, 34, 150±159. Beetle Ecology (ed.by I.Hanski and Y.Cambefort), pp.211±229. Nealis, V.G. (1977) Habitat associations and community analysis Princeton University Press, Princeton, New Jersey. of south Texas dung beetles (Coleoptera: ). Giller, P.S. & Doube, B.M. (1994) Spatial and temporal Canadian Journal of Zoology, 55, 138±147. co-occurrence of competitors in Southern African dung beetle Osberg, D.C., Doube, B.M. & Hanrahan, S.A. (1994) Habitat communities. Journal of Animal Ecology, 63, 629±643. specificity in African dung beetles: the effect of soil type on the Halffter, G.& Edmonds, W.D.(1982) The Nesting Behavior of survival of dung beetle immatures (Coleoptera: Scarabaeidae). Dung Beetles (Scarabaeinae). An Ecological and Evolutive Tropical Zoology, 7, 1±10. Approach. Instituto de Ecologia, Mexico, D.F. Peck, S.B. & Forsyth, A. (1982) Composition, structure, and Hanski, I.(1980) Spatial variation in the timing of the seasonal competitive behaviour in a guild of Ecuadorian rain forest dung occurrence in coprophagous beetles. Oikos, 34, 311±321. beetles (Coleoptera; Scarabaeidae). Canadian Journal of Hanski, I.& Cambefort, Y.(eds) (1991a) Dung Beetle Ecology. Zoology, 60, 1624±1634. Princeton University Press, Princeton, New Jersey. Peck, S.B. & Howden, H.F. (1984) Response of a dung beetle guild Hanski, I.& Cambefort, Y.(1991b) Resource partitioning. to different sizes of dung bait in a Panamanian rainforest. Dung Beetle Ecology (ed.by I.Hanski and Y.Cambefort), Biotropica, 16, 235±238. pp.330±349.Princeton University Press, Princeton, New Jersey. Price, M.V. & Jenkins, S.H. (1986) Rodents as seed consumers and Hanski, I.& Cambefort, Y.(1991c) Competition in dung beetles. dispersers. Seed Dispersal (ed.by D.R.Murray), pp.191±235. Dung Beetle Ecology (ed.by I.Hanski and Y.Cambefort), Academic Press, Sydney, Australia. pp.305±329.Princeton University Press, Princeton, New Jersey. Shepherd, V.E. & Chapman, C.A. (1998) Dung beetles as Hanski, I.& Cambefort, Y.(1991d) Species richness. Dung Beetle secondary seed dispersers: impact on seed predation and Ecology (ed.by I.Hanski and Y.Cambefort), pp.350±365. germination. Journal of Tropical Ecology, 14, 199±215. Princeton University Press, Princeton, New Jersey. Siegel, S. & Castellan, N.J., Jr (1988) Nonparametric Statistics for Hoshizaki, K., Suzuki, W. & Sasaki, S. (1997) Impacts of the Behavioral Sciences.McGraw-Hill Co.,New York. secondary seed dispersal and herbivory on seedling survival in Sokal, R.R. & Rohlf, F.J. (1995) Biometry.W.H.Freeman, Aesculus turbinata. Journal of Vegetation Science, 8, 735±742. New York. Howden, H.F. & Nealis, V.G. (1975) Effects of clearing in a Terborgh, J.(1986) Community aspects of frugivory in tropical tropical rain forest on the composition of the coprophagous forests. Frugivores and Seed Dispersal (ed.by A.Estrada and scarab beetle fauna (Coleoptera). Biotropica, 7, 777±783. T.H.Fleming), pp.371±384.Dr W.Junk Publishers, Dordrecht, Howe, H.F. (1989) Scatter- and clump-dispersal and seedling The Netherlands. demography: hypothesis and implications. Oecologia, 79, Vulinec, K.(2000) Dung beetles (Coleoptera: Scarabeidae), 417±426. monkeys, and conservation in Amazonia. Florida Entomologist, Howe, H.F. (1990) Seed dispersal by birds and mammals: 83, 229±241. implications for seedling demography. Reproductive Ecology of Waage, J.K. & Best, R.C. (1985) associates of sloths. Tropical Forest Plants (ed.by K.S.Bawa and M.Hadley), The Evolution and Ecology of Armadillos, Sloths, and Vermi- pp.191±218.UNESCO and The Parthenon Publishing Group, linguas (ed.by G.G.Montgomery), pp.319±322.Smithsonian Paris. Institution Press, Washington, DC. Howe, H.F. & Smallwood, J. (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201±228. Accepted 23 August 2001

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 Dung beetles as seed dispersers 269

Appendix. Species of dung beetles captured in 14 diurnal and 14 nocturnal trapping periods (10 traps per period, each baited with 25 g of dung).

