Leopard predation on gelada monkeys at Guassa, Ethiopia.

Predation is widely believed to exert strong selective pressure on primate behavior and ecology but is difficult to study and rarely observed. In this study, we describe seven encounters between lone wild leopards (Panthera pardus) and herds of geladas (Theropithecus gelada) over a 6-year period in an intact Afroalpine grassland ecosystem at the Guassa Community Conservation Area, Ethiopia. Three encounters consisted of attempted predation on geladas by leopards, one of which was successful. All three attacks occurred in low-visibility microhabitats (dominated by tussock graminoids, mima mounds, or tall shrubs) that provided leopards with hidden viewsheds from which to ambush geladas. An additional four encounters did not result in an attempted attack but still document the consistently fearful responses of geladas to leopards. In encounters with leopards, geladas typically gave alarm calls (n = 7 of 7 encounters), reduced interindividual distances (n = 5), and collectively fled towards or remained at their sleeping cliffs (n = 7), the only significant refugia in the open-country habitat at Guassa. Geladas did not engage in mobbing behavior towards leopards. Encounters with leopards tended to occur on days when gelada herd sizes were small, raising the possibility that leopards, as ambush hunters, might stalk geladas on days when fewer eyes and ears make them less likely to be detected. We compare the behavioral responses of geladas to leopards at Guassa with those previously reported at Arsi and the Simien Mountains and discuss how gelada vulnerability and responses to leopards compare with those of other primate species living in habitats containing more refugia. Lastly, we briefly consider how living in multilevel societies may represent an adaptive response by geladas and other open-country primates to predation pressure from leopards and other large carnivores.

New approaches to modeling primate socioecology: Does small female group size BEGET loyal males?

Humans are unusual in having stable male-female breeding bonds within multi-level societies. Such societies are not found in other apes, but have evolved independently in other primates, including several African papionins: hamadryas and Guinea baboons and gelada monkeys. Stable breeding bonds have been proposed to evolve either (1) because males can monopolize females when food distribution forces females to forage in small groups or (2) because females exchange exclusive mating for male services, such as protection from infanticide. Comparative studies are needed to test these hypotheses. In the meantime, we used an agent-based computer model to test the plausibility of these hypotheses. We simulated primates living in social groups within a larger population using a model we call BEGET (Behavior, Ecology, Genetics, Evolution, and Tradeoffs), which employed decision vectors, experimental evolution, realistic trade-offs, and phenotypic plasticity. We employed experimental evolution to generate male genotypes that varied in their competitive ability and in their long-term mating strategy. "Rover" males searched for and mated with any sexually receptive females whereas "Loyalist" males formed stable associations with particular groups of females. Much like living primates, the virtual primates exhibited tradeoffs between contest and scramble competition for access to females: Loyalists evolved larger body size than Rovers. We tested the effect of female foraging group size and the presence of infanticide and infant protection on the relative success of these strategies. We found that Loyalists achieved greater reproductive success than Rovers only when females were in groups smaller than four. Both Rovers and Loyalists sometimes evolved infanticidal behavior, but the presence of infanticide benefited Rovers rather than Loyalists, suggesting that the evolution of stable breeding bonds depends on the spatial distribution of females, rather than the risk of infanticide.

Carbon Amendments Alter Microbial Community Structure and Net Mercury Methylation Potential in Sediments.

Neurotoxic methylmercury (MeHg) is produced by anaerobic Bacteria and Archaea possessing the genes hgcAB, but it is unknown how organic substrate and electron acceptor availability impacts the distribution and abundance of these organisms. We evaluated the impact of organic substrate amendments on mercury (Hg) methylation rates, microbial community structure, and the distribution of hgcAB+ microbes with sediments. Sediment slurries were amended with short-chain fatty acids, alcohols, or a polysaccharide. Minimal increases in MeHg were observed following lactate, ethanol, and methanol amendments, while a significant decrease (∼70%) was observed with cellobiose incubations. Postincubation, microbial diversity was assessed via 16S rRNA amplicon sequencing. The presence of hgcAB+ organisms was assessed with a broad-range degenerate PCR primer set for both genes, while the presence of microbes in each of the three dominant clades of methylators (Deltaproteobacteria, Firmicutes, and methanogenic Archaea) was measured with clade-specific degenerate hgcA quantitative PCR (qPCR) primer sets. The predominant microorganisms in unamended sediments consisted of Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria Clade-specific qPCR identified hgcA+Deltaproteobacteria and Archaea in all sites but failed to detect hgcA+Firmicutes Cellobiose shifted the communities in all samples to ∼90% non-hgcAB-containing Firmicutes (mainly Bacillus spp. and Clostridium spp.). These results suggest that either expression of hgcAB is downregulated or, more likely given the lack of 16S rRNA gene presence after cellobiose incubation, Hg-methylating organisms are largely outcompeted by cellobiose degraders or degradation products of cellobiose. These results represent a step toward understanding and exploring simple methodologies for controlling MeHg production in the environment.IMPORTANCE Methylmercury (MeHg) is a neurotoxin produced by microorganisms that bioacummulates in the food web and poses a serious health risk to humans. Currently, the impact that organic substrate or electron acceptor availability has on the mercury (Hg)-methylating microorganisms is unclear. To study this, we set up microcosm experiments exposed to different organic substrates and electron acceptors and assayed for Hg methylation rates, for microbial community structure, and for distribution of Hg methylators. The sediment and groundwater was collected from East Fork Poplar Creek in Oak Ridge, TN. Amendment with cellobiose (a lignocellulosic degradation by-product) led to a drastic decrease in the Hg methylation rate compared to that in an unamended control, with an associated shift in the microbial community to mostly nonmethylating Firmicutes This, along with previous Hg-methylating microorganism identification methods, will be important for identifying strategies to control MeHg production and inform future remediation strategies.

