Demographic Modeling of a Predator-Prey System and Its implication for the Gombe Population of <Emphasis Type="Italic">Procolobus rufomitratus tephrosceles</Emphasis>

We evaluated the viability of colobus populations under conservative estimates of predation by chimpanzees. If fertility and mortality schedules remain constant, intensely hunted red colobus populations will experience negative growth rates if one allows the assumption of stable age structure to persist into the future. Demographic models have many advantages in studies of primate behavior and ecology. Researchers use them to investigate the quality of observed data and to project population growth rates to changes in mortality, fertility, and migration schedules. We used published age-specific death rates for red colobus (Procolobus rufomitratus tephrosceles) in Gombe National Park, Tanzania, to construct model life tables under various mortality scenarios. Selection in life-history traits toward shorter interbirth intervals, reduction in gestation length, and increased dispersal of individuals from source to sink populations and antipredator behavior, show a limited ability to counter the effects of intense predation. At Gombe, where factors such as small reserve size and isolation prevail, current levels of predation by chimpanzees may depress intrinsic growth rates low enough to cause the extirpation of red colobus in the near future.     

Has Predation Shaped the Social Systems of Arboreal Primates?

I studied antipredator behavior in two species of monkeys to elucidate the role of predation in shaping the social systems of arboreal primates. I compared the responses of monkeys to auditory and visual contact with predators to response elicited by sound playback experiments using the recorded calls of predators. Changes in vigilance and aggregation persisting up to 30 min after predator encounter occurred in both cases. Measures of vigilance shed light on individual perceptions of risk, while aggregation measures—intragroup spatial cohesion and polyspecific associations—permit direct inference about the protective benefits of grouping for the monkeys. They responded to real predator encounters and simulations in similar ways. Thus, sound playbacks of predator vocalizations are effective to simulate predator proximity. Contrary to predictions, predator encounters did not lead invariably to increased cohesion within groups or to increased time spent vigilant. Moreover, behavior in polyspecific associations was no different from that in single-species groups. Only red colobus encountering chimpanzees behaved as predicted by increasing vigilance and intragroup cohesion. The red colobus social system may have developed to protect against chimpanzee attack. In contrast, red-tailed monkey encounters with raptors and chimpanzees involved no change in time spent vigilant, coupled with decreases in intragroup cohesion. I conclude that predation is not a uniform selective pressure and patterns of social behavior within groups do not predict antipredator behavior.     

Primate population dynamics over 32.9 years at Ngogo, Kibale National Park, Uganda

We present census data for eight primate species spanning 32.9 years along the same transect at Ngogo, Kibale National Park, Uganda, demonstrating major changes in the composition of the primate community. Correlated with an estimated decline of ～89% in the red colobus population was an increase in encounter rates with chimpanzee parties. Our data, along with the unusually high rates of predation by chimpanzees on red colobus at Ngogo and the fact that the chimpanzee community at Ngogo is the largest ever recorded, support the conclusion that the red colobus decline was caused primarily by chimpanzee predation. This seems to be the first documented case of predation by one nonhuman primate causing the population decline in another. We evaluated disease and interspecific competition as other possible causes of the red colobus decline, but judged them to be relatively insignificant compared with predation by chimpanzees. Notable changes in encounter rates with other primate species may have resulted from forest expansion. Those for mangabeys, redtails, and black and white colobus increased significantly. Encounter rates increased for l'Hoest's monkeys too, but the increased sightings may have been an artifact of increased habituation. Sightings of blue monkey and baboon groups declined. There was no significant change in encounter rates for all species combined. The Ngogo primate community seemed to be in a nonequilibrium state, changing from one dominated by two species, a folivore (red colobus) and a frugivorous omnivore (redtails), to one dominated by three species of frugivorous omnivores (redtails, mangabeys, and chimpanzees). This study demonstrates the importance of long-term monitoring in understanding population dynamics and the role of intrinsic variables in shaping the species composition of a community.     

