Showing papers by "Martha M. Robbins published in 2013"

Impact of male infanticide on the social structure of mountain gorillas

Abstract: Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2–3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.

Effective sociodemographic population assessment of elusive species in ecology and conservation management

Abstract: Wildlife managers are urgently searching for improved sociodemographic population assessment methods to evaluate the effectiveness of implemented conservation activities. These need to be inexpensive, appropriate for a wide spectrum of species and straightforward to apply by local staff members with minimal training. Furthermore, conservation management would benefit from single approaches which cover many aspects of population assessment beyond only density estimates, to include for instance social and demographic structure, movement patterns, or species interactions. Remote camera traps have traditionally been used to measure species richness. Currently, there is a rapid move toward using remote camera trapping in density estimation, community ecology, and conservation management. Here, we demonstrate such comprehensive population assessment by linking remote video trapping, spatially explicit capture–recapture (SECR) techniques, and other methods. We apply it to three species: chimpanzees Pan troglodytes troglodytes, gorillas Gorilla gorilla gorilla, and forest elephants Loxodonta cyclotis in Loango National Park, Gabon. All three species exhibited considerable heterogeneity in capture probability at the sex or group level and density was estimated at 1.72, 1.2, and 1.37 individuals per km2 and male to female sex ratios were 1:2.1, 1:3.2, and 1:2 for chimpanzees, gorillas, and elephants, respectively. Association patterns revealed four, eight, and 18 independent social groups of chimpanzees, gorillas, and elephants, respectively: key information for both conservation management and studies on the species' ecology. Additionally, there was evidence of resident and nonresident elephants within the study area and intersexual variation in home range size among elephants but not chimpanzees. Our study highlights the potential of combining camera trapping and SECR methods in conducting detailed population assessments that go far beyond documenting species diversity patterns or estimating single species population size. Our study design is widely applicable to other species and spatial scales, and moderately trained staff members can collect and process the required data. Furthermore, assessments using the same method can be extended to include several other ecological, behavioral, and demographic aspects: fission and fusion dynamics and intergroup transfers, birth and mortality rates, species interactions, and ranging patterns.

Long-Term Temporal and Spatial Dynamics of Food Availability for Endangered Mountain Gorillas in Volcanoes National Park, Rwanda

Abstract: Monitoring temporal and spatial changes in the resource availability of endangered species contributes to their conservation. The number of critically endangered mountain gorillas (Gorilla beringei beringei) in the Virunga Volcano population has doubled over the past three decades, but no studies have examined how food availability has changed during that period. First, we assessed if the plant species consumed by the gorillas have changed in abundance and distribution during the past two decades. In 2009–2010, we replicated a study conducted in 1988–1989 by measuring the frequency, density, and biomass of plant species consumed by the gorillas in 496 plots (ca. 6 km2) in the Karisoke study area in Volcanoes National Park, Rwanda. We expected to observe a decreased presence of major gorilla food plants as a likely result of density-dependent overharvesting by gorillas. Among the five most frequently consumed species (composing approximately 70% of the gorilla's diet, excluding bamboo), two have decreased in availability and abundance, while three have increased. Some species have undergone shifts in their altitudinal distribution, possibly due to regional climatic changes. Second, we made baseline measurements of food availability in a larger area currently utilized by the gorillas. In the extended sampling (n = 473 plots) area (ca. 25 km2), of the five most frequently consumed species, two were not significantly different in frequency from the re-sampled area, while two occurred significantly less frequently, and one occurred significantly more frequently. We discuss the potential impact of gorilla-induced herbivory on changes of vegetation abundance. The changes in the species most commonly consumed by the gorillas could affect their nutrient intake and stresses the importance of monitoring the interrelation among plant population dynamics, species density, and resource use. Am. J. Primatol. 75:267-280, 2013. © 2012 Wiley Periodicals, Inc.

