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Dung Beetles in a Central Amazonian Rainforest and Their Ecological Role As Secondary Seed Dispersers

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Dung Beetles in a Central Amazonian Rainforest and Their Ecological Role As Secondary Seed Dispersers Ecological Entomology (2002) 27, 257±270 Dung beetles 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 beetle 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±animal interaction, Scarabaeidae, 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,
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