Species,age and sex differences in type and frequencies of injuries and impairments among four arboreal primate species in Kibale National Park,Uganda

Animals in the wild often have physical impairments that can affect their fitness. The aim of this study was to compare injuries and impairments of four different primate species (black-and-white colobus, red colobus, red-tailed monkeys, and grey-cheeked mangabeys) living in Kibale National Park (Uganda), and estimate the proportion of injured and impaired individuals among the sexes and age classes. The species differed in the proportion of individuals with injuries and impairments, with 16.7% in black-and-white colobus, 23.1% in red colobus, 16.2% in red-tailed monkey and 30.2% in grey-cheeked mangabeys. Species also differed in the types and location on the body of injuries. Adult animals had more injuries than immatures. Males had more injuries than females, in all but red-tailed monkeys. The results are discussed in relation to the literature on aggressive behavior, locomotion, and predation in these species.     

Killing of a pearl-spotted owlet (Glaucidium perlatum) by male red colobus monkeys (Procolobus tephrosceles) in a forest fragment near Kibale National Park, Uganda

Adult male red colobus (Procolobus tephrosceles) were observed capturing and killing an owl (Glaucidium perlatum) in the Rurama forest fragment near Kibale National Park in western Uganda. The owl was not subsequently eaten by the colobus, their conspecifics, or the other primates present during the attack. Because the incident was preceded by an agonistic encounter with a raptor, the event is best interpreted as a misdirected antipredator behavior. Although antipredator behaviors are not unknown in red colobus, this is the first such incident directed against a raptor to be documented.     

Predator-induced neophobia in juvenile cichlids

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.     

EVOLUTION OF AVIAN COOPERATIVE BREEDING: COMPARATIVE TESTS OF THE NEST PREDATION HYPOTHESIS

Comparative analyses carried out on two different phylogenies of cooperatively and noncooperatively breeding Australian passerine birds (parvorder Corvida) were unable to detect a significant difference in nest predation rates after controlling for body mass and risk of predation due to location of the nest (nest safety). Nest predation rates, however, decrease as nest safety and body mass increase. We suggest that cooperative breeding does not bring about a current net change in rates of nest predation among Australian passerines. Species breeding cooperatively may have developed antipredator strategies that produce results similar to those adopted by noncooperatively breeding species. The function of cooperative breeding may lie outside of antipredator strategies.     

Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus)

Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners.     

Group Size Dynamics over 15+ Years in an African Forest Primate Community

Group size affects many aspects of the ecology and social organization of animals. We investigated group size stability for five primate species in Kibale National Park, Uganda from 1996 to 2011 at three nested spatial scales. Survey data indicated that group sizes did not change for most species, with the exception of red colobus monkeys (Procolobus rufomitratus), in which group size increased at all spatial scales. Mangabey (Lophocebus albigena) group size increased in old‐growth forest, but the sample size and increase were small. To augment this survey data, we collected several years of demographic data on three habituated groups of redtail monkeys (Cercopithecus ascanius), eight groups of black‐and‐white colobus (Colobus guereza), and one red colobus group. The red colobus group increased from 59 to 104 individuals, while redtail monkey and black‐and‐white colobus group sizes were stable, mirroring our survey results. To understand mechanisms behind group size changes in red colobus versus stability in other primates, we monitored forest dynamics at two spatial scales between 1990 and 2013, considered changes in predator population, and explored evidence of disease dynamics. The cumulative size of all trees and red colobus food trees increased over 24 yr, suggesting that changing food availability was driving group size changes for red colobus, while predation and disease played lesser roles. Overall, our results and evidence of changing primate densities suggest that the Kibale primate community is in a non‐equilibrium state. We suggest future conservation and management efforts take this into consideration.     