Number of Body length (mm) individuals captured Dung Diel processing Species Mean SE n Day Night Total activity behaviour Aphodius sp. 1 3.5 0.13 8 3 200 203 n D Aphodius sp. 2 2.4 0.12 7 12 155 167 n D Ateuchus sp. 2 4.3 0.12 9 936 129 1065 d T Ateuchus sp. 3 2.9 0.11 5 227 30 257 d T Ateuchus sp. 4 4.4 0.08 6 4 2 6 ? T Ateuchus sp. 5 6.5 0.10 10 12 316 328 n T Ateuchus sp. 6 6.7 0.09 8 9 194 203 n T Ateuchus sp. 7 4.4 0.10 6 9 7 16 ? T Canthidium sp. 1 3.2 0.06 10 375 43 418 d T Canthidium sp. 2 6.4 0.24 8 50 2 52 d T Canthidium sp. 3 3.6 0.08 6 15 4 19 d T Canthidium sp. 4 4.6 0.11 6 30 849 879 n T Canthidium sp. 5 3.4 0.10 7 82 2 84 d T Canthidium sp. 6 5.5 0.14 10 243 21 264 d T Canthidium sp. 7 4.8 0.12 10 416 37 453 d T Canthidium sp. 8 7.4 0.26 10 0 345 345 n T Canthidium sp. 9 7.7 0.22 9 0 34 34 n T Canthon sordidus (Har.) 6.2 0.14 10 11 0 11 d R Canthon sp.1 6.5 1 2 0 2 ? R Canthon sp. 2 5.1 0.15 9 73 5 78 d R Canthon sp. 3 6.6 0.19 10 34 0 34 d R Canthon triangularis (Drury) 9.5 0.21 10 75 3 78 d R Coprophanaeus lancifer (L.) 38.4 0.91 10 0 1 1 ? T Cryptocanthon peckorum (Howden) 2.3 0.10 5 7 22 29 n R Deltochilum carinatum Westwood 7.7 0.15 9 0 7 7 n R Deltochilum guyanensis Paulian 12.4 0.19 10 0 27 27 n R Deltochilum orbiculare Lansberge 24.8 0.61 10 1 28 29 n R Deltochilum pseudoicarus Balthasar 24.3 0.55 9 0 9 9 n R Dichotomius boreus (Oliv.) 24.7 0.50 10 0 254 254 n T Dichotomius lucasi (LuÈ derwaldt) 12.1 0.24 9 3 629 632 n T Dichotomius sp. 1 16.1 0.34 7 0 44 44 n T Dichotomius sp. 2 15.3 0.24 8 0 25 25 n T Dichotomius subaeneus (Laporte) 16.6 0.50 10 0 38 38 n T Eurysternus caribaeus (Herbst) 14.1 0.44 10 18 20 38 d=n* Eurysternus hirtellus Dalman 6.1 0.29 10 65 0 65 d * Eurysternus velutinus Bates 16.9 0.30 10 7 2 9 ? * Neocanthidium atricolle (Preudh.) 8.9 0.30 10 49 1 50 d T Neocanthidium auricolle (Har.) 8.1 0.17 10 27 5 32 d T Neocanthidium sp.1 4.9 1 7 0 7 d T Ontherus carinifrons LuÈ derwaldt 12.4 0.45 10 0 51 51 n T Onthophagus bidentatus Drapiez 5.3 0.20 10 146 48 194 d T Onthophagus sp.2 5.0 1 31 3 34 d T Oxysternon durantoni Arnaud 14.6 0.35 8 85 0 85 d T Oxysternon festivum d'Olsovfieff 20.1 0.48 6 27 0 27 d T Oxysternon prox. silenum 15.2 0.45 10 52 1 53 d T Phanaeus chalcomelas (Perty) 13.5 0.27 8 54 0 54 d T Scybalocanthon pygidialis (Schmidt) 8.4 0.11 10 87 10 97 d R Uroxys pygmaeus Har. 2.7 0.10 10 81 1655 1736 n T sp. AA 2.8 0.60 2 5 2 7 ? ? sp. DD 10.2 0.21 5 0 1 1 ? ? sp.EE 2.2 1 0 1 1 ? ? sp. FF 14.3 0.39 6 0 4 4 n ? sp. GG 6.3 0.12 10 0 25 25 n ?

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270 270 Ellen Andresen

Appendix. Continued.

Number of Body length (mm) individuals captured Dung Diel processing Species Mean SE n Day Night Total activity behaviour sp. H 3.5 0.32 4 5 0 5 d ? sp. HH 4.3 0.10 2 0 2 2 ? ? sp.JJ 9.8 1 0 1 1 ? ? sp.O 2.0 1 9 9 18 d =n? sp. P 1.6 0.10 2 28 6 34 d ? sp. R 6.2 0.22 6 0 7 7 n ? sp. W 2.7 0.10 10 11 4 15 d ? sp.Y 1.5 1 101 1 102 d ?

Mean body length, standard error, and number of individuals measured are given in the first three columns.The last two columns classify dung beetles according to their diel activity (d ˆ mostly diurnal, n ˆ mostly nocturnal), and according to their dung processing behaviour (T ˆ tunnellers, R ˆ rollers, D ˆ dwellers).*Indicates a unique dung processing behaviour in which dung balls are only lightly covered by soil.

# 2002 Royal Entomological Society, Ecological Entomology, 27, 257±270