Humans as a model species for sexual selection research.

Ever since Darwin, questions about humans have driven sexual selection research. While studies of other organisms are often justified as useful for improving understanding of humans, humans themselves can be useful models. Although humans present some drawbacks as model organisms (complicated societies, slow reproduction and strong ethical constraints on experimental options), humans nonetheless offer many advantages (being abundant, accessible and having detailed historical records for some populations). As an additional challenge, humans exhibit a rather puzzling combination of traits. Some traits (pair-bonding, biparental care and modest sexual dimorphism in body size) suggest selection for monogamous mating, while other traits (including sexual dimorphism in body composition and appearance) suggest selection for polygyny. Such puzzles have motivated research on other species, resulting in a rich set of comparative data that provides insights into humans and other species. Recent studies of visual trait dimorphism suggest that human appearance reflects adaptation for multi-level societies, rather than high levels of polygyny. In addition to biological traits, human cultural traits have undergone rapid evolution. Changes in subsistence strategies profoundly affect opportunities for sexual selection. The enormous variability of human behaviour and ecology provides abundant opportunities to test key hypotheses, and poses challenging puzzles for future research.

Comparative primate obstetrics: Observations of 15 diurnal births in wild gelada monkeys (Theropithecus gelada) and their implications for understanding human and nonhuman primate birth evolution.

OBJECTIVES: The birth process has been studied extensively in many human societies, yet little is known about this essential life history event in other primates. Here, we provide the most detailed account of behaviors surrounding birth for any wild nonhuman primate to date. MATERIALS AND METHODS: Over a recent ∼10-year period, we directly observed 15 diurnal births (13 live births and 2 stillbirths) among geladas (Theropithecus gelada) at Guassa, Ethiopia. During each birth, we recorded the occurrence (or absence) of 16 periparturitional events, chosen for their potential to provide comparative evolutionary insights into the factors that shaped birth behaviors in humans and other primates. RESULTS: We found that several events (e.g., adopting standing crouched positions, delivering infants headfirst) occurred during all births, while other events (e.g., aiding the infant from the birth canal, licking infants following delivery, placentophagy) occurred during, or immediately after, most births. Moreover, multiparas (n = 9) were more likely than primiparas (n = 6) to (a) give birth later in the day, (b) isolate themselves from nearby conspecifics while giving birth, (c) aid the infant from the birth canal, and (d) consume the placenta. DISCUSSION: Our results suggest that prior maternal experience may contribute to greater competence or efficiency during the birth process. Moreover, face presentations (in which infants are born with their neck extended and their face appearing first, facing the mother) appear to be the norm for geladas. Lastly, malpresentations (in which infants are born in the occiput anterior position more typical of human infants) may be associated with increased mortality in this species. We compare the birth process in geladas to those in other primates (including humans) and discuss several key implications of our study for advancing understanding of obstetrics and the mechanism of labor in humans and nonhuman primates.

Fitness impacts of tapeworm parasitism on wild gelada monkeys at Guassa, Ethiopia.

Parasitism is expected to impact host morbidity or mortality, although the fitness costs of parasitism have rarely been quantified for wildlife hosts. Tapeworms in the genus Taenia exploit a variety of vertebrates, including livestock, humans, and geladas (Theropithecus gelada), monkeys endemic to the alpine grasslands of Ethiopia. Despite Taenia's adverse societal and economic impacts, we know little about the prevalence of disease associated with Taenia infection in wildlife or the impacts of this disease on host health, mortality and reproduction. We monitored geladas at Guassa, Ethiopia over a continuous 6½ year period for external evidence (cysts or coenuri) of Taenia-associated disease (coenurosis) and evaluated the impact of coenurosis on host survival and reproduction. We also identified (through genetic and histological analyses) the tapeworms causing coenurosis in wild geladas at Guassa as Taenia serialis. Nearly 1/3 of adult geladas at Guassa possessed ≥1 coenurus at some point in the study. Coenurosis adversely impacted gelada survival and reproduction at Guassa and this impact spanned two generations: adults with coenuri suffered higher mortality than members of their sex without coenuri and offspring of females with coenuri also suffered higher mortality. Coenurosis also negatively affected adult reproduction, lengthening interbirth intervals and reducing the likelihood that males successfully assumed reproductive control over units of females. Our study provides the first empirical evidence that coenurosis increases mortality and reduces fertility in wild nonhuman primate hosts. Our research highlights the value of longitudinal monitoring of individually recognized animals in natural populations for advancing knowledge of parasite-host evolutionary dynamics and offering clues to the etiology and control of infectious disease.