The value of trophic interactions for ecosystem function: dung beetle communities influence seed burial and seedling recruitment in tropical forests.
ABSTRACT: Anthropogenic activities are causing species extinctions, raising concerns about the consequences of changing biological communities for ecosystem functioning. To address this, we investigated how dung beetle communities influence seed burial and seedling recruitment in the Brazilian Amazon. First, we conducted a burial and retrieval experiment using seed mimics. We found that dung beetle biomass had a stronger positive effect on the burial of large than small beads, suggesting that anthropogenic reductions in large-bodied beetles will have the greatest effect on the secondary dispersal of large-seeded plant species. Second, we established mesocosm experiments in which dung beetle communities buried Myrciaria dubia seeds to examine plant emergence and survival. Contrary to expectations, we found that beetle diversity and biomass negatively influenced seedling emergence, but positively affected the survival of seedlings that emerged. Finally, we conducted germination trials to establish the optimum burial depth of experimental seeds, revealing a negative relationship between burial depth and seedling emergence success. Our results provide novel evidence that seed burial by dung beetles may be detrimental for the emergence of some seed species. However, we also detected positive impacts of beetle activity on seedling recruitment, which are probably because of their influence on soil properties. Overall, this study provides new evidence that anthropogenic impacts on dung beetle communities could influence the structure of tropical forests; in particular, their capacity to regenerate and continue to provide valuable functions and services.
Project description:Dung beetles are secondary seed dispersers, incidentally moving many of the seeds defecated by mammals vertically (seed burial) and/or horizontally as they process and relocate dung. Although several studies have quantified this ecological function of dung beetles, very few have followed seed fate until seedling establishment, and most of these have focused on the effects of seed burial. We know very little about the effects of horizontal seed movement by dung beetles, though it is generally assumed that it will affect plant recruitment positively through diminishing seed clumping. The objective of our study was to assess the effects of dung beetle activity on the spatial distribution of seeds and seedlings, and on the probability of seedling establishment. In a tropical rainforest in Mexico we carried out two complementary field experiments for each of two tree species (Bursera simaruba and Poulsenia armata), using seeds experimentally imbedded in pig dung and recording their fate and spatial location over time. For both species, dung beetle activity reduced the spatial clumping of seeds and seedlings; however, it did not increase the probability of seedling establishment. We discuss the context- and species-specificity of the combined effects of horizontal and vertical dispersal of seeds by dung beetles, and the need to quantify long-term seedling fates to more accurately determine the effects of seed movement by dung beetles on plant recruitment.
Project description:Seed burial in the sediment is critical for successful seedling establishment in seagrasses because it protects from predation and dispersal into unsuitable sites, and it may enhance germination by exposing the seeds to suitable germination stimuli. However, relatively little is known about the fate of buried seeds and their ability to emerge from greater depths. The goal of this study was to determine seed survival in the sediment, seedling emergence success and initial seedling biomass of Zostera marina in relation to burial depth and to evaluate if large seeds, having larger energy reserves, are more tolerant to burial than small seeds. Seeds from a perennial Z. marina population were buried at 7 different sediment depths (0.1-8 cm), and seeds sorted by size (large and small) were buried at depths of 2, 4 and 6 cm in outdoor mesocosms. Total seedling emergence after 2 months was significantly affected by seed burial depth, with maximum values in the top 2 cm of the sediment (48.1-56.7% of planted seeds), and a marked decline below 4 cm depth to only 5% seedling emergence at the deepest burial depth of 8 cm. Moreover, seeds had shorter time to emergence from shallow compared to deep burial depths. At all burial depths, a small fraction of seeds (<10%) died after germination but before emerging, and 15-30% remained viable after 6 months. Seed mortality was the major limitation to seedling recruitment from the deeper burial depths. The effect of seed size on seedling emergence success and time was not clear, but heavier seeds displayed greater longevity and gave rise to seedlings of significantly higher biomass, indicating that the mobilization of metabolic reserves may be important during initial seedling development.
Project description:Because animal feces contain organic matter and plant seeds, dung beetles (Scarabaeinae) are important for the circulation of materials and secondary seed dispersal through burying feces. Dung beetles are usually generalists and use the feces of various mammals. Additionally, the larval stages have access to feces from only one mammal species leaving them susceptible to changes in animal fauna and variations in animal populations. Here, we explain the effects of resource availability changes associated with sika deer (Cervus nippon) overabundance on dung beetle larvae feeding habits in Japan. ?15N values were notably higher in raccoon dog and badger dung than in that of other mammals. A dung beetle breeding experiment revealed that the ?15N values of dung beetle exoskeletons that had fed on deer feces during their larval stage were significantly lower than those of beetles that had fed on raccoon dog feces. The ?15N values of the adult exoskeleton were significantly lower in a deer high-density area than in a low-density area in large dung beetles only. It is possible that the high-quality feces, such as those of omnivores, preferred by the large beetles decrease in availability with an increase in deer dung; large beetles may therefore be unable to obtain sufficient high-quality feces and resort to using large amounts of low-quality deer feces. Small dung beetles may use the easily obtained feces that is in high abundance and they may also use deer feces more frequently with increases in deer density. These findings suggest that a larval resource shift associated with deer overabundance may affect ecosystem functions such as soil nutrient cycling and seed dispersal.
