Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale.

Understanding the distribution of biodiversity across the Earth is one of the most challenging questions in biology. Much research has been directed at explaining the species latitudinal pattern showing that communities are richer in tropical areas; however, despite decades of research, a general consensus has not yet emerged. In addition, global biodiversity patterns are being rapidly altered by human activities. Here, we aim to describe large-scale patterns of species richness and diversity in terrestrial vertebrate scavenger (carrion-consuming) assemblages, which provide key ecosystem functions and services. We used a worldwide dataset comprising 43 sites, where vertebrate scavenger assemblages were identified using 2,485 carcasses monitored between 1991 and 2018. First, we evaluated how scavenger richness (number of species) and diversity (Shannon diversity index) varied among seasons (cold vs. warm, wet vs. dry). Then, we studied the potential effects of human impact and a set of macroecological variables related to climatic conditions on the scavenger assemblages. Vertebrate scavenger richness ranged from species-poor to species rich assemblages (4-30 species). Both scavenger richness and diversity also showed some seasonal variation. However, in general, climatic variables did not drive latitudinal patterns, as scavenger richness and diversity were not affected by temperature or rainfall. Rainfall seasonality slightly increased the number of species in the community, but its effect was weak. Instead, the human impact index included in our study was the main predictor of scavenger richness. Scavenger assemblages in highly human-impacted areas sustained the smallest number of scavenger species, suggesting human activity may be overriding other macroecological processes in shaping scavenger communities. Our results highlight the effect of human impact at a global scale. As species-rich assemblages tend to be more functional, we warn about possible reductions in ecosystem functions and the services provided by scavengers in human-dominated landscapes in the Anthropocene.

Multilocus phylogeny of the zebra mussel family Dreissenidae (Mollusca: Bivalvia) reveals a fourth Neotropical genus sister to all other genera.

Dreissenidae is one of the most economically and ecologically important families of freshwater and estuarine mollusks. Fourteen extant species and three genera are currently recognized: Congeria contains three species from karst caves along the eastern Adriatic coast and one from the Orinoco River of Venezuela, Dreissena contains six species native to Eastern European rivers and estuaries, and Mytilopsis contains three species from the Gulf of Mexico, Caribbean, and northwestern coast of South America and one from the Tocantins River of Brazil. Previous molecular phylogenetic studies have examined all species except those from South American rivers, and found each genus to be monophyletic with Congeria and Mytilopsis forming a clade sister to Dreissena. We present the first multilocus phylogeny of Dreissenidae inclusive of South American riverine species. Bayesian and maximum likelihood analyses of a 3085 bp alignment consisting of mitochondrial (COI and 16S) and nuclear (18S and 28S) gene regions found Neotropical species to be consistently and strongly supported as sister to all other dreissenids, although incomplete sequencing of the single Orinoco specimen obscured Neotropical monophyly. Our intergeneric relationships are inconsistent with an extensive fossil record suggesting that dreissenids originated in Europe approximately 30 My before dispersing to the Western Hemisphere. Fossil-calibrated analyses indicated that Neotropical dreissenids diverged from European lineages in the mid to late Eocene (∼39.3 Ma), and Brazilian and Guiana shield populations diversified during the Oligocene to Miocene. We erect the new genus Rheodreissena for all Neotropical freshwater dreissenids and present haplotype data indicative of at least three species. Widespread anthropogenic alteration of the middle Xingu River and lower Amazon threatens the persistence of these endemic, poorly studied mussels and may facilitate introduction beyond their native range.

Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities.

Carrion is a valuable nutrient resource used by a diversity of vertebrates across the globe. However, vertebrate scavenging ecology remains an understudied area of science, especially in regards to how biotic and abiotic factors influence scavenging community composition. Here we elucidate how fundamental biotic and abiotic factors interact to modulate the efficiency and composition of vertebrate scavengers by investigating scavenging dynamics across a large gradient in carcass sizes and habitat types representative of many temperate ecosystems, as well as between two seasons reflecting differences in invertebrate activity. We found carcass size and season influenced carcass fate and persistence, as well as the richness and composition of vertebrate scavenger communities utilizing carrion resources. Species richness, which increased as carcass size increased and was higher during the cool season, had a significant effect on carcass persistence. In addition, habitat type influenced carcass detection times by vertebrates, and we observed relatively distinct scavenging communities associated with carcasses of differing sizes. This research highlights a pervasive limitation to the interpretation of results of previous studies as research failing to incorporate carcass size and habitat type could result in the over or underrepresentation of vertebrate scavengers in food web dynamics.

Bioaccumulation of contaminants in Scarabaeidae and Silphidae beetles at sites polluted by coal combustion residuals and radiocesium.