Anthropogenic influences on primate antipredator behavior and implications for research and conservation

Predation risk affects prey species' behavior, even in the absence of a direct threat, but human-induced environmental change may disturb ecologically significant predator–prey interactions. Here, we propose various ways in which knowledge of antipredator tactics, behavioral risk effects, and primate–predator interactions could assist in identifying human-caused disruption to natural systems. Using behavior to evaluate primate responses to the ongoing environmental change should be a potentially effective way to make species conservation more predictive by identifying issues before a more dramatic population declines. A key challenge here is that studies of predation on primates often use data collected via direct observations of habituated animals and human presence can deter carnivores and influence subjects' perception of risk. Hence, we also review various indirect data collection methods to evaluate their effectiveness in identifying where environmental change threatens wild species, while also minimizing observer bias.     

Thirty Years of Research in Kibale National Park,Uganda, Reveals a Complex Picture for Conservation

Kibale National Park, Uganda, has a rich and abundant primate community and a complicated history of anthropogenic disturbance. Moreover, it has been the focus of over 30 yr of research and has received considerable attention from nongovernmental and governmental conservation organizations. As a result, Kibale serves as a valuable case study with which to evaluate the factors that regulate primate population density and the challenges of deriving generalizations for conservation. We review the impact of logging and forest fragmentation on primate population density and trace the efficacy of various conservation strategies. A 28-yr comparison of primate abundance in logged and unlogged forests and a 10-yr study of forest dynamics showed that primate recovery in logged areas is generally slow or not occurring at all for some species, which is likely driven by the fact that the forest is not recovering as expected. No primate species characteristic predicted their ability to live in forest fragments around Kibale. While a nutritional model was useful to predict the abundance of colobus in forest fragments outside of Kibale, a 5-yr study revealed that human land-use practices are more fundamentally shaping population dynamics. We evaluate data on primate abundance in light of Milton’s protein/fiber model to predict colobine biomass. We demonstrate that while the model can predict colobus biomass in pristine habitats, the 2 colobus species respond differently to disturbance. We offer suggestions for future conservation research and consider strategies to conserve forested national parks based on experiences gained over 30 yr.     

Primate abundance along five transect lines at Ngogo, Kibale National Park, Uganda

Using the line transect methods, I studied the primate density at Ngogo, Kibale National Park, Uganda for 18 months. Comparisons with other studies show that the population of red colobus monkeys (Procolobus rufomitratus) and blue monkeys (Cercopithecus mitis) is declining, whereas the populations of black-and-white colobus (Colobus guereza), red-tailed monkeys (Cercopithecus ascanius), grey-cheeked mangabeys (Lophocebus albigena), baboons (Papio anubis), and chimpanzees (Pan troglodytes) remain constant or slightly increase. In this paper, I compare data on density from this study to data from previous and recent censuses at Ngogo and with data from other sites in the Kibale forest to examine the stability of primate populations. Furthermore, I test the hypothesis that the changes in red colobus and blue monkey density are due to changes in the forest structure and abundance of their most selected feeding trees, and show that changes in forest composition cannot account for changes in their red colobus abundance, but that hunting by chimpanzees provides a reasonable explanation.     

Referential calls signal predator behavior in a group-living bird species

Predation is a powerful agent of natural selection, driving the evolution of antipredator calls [1]. These calls have been shown to communicate predator category [2-4] and/or predator distance to conspecifics [5-7]. However, the risk posed by predators depends also on predator behavior [8], and the ability of prey to communicate predator behavior to conspecifics would be a selective advantage reducing their predation risk. I tested this idea in Siberian jays (Perisoreus infaustus), a group-living bird species. Predation by hawks, and to a lesser extent by owls, is substantial and the sole cause of mortality in adult jays [9]. By using field data and predator-exposure experiments, I show here that jays used antipredator calls for hawks depending on predator behavior. A playback experiment demonstrated that these prey-to-prey calls were specific to hawk behavior (perch, prey search, attack) and elicited distinct, situation-specific escape responses. This is the first study to demonstrate that prey signals convey information about predator behavior to conspecifics. Given that antipredator calls in jays aim at protecting kin group members [10, 11], consequently lowering their mortality [9], kin-selected benefits could be an important factor for the evolution of predator-behavior-specific antipredator calls in such systems.     