RESEARCH ARTICLE Long-Term Temporal and Spatial Dynamics of Food Availability for Endangered Mountain Gorillas in Volcanoes National Park, Rwanda

Abstract: biomass of plant species consumed by the gorillas in 496 plots (ca. 6 km 2 ) in the Karisoke study area in Volcanoes National Park, Rwanda. We expected to observe a decreased presence of major gorilla food plants as a likely result of density-dependent overharvesting by gorillas. Among the five most frequently consumed species (composing approximately 70% of the gorilla’s diet, excluding bamboo), two have decreased in availability and abundance, while three have increased. Some species have undergone shifts in their altitudinal distribution, possibly due to regional climatic changes. Second, we made baseline measurements of food availability in a larger area currently utilized by the gorillas. In the extended sampling (n = 473 plots) area (ca. 25 km 2 ), of the five most frequently consumed species, two were not significantly different in frequency from the re-sampled area, while two occurred significantly less frequently, and one occurred significantly more frequently. We discuss the potential impact of gorilla-induced herbivory on changes of vegetation abundance. The changes in the species most commonly consumed by the gorillas could affect their nutrient intake and stresses the importance of monitoring the interrelation among plant population dynamics, species density, and resource use. Am. J. Primatol. 75:267–280, 2013. C � 2012 Wiley Periodicals, Inc.

Novel Polyomaviruses of Nonhuman Primates: Genetic and Serological Predictors for the Existence of Multiple Unknown Polyomaviruses within the Human Population

Abstract: Polyomaviruses are a family of small non-enveloped DNA viruses that encode oncogenes and have been associated, to greater or lesser extent, with human disease and cancer. Currently, twelve polyomaviruses are known to circulate within the human population. To further examine the diversity of human polyomaviruses, we have utilized a combinatorial approach comprised of initial degenerate primer-based PCR identification and phylogenetic analysis of nonhuman primate (NHP) polyomavirus species, followed by polyomavirus-specific serological analysis of human sera. Using this approach we identified twenty novel NHP polyomaviruses: nine in great apes (six in chimpanzees, two in gorillas and one in orangutan), five in Old World monkeys and six in New World monkeys. Phylogenetic analysis indicated that only four of the nine chimpanzee polyomaviruses (six novel and three previously identified) had known close human counterparts. To determine whether the remaining chimpanzee polyomaviruses had potential human counterparts, the major viral capsid proteins (VP1) of four chimpanzee polyomaviruses were expressed in E. coli for use as antigens in enzyme-linked immunoassay (ELISA). Human serum/plasma samples from both Cote d'Ivoire and Germany showed frequent seropositivity for the four viruses. Antibody pre-adsorption-based ELISA excluded the possibility that reactivities resulted from binding to known human polyomaviruses. Together, these results support the existence of additional polyomaviruses circulating within the human population that are genetically and serologically related to existing chimpanzee polyomaviruses.

Generalized additive mixed models for disentangling long-term trends, local anomalies, and seasonality in fruit tree phenology.

Abstract: Quantifying temporal patterns of ephemeral plant structures such as leaves, flowers, and fruits gives insight into both plant and animal ecology. Different scales of temporal changes in fruits, for example within- versus across-year variability, are driven by different processes, but are not always easy to disentangle. We apply generalized additive mixed models (GAMMs) to study a long-term fruit presence–absence data set of individual trees collected from a high-altitude Afromontane tropical rain forest site within Bwindi Impenetrable National Park (BINP), Uganda. Our primary aim was to highlight and evaluate GAMM methodology, and quantify both intra- and interannual changes in fruit production. First, we conduct several simulation experiments to study the practical utility of model selection and smooth term estimation relevant for disentangling intra- and interannual variability. These simulations indicate that estimation of nonlinearity and seasonality is generally accurately identified using asymptotic theory. Applied to the empirical data set, we found that the forest-level fruiting variability arises from both regular seasonality and significant interannual variability, with the years 2009–2010 in particular showing a significant increase in the presence of fruits-driven by increased productivity of most species, and a regular annual peak associated occurring at the end of one of the two dry seasons. Our analyses illustrate a statistical framework for disentangling short-term increases/decreases in fruiting effort while pinpointing specific times in which fruiting is atypical, providing a first step for assessing the impacts of regular and irregular (e.g., climate change) abiotic covariates on fruiting phenology. Some consequences of the rich diversity of fruiting patterns observed here for the population biology of frugivores in BINP are also discussed.