Anthropogenic contamination from coal-fired power plants and nuclear reactors is a pervasive issue impacting ecosystems across the globe. As a result, it is critical that studies continue to assess the accumulation and effects of trace elements and radionuclides in a diversity of biota. In particular, bioindicator species are a powerful tool for risk assessment of chemically contaminated habitats. Using inductively coupled plasma mass spectrometry (ICP-MS) and auto-gamma counting, we analyzed trace element and radiocesium contaminant concentrations in Scarabaeidae and Silphidae beetles (Order: Coleoptera), important taxa in decomposition and nutrient cycling, at contaminated and reference sites on the Savannah River Site, South Carolina, U.S. Our results revealed variability in trace element concentrations between Scarabaeidae and Silphidae beetles at uncontaminated and contaminated sites. Compared to Scarabaeidae, Silphidae had higher levels of chromium (Cr), copper (Cu), iron (Fe), manganese (Mn), nickel (Ni), and zinc (Zn). Unexpectedly, concentrations of Cr, Cu, and Ni were higher in both taxa at the uncontaminated sites. Scarabaeidae and Silphidae beetles at the coal combustion waste site consistently had high concentrations of arsenic (As), and Scarabaeidae had high concentrations of selenium (Se). Of the 50 beetles analyzed for radiocesium levels, two had elevated radioactivity concentrations, both of which were from a site contaminated with radionuclides. Our results suggest carrion beetles may be particularly sensitive to bioaccumulation of contaminants due to their trophic position and role in decomposition, and thus are useful sentinels of trace element and radionuclide contamination.

Functional traits driving species role in the structure of terrestrial vertebrate scavenger networks.

Species assemblages often have a non-random nested organization, which in vertebrate scavenger (carrion-consuming) assemblages is thought to be driven by facilitation in competitive environments. However, not all scavenger species play the same role in maintaining assemblage structure, as some species are obligate scavengers (i.e., vultures) and others are facultative, scavenging opportunistically. We used a database with 177 vertebrate scavenger species from 53 assemblages in 22 countries across five continents to identify which functional traits of scavenger species are key to maintaining the scavenging network structure. We used network analyses to relate ten traits hypothesized to affect assemblage structure with the "role" of each species in the scavenging assemblage in which it appeared. We characterized the role of a species in terms of both the proportion of monitored carcasses on which that species scavenged, or scavenging breadth (i.e., the species "normalized degree"), and the role of that species in the nested structure of the assemblage (i.e., the species "paired nested degree"), therefore identifying possible facilitative interactions among species. We found that species with high olfactory acuity, social foragers, and obligate scavengers had the widest scavenging breadth. We also found that social foragers had a large paired nested degree in scavenger assemblages, probably because their presence is easier to detect by other species to signal carcass occurrence. Our study highlights differences in the functional roles of scavenger species and can be used to identify key species for targeted conservation to maintain the ecological function of scavenger assemblages.

Effects of industrial disturbances on biodiversity of carrion-associated beetles.

Energy production systems such as nuclear reactors and coal-burning power plants produce a multitude of waste contaminants including radionuclides, trace elements, and heavy metals. Among invertebrates, much of the effort to understand the impact of these contaminants has focused in aquatic environments, while relatively less attention has been on terrestrial communities. We investigated the effects of trace element and radionuclide contamination on assemblages of beetles that are drawn to vertebrate carrion. Samples were collected from riparian sites at the Savannah River Site in South Carolina to compare trap catches (i.e., measure of relative abundance) of beetles and species diversity along a habitat gradient (0-300 m) away from an aquatic habitat and between uncontaminated and contaminated sites. We collected 17,800 carrion-associated beetles representing 112 species in nine families, which were classified as either scavenger or predatory beetles. Beetle catches and species diversity were generally higher at contaminated than uncontaminated sites. These trends were likely driven by scavenger species, which showed similar patterns between sites, whereas patterns of catches and species diversity were variable between sites for predatory beetles. Species compositions of contaminated and uncontaminated sites were generally distinct, however habitat edges appeared to substantially affect beetle assemblages. Overall, our study suggests carrion beetle assemblages are sensitive to edge effects and may exhibit variable responses to the presence of anthropogenic contaminants or disturbances associated with energy production systems. Such results reflect the inherent variability among individual beetle species, populations, and communities to local environmental conditions, and underscores the need for multi-taxa approach in environmental impact assessments.

Development and characterization of 33 novel polymorphic microsatellite markers for the brown tree snake Boiga irregularis.

BACKGROUND: Boiga irregularis is a widespread invasive species on Guam and has led to extirpation of most of the island's native avifauna. There are presently no microsatellite markers for this invasive species, hence we developed highly polymorphic microsatellite markers to allow for robust population genetic studies on Guam. FINDINGS: We isolated and characterized 33 microsatellite loci for the brown tree snake, B. irregularis. The loci were screened across 32 individuals from Guam. The number of alleles per locus ranged from three to ten, with an average of 4.62. The expected (He) and observed heterozygosity (Ho) ranged from 0.294 to 0.856 and from 0.031 to 0.813, with an average of 0.648 and 0.524, respectively. Significant deviations from Hardy-Weinberg equilibrium were detected at seven loci after Bonferoni correction. Probability of identity values ranged from 0.043 to 0.539. CONCLUSIONS: These genetic markers are useful for understanding a suite of post-invasion population genetic parameters, sources of invasions, and effectiveness of management strategies for this invasive species.