Animal behaviour and algal camouflage jointly structure predation and selection

Trait variation can structure interactions between individuals, thus shaping selection. Although antipredator strategies are an important component of many aquatic systems, how multiple antipredator traits interact to influence consumption and selection remains contentious. Here, I use a common larval dragonfly (Epitheca canis) and its predator (Anax junius) to test for the joint effects of activity rate and algal camouflage on predation and survival selection. I found that active and poorly camouflaged Epitheca were more likely to be consumed, and thus, survival selection favoured inactive and well‐camouflaged individuals. Notably, camouflage dampened selection on activity rate, likely by reducing attack rates when Epitheca encountered a predator. Correlational selection is therefore conferred by the ecological interaction of traits, rather than by opposing selection acting on linked traits. I suggest that antipredator traits with different adaptive functions can jointly structure patterns of consumption and selection.     

Persistence of antipredator behavior in an island population of California quail

Island populations may provide unique insights into the evolution and persistence of antipredator behavior. If antipredator behavior is costly and islands have reduced predation risk, then we expect the reduction or loss of antipredator behavior on islands. However, if even a single predator remains, the multipredator hypothesis predicts that antipredator behaviors will be conserved. We compared the flight initiation distances (FID) of California quail (Callipepla californica) on Santa Catalina Island (a location with reduced predation pressure) with quail on the mainland. We found no differences in FID between mainland and island quail. However, despite employing consistent testing methods, the starting distance from which quail were approached was significantly reduced for quail studied on the island when compared with quail studied on the mainland. Our results are consistent with the multipredator hypothesis because, while the island population had substantially fewer predators, some predators remained and some antipredator behavior persisted.     

The role of innate and environmental influences in shaping antipredator behavior of mainland and insular gartersnakes (Thamnophis sirtalis)

Vertebrates inhabiting islands are often characterized by fearlessness and tame behavior. While this relaxation of antipredator behavior has been documented in many species endemic to islands, fewer researchers have examined it in species that occur both in insular and mainland habitats. In addition, the mechanisms underlying this shift in behavior are still poorly known. For this work, antipredator behavior of island and mainland populations of the common gartersnake (Thamnophis sirtalis) was surveyed. Observed differences were explained in terms of innate tendencies and/or environmental influences using both neonates and adults in laboratory experiments designed to tease apart these two underlying mechanisms. While antipredator behavior of adults was positively correlated with the predation pressures associated with capture sites, neonate behavior did not fully reflect this pattern. However, some support for hard-wired antipredator behavior at birth was evident. Plasticity experiments also revealed that environmental factors appear to influence antipredator behavior. Thus, the data presented here suggest that predation pressures play a strong role in shaping the antipredator behavior of island animals and that the resulting behaviors are most likely the result of some combination of both nature and nurture.     

Demographic influences on the hunting behavior of chimpanzees

We investigated hunting in an unusually large community of wild chimpanzees at Ngogo in the Kibale National Park, Uganda. Aspects of predation were recorded with respect to the prey, the predators, and hunting episodes. During 23 months of observation, the Ngogo chimpanzees caught 128 prey items from four primate and three ungulate species. Chimpanzees preyed selectively on immature red colobus primarily during group hunts, with adult males making the majority of kills. Party size and composition were significant predictors of the probability that chimpanzees would hunt and of their success during attempts. Chimpanzees were more likely to hunt red colobus if party size and the number of male hunters were large; party size and the number of male hunters were also significantly larger in successful compared with unsuccessful hunts. The Ngogo chimpanzees did not appear to hunt cooperatively, but reciprocal meat-sharing typically took place after kills. Hunts occurred throughout the year, though there was some seasonality as displayed by periodic hunting binges. The extremely high success rate and large number of kills made per successful hunt are the two most striking aspects of predation by the Ngogo chimpanzees. We compare currently available observations of chimpanzee hunting behavior across study sites and conclude that the large size of the Ngogo community contributes to their extraordinary hunting success. Demographic differences between groups are likely to contribute to other patterns of interpopulation variation in chimpanzee predation. Am J Phys Anthropol 109:439–454, 1999. © 1999 Wiley-Liss, Inc.     