Project description:Body-size is an important trait for predicting how species contribute to ecosystem functions and respond to environmental stress. Using the dung beetle <i>Onthophagus nuchicornis</i> (Coleoptera: Scarabaeidae), we explored how variation in body-size affected ecosystem functioning (dung burial) and sensitivity to an environmental stressor (exposure to the veterinary anthelmintic ivermectin). We found that large beetles buried nearly 1.5-fold more dung than small beetles, but that mortality from exposure to a range of concentrations of ivermectin did not differ between large and small beetles. Unexpectedly, we found that exposure to low concentrations of ivermectin (0.01?-1 mg ivermectin per kg dung) stimulated dung burial in both small and large beetles. Our results provide evidence of ecological functioning hormesis stemming from exposure to low amounts of a chemical stressor that causes mortality at high doses.
Project description:The interaction between the seed beetle Zabrotes subfasciatus and its parasitoid Stenocorse bruchivora, was investigated on seeds of two populations of wild lima bean, Phaseolus lunatus. By manipulating the number of beetle larvae per seed and the presence of parasitoids, we determined how factors related to beetle larvae density, the seed in which they feed and the parasitoid, may interact and affect host and parasitoid survival. Results showed that an increase in larval beetle density had a negative impact on beetle performance. This effect cascaded up to parasitoids, high larval density strongly reduced parasitoid emergence. Also, parasitoid presence resulted in faster beetle development and lower female weight. An interactive effect between larval host density and parasitoid presence affected the number of insects that emerged from the seeds. Beetle performance was better in the bean population with the largest seeds, while parasitoid emergence was the lowest in these seeds. This study shows that the impact of parasitoids on seed beetles is contingent on the interaction between density-mediated (direct mortality) and trait-mediated (e.g. non-consumptive) effects. Indirect trait-mediated effects of natural enemies are likely prevalent across insect communities, understanding their role in driving host-parasitoid interactions can have important implications for biological control.
Project description:Scatter hoarding of seeds by animals contributes significantly to forest-level processes, including plant recruitment and forest community composition. However, the potential positive and negative effects of caching on seed survival, germination success, and seedling survival have rarely been assessed through experimental studies. Here, I tested the hypothesis that seed burial mimicking caches made by scatter hoarding Central American agoutis (Dasyprocta punctate) enhances seed survival, germination, and growth by protecting seeds from seed predators and providing favorable microhabitats for germination. In a series of experiments, I used simulated agouti seed caches to assess how hoarding affects seed predation by ground-dwelling invertebrates and vertebrates for four plant species. I tracked germination and seedling growth of intact and beetle-infested seeds and, using exclosures, monitored the effects of mammals on seedling survival through time. All experiments were conducted over three years in a lowland wet forest in Costa Rica. The majority of hoarded palm seeds escaped predation by both invertebrates and vertebrates while exposed seeds suffered high levels of infestation and removal. Hoarding had no effect on infestation rates of D. panamensis, but burial negatively affected germination success by preventing endocarp dehiscence. Non-infested palm seeds had higher germination success and produced larger seedlings than infested seeds. Seedlings of A. alatum and I. deltoidea suffered high mortality by seed-eating mammals. Hoarding protected most seeds from predators and enhanced germination success (except for D. panamensis) and seedling growth, although mammals killed many seedlings of two plant species; all seedling deaths were due to seed removal from the plant base. Using experimental caches, this study shows that scatter hoarding is beneficial to most seeds and may positively affect plant propagation in tropical forests, although tradeoffs in seed survival do exist.
Project description:Research suggests dung beetles can churn, aerate, and desiccate dung in ways that influence the dung and soil microbes producing greenhouse gases (GHGs). We examined the impacts of the tunneling beetle, Onthophagus taurus (Schreber), and the dwelling beetle, Labarrus pseudolividus (Balthasar), on the carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O) emitted from pasture-laid bovine dung as well as their sum-total (CO2 + CH4 + N2O) effect on global warming, or their carbon dioxide equivalent (CO2e). Despite dung beetles potential effects on CH4 and N2O, the existing literature shows no ultimate CO2e reductions. We hypothesized that more dung beetles would degrade pats faster and reduce CO2e, and so we increased the average dung beetle biomass per dung volume 6.22× above previously published records, and visually documented any dung damage. However, the time effects were 2-5× greater for any GHG and CO2e (E = 0.27-0.77) than dung beetle effects alone (E = 0.09-0.24). This suggests that dung beetle communities cannot adequately reduce GHGs unless they can accelerate dung decomposition faster than time alone.