RESEARCH ARTICLE Monitoring Ovarian Cycle Activity Via Progestagens in Urine and Feces of Female Mountain Gorillas: A Comparison of EIA and LC-MS Measurements

Abstract: Understanding the reproductive biology of endangered mountain gorillas (Gorilla beringei beringei )i s essential for optimizing conservation strategies, determining any demographic impact of socioecological changes, and providing information for comparative studies of primates. Non‐invasive techniques have been used to assess the reproductive function of many primates and the importance of validating the measurements of hormones metabolites is widely recognized because they may vary even within closely related species. To determineif itis possible to non‐invasively monitorovarian activity in wild mountain gorillas, we used enzyme immunoassays (EIA) to quantify both urinary and fecal excretion of immunoreactive pregnanediol‐3‐glucuronide (iPdG), defined as all metabolites detected by a pregnanediol‐3‐glucuronide immunoassay (PdG EIA). Simultaneously, we performed the liquid chromatography mass spectrometry (LC–MS) to quantify the excretion of pregnanediol in urine and feces. Samples were analyzed over nine cycles of five females from the habituated gorillas monitored by Karisoke Research Center, Rwanda. As an additional indicator for ovulation timing, estrone conjugates (E1C) were measured in a subset of urine samples. The concentrations of iPdG and pregnanediol measured in the same samples were significantly correlated. Urinary concentrations of iPdG and pregnanediol fluctuated over the menstrual cycle but did not reveal any cyclic pattern, whereas a typical preovulatory urinary E1C surge and postovulatory increases of fecal iPdG and pregnanediol were detected. The luteal peaks of iPdG and pregnanediol levels in feces were on average 2.8 and 7.6 times higher, respectively, than averaged levels in the corresponding follicular phase. The relative number of days with observed matings was higher within the presumed fertile window than in the preceding period. Overall, the results indicate that fecal analysis ofiPdG and pregnanediol is suitable for detecting ovulation in female mountain gorillas. Urinary measurements using both EIA and LC–MS appeared to be uninformative for monitoring ovarian activity in this primate. Am. J. Primatol. © 2013 Wiley Periodicals, Inc.

Hand use during non-locomotor behaviours in the wild African Apes

Abstract: Comparative studies of primate grasping and manipulative behaviours in captivity are numerous but there has been little research on hand use in the wild. Hand use during wild non-locomotor behaviours may reveal increased ranges of joint mobility or manipulative behaviours that have been previously ignored or underestimated. Manipulative behaviours in apes can strongly correlate with different habitats at the species and population level. Chimpanzees more often use tools in the wild and thus are thought to be more manipulative than gorillas. However, captive studies have demonstrated high dexterity in both taxa. We investigate hand use during manipulation (e.g. food processing, tool-use) in wild mountain gorillas (Gorilla beringei, Bwindi Impenetrable National Park, Uganda) and wild chimpanzees (Pan troglodytes verus, Tai National Park, Cote d’Ivoire). We used video data collected in the wild that included 32 gorilla (n=9 individuals) and 53 chimpanzee (n=11 individuals) instances of manipulative tasks. Digital images were extracted and analysed frame by frame. Preliminary results show that hand grips are similar between gorillas and chimpanzees during the manipulation of common food objects, such as long plant stems or branches. During the manipulation of species-specific food objects, gorillas use variable thumb-index grips during the manipulation of thistles and small plant stems, while chimpanzees use similar grips during nut-cracking. These preliminary results suggest that Bwindi mountain gorillas have similarly high dexterity as that of Tai chimpanzees despite not being tool-users. Gorillas frequently use precision grasping more to obtain small rather than large food items, which is similar to chimpanzees and other non-human primates.