Ontogenetic Shift in Efficacy of Antipredator Mechanisms in a Top Aquatic Predator,Anax junius (Odonata: Aeshnidae)

The ability of prey to escape predation often lies in the occurrence and efficacy of their predator avoidance and antipredator behaviors, which are often coupled with specialized morphology. How the use and efficacy of these behaviors change throughout ontogeny may be indicative of the vulnerability and ecological roles these animals experience throughout their lives. We examined the antipredator behavior of a large dragonfly nymph, Anax junius, from a historically fishless pond where these animals have traditionally been classified as top predators. These dragonfly nymphs displayed a series of distinct aggressive antipredator behaviors when grasped that involved stabbing with lateral and posterior spines and seizing with labial hooks. Larger (older) nymphs displayed these aggressive behaviors significantly more than smaller (younger) animals in simulated predation trials. During encounters with live larval salamander predators (Ambystoma tigrinum), all large nymphs, but only 12.5% of small nymphs successfully escaped predation attempts by the amphibians through the use of antipredator behavior. Large nymphs were also significantly more active than smaller nymphs in the presence of salamander larvae. Despite often being considered top predators in fishless ponds, our study demonstrates that their true role is more complex, depending on ontogeny and body size, and that effective antipredator behavior is likely necessary for survival in these systems.     

Foraging behavior of three Tasmanian macropodid marsupials in response to present and historical predation threat

It is often essential to understand historical selection regimes to explain current traits. We studied antipredator behavior of three Tasmanian macropodid marsupials – Forester kangaroos Macropus giganteus , Bennett's wallabies M. rufogriseus , and Tasmanian pademelons Thylogale billardierii – to understand how antipredator behavior functions in a relatively intact predator community. We also compared behavior of the kangaroos and wallabies on a predator-free island where they were translocated from mainland Tasmania 30 yr ago. Both species allowed humans to get closer to them on the predator-free island; a finding consistent with a reduced risk of predation on the island. Neither kangaroos, nor wallabies, exhibited group size effects – they did not modify time allocated to foraging or antipredator vigilance as a function of group size at either site. Nor did overall time allocation vary in any consistent way. In contrast, mainland Australian sibling-species of Forester kangaroos and Bennett's wallabies have both been reported to have group size effects. It is possible either that the extinction of the thylacine Thylacinus cynocephalus in the last century has led to an evolutionary loss of group size effects and other antipredator behavior, or that thylacines were never that important a predator on Tasmanian subspecies. In contrast, Tasmanian pademelons studied on the Tasmanian mainland modified time allocation as a function of group size suggesting that they perceived safety in numbers. Pademelons, because of their body size, are relatively more vulnerable than larger-bodied macropodids to the rich community of marsupial carnivores in Tasmania, and used a mix of social and individual strategies to manage predation risk.     

Habitat alteration,hunting and the conservation of folivorous primates in African forests

Abstract The colobus monkeys and gorillas of African forests share a strong tendency to depend on foliage during lean seasons. In many areas, both kinds of primate are threatened by habitat destruction. But while the total removal of natural habitat is clearly a major threat to the survival of many African forest primates, an analysis of survey data suggests that human predation tends to have a greater negative impact on primate populations than does selective logging or low-intensity bush-fallow agriculture. In the absence of hunting, the population density of colobus monkeys correlates with the protein: fibre ratio of mature tree foliage in their habitat, and the density of gorillas appears to be correlated with the abundance of terrestrial herbaceous vegetation. Because moderately disturbed forest can be relatively rich in high-quality lean-season folivore foods, such forest sometimes supports a higher density of folivorous primates than forest that has not been recently disturbed but that has been subject to hunting. Conservation plans for African forests should place more emphasis on the control of hunting and less on rural development, and long-range plans should also allow for the strong possibility of political instability.