Project description:Insects in seasonal tropics experience a wide range of temperatures along seasons, habitats, and a day. Therefore, the thermal tolerance of the insects can be a major driver for their habitat preference, temporal patterns of activity, and formation of communities. We examined the dung beetle communities of eleven pairs of neighboring open (home gardens) and closed habitats (sacred groves) during dry and wet seasons and diel periods (day and night) to understand the dung beetle activities along a spatiotemporal gradient constituted by the sacred groves-home garden matrix on a tropical village landscape. We tested the following hypotheses: (i) closed habitats have greater activities of dung beetles over open habitats; (ii) the diurnal communities of dung beetles are different from the nocturnal communities; and (iii) the diurnal-nocturnal activities of dung beetles could be predicted by the habitat and season. We considered abundance, richness, total biomass, and Shannon diversity of overall beetles, abundance of different functional groups, and species composition in communities as the quantitative measures in the predictive statistical models. In total, 2727 dung beetles belonging to 38 species, ten genera, and three functional groups were collected. The open habitat supported more number of dung beetles (N = 2318) than the closed habitat (N = 409). The diurnal communities were different from nocturnal communities, particularly in open habitat, where the temperature was different between day and night. The dominant species of the diurnal communities of open habitat hardly used the closed habitat in any context including dry-wet seasons, but the nocturnal communities of the open habitat were closer to the communities of closed habitat. The diel period and habitat predicted the abundance activity of functional groups; season was a poor predictor of dung beetle activities. Given that the species composition has turned over across habitats, and the closed habitat supported remarkably lesser number of beetles than the open habitats, the closed habitat is unlikely to be a thermal refuge for the open habitat species in village landscapes that have island forests, such as sacred groves, and home gardens form a matrix.
Project description:The process of seed dispersal of many animal-dispersed plants is frequently mediated by a small set of biotic agents. However, the contribution that each of these dispersers makes to the overall recruitment may differ largely, with important ecological and management implications for the population viability and dynamics of the species implied in these interactions. In this paper, we compared the relative contribution of two local guilds of scatter-hoarding animals with contrasting metabolic requirements and foraging behaviours (rodents and dung beetles) to the overall recruitment of two Quercus species co-occurring in the forests of southern Spain. For this purpose, we considered not only the quantity of dispersed seeds but also the quality of the seed dispersal process. The suitability for recruitment of the microhabitats where the seeds were deposited was evaluated in a multi-stage demographic approach. The highest rates of seed handling and predation occurred in those microhabitats located under shrubs, mostly due to the foraging activity of rodents. However, the probability of a seed being successfully cached was higher in microhabitats located beneath a tree canopy as a result of the feeding behaviour of beetles. Rodents and beetles showed remarkable differences in their effectiveness as local acorn dispersers. Quantitatively, rodents were much more important than beetles because they dispersed the vast majority of acorns. However, they were qualitatively less effective because they consumed a high proportion of them (over 95%), and seeds were mostly dispersed under shrubs, a less suitable microhabitat for short-term recruitment of the two oak species. Our findings demonstrate that certain species of dung beetles (such as Thorectes lusitanicus), despite being quantitatively less important than rodents, can act as effective local seed dispersers of Mediterranean oak species. Changes in the abundance of beetle populations could thus have profound implications for oak recruitment and community dynamics.
Project description:Invertebrate-derived DNA (iDNA) sampling in biodiversity surveys is becoming increasingly widespread, with most terrestrial studies relying on DNA derived from the gut contents of blood-feeding invertebrates, such as leeches and mosquitoes. Dung beetles (superfamily Scarabaeoidea) primarily feed on the faecal matter of terrestrial vertebrates and offer several potential benefits over blood-feeding invertebrates as samplers of vertebrate DNA. Importantly, these beetles can be easily captured in large numbers using simple, inexpensive baited traps, are globally distributed, and occur in a wide range of habitats. To build on the few existing studies demonstrating the potential of dung beetles as sources of mammalian DNA, we subjected the large-bodied, Bornean dung beetle (<i>Catharsius renaudpauliani</i>) to a controlled feeding experiment. We analysed DNA from gut contents at different times after feeding using qPCR techniques. Here, we first describe the window of DNA persistence within a dung beetle digestive tract. We found that the ability to successfully amplify cattle DNA decayed over relatively short time periods, with DNA copy number decreasing by two orders of magnitude in just 6 h. In addition, we sampled communities of dung beetles from a lowland tropical rainforest in Sabah, Malaysia, in order to test whether it is possible to identify vertebrate sequences from dung beetle iDNA. We sequenced both the gut contents from large dung beetle species, as well as whole communities of smaller beetles. We successfully identified six mammalian species from our samples, including the bearded pig (<i>Sus barbatus</i>) and the sambar deer (<i>Rusa unicolor</i>)-both vulnerable species on the IUCN red list. Our results represent the first use of dung beetle iDNA to sample Southeast Asian vertebrate fauna, and highlight the potential for dung beetle iDNA to be used in future biodiversity monitoring surveys.