Apes in a changing world – the effects of global warming on the behaviour and distribution of African apes

Aim In this study we use a modelling approach to identify: (1) the factors responsible for the differences in ape biogeography, (2) the effects that global warming might have on distribution patterns of African apes, (3) the underlying mechanisms for these effects, and (4) the implications that behavioural flexibility might be expected to have for ape survival. All African apes are highly endangered, and the need for efficient conservation methods is a top priority. The expected changes in world climate are likely to further exacerbate the difficulties they face. Our study aims to further understand the mechanisms that link climatic conditions to the behaviour and biogeography of ape species. Location Africa. Method We use an existing validated time budgets model, derived from data on 20 natural populations of gorillas (Gorilla beringei and Gorilla gorilla) and chimpanzees (Pan troglodytes and Pan paniscus), which specifies the relationship between climate, group size, body weight and time available for various activities, to predict ape distribution across Africa under a uniform worst‐case climate change scenario. Results We demonstrate that a worst‐case global warming scenario is likely to alter the delicate balance between different time budget components. Our model points to the importance of annual temperature variation, which was found to have the strongest impact on ape biogeography. Our simulation indicates that rising temperatures and changes in rainfall patterns are likely to have strong effects on ape survival and distribution, particularly for gorillas. Even if they behaved with maximum flexibility, gorillas may not be able to survive in most of their present habitats if the climate was to undergo extreme changes. The survival of chimpanzees was found to be strongly dependent on the minimum viable group size required. Main conclusions Our model allows us to explore how climatic conditions, individual behaviour and morphological traits may interact to limit the biogeographical distributions of these species, thereby allowing us to predict the effects of climate change on African ape distributions under different climate change regimes. The model suggests that climate variability (i.e. seasonality) plays a more important role than the absolute magnitude of the change, but these data are not normally provided by climate models.     

Evidence of leopard predation on bonobos (Pan paniscus)

Current models of social organization assume that predation is one of the major forces that promotes group living in diurnal primates. As large body size renders some protection against predators, gregariousness of great apes and other large primate species is usually related to other parameters. The low frequency of observed cases of nonhuman predation on great apes seems to support this assumption. However, recent efforts to study potential predator species have increasingly accumulated direct and indirect evidence of predation by leopards (Panthera pardus) on chimpanzees and gorillas. The following report provides the first evidence of predation by a leopard on bonobos (Pan paniscus).     

Body mass variations in disturbed mallards Anas platyrhynchos fit to the mass‐dependent starvation‐predation risk trade‐off

For passerines the starvation‐predation risk theory predicts that birds should decrease their body mass to improve escape flight performance, when predation pressure increases. To investigate whether this theory may apply to large birds, which manage body reserves differently from small passerines, we experimentally increased the predation risk in mallards Anas platyrhynchos. Two groups were disturbed at different frequencies during experimental sessions lasting one week, while a control group was left undisturbed. We found that body mass loss and final wing loading were similar in both disturbed groups and significantly differed from the control group. Food intake in disturbed groups was reduced up to day four of the disturbance session and was lower than in the control group. Altogether our results suggest that disturbed mallards may adjust their body mass to reach a more favorable wing loading, supposedly to improve escape flight performance. Nevertheless, body mass loss in our mallards was double than what has been observed in passerines. This greater mass decrease might be explained by different strategies concerning energy storage. Furthermore, in large birds the predation component of the starvation‐predation trade‐off might be of greater importance. Hence, the observed relevance of this trade‐off over a large size range suggests that the starvation‐predation risk theory is of major ecological significance for many animal species.     

Ontogeny of body size variation in African apes

Size variation in African apes (Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) is substantial, both within and between species. We investigate the possible evolutionary significance of this variation through an analysis of the ontogeny of size variation in this group. In addition, we highlight possible areas of future endocrinological research, and evaluate recently proposed alternative models that attempt to account for ontogenetic variation in apes. The present study shows that intergeneric variation in size is largely a consequence of differences among species in the rate of body weight growth. Interspecific size variation in Pan is a product of both rate and duration differences in growth. The ontogenetic bases of sexual dimorphism vary in this group. Dimorphism is largely a result of sex differences in the duration of body weight growth in gorillas and pygmy chimpanzees, but results from differences in the rate of growth in common chimpanzees. Ontogenetic analyses largely confirm earlier interpretations, but with better data and methods. The great degree of ontogenetic variation within and among these species, especially in the timing and magnitude of “pubertal” growth spurts, implies that studies of endocrine growth control in African apes could be a productive line of future research. We also suggest that ontogenetic variation can be understood with respect to ecological risks. Growth rates seem to be negatively correlated with ecological risk in African apes, suggesting links between ontogenetic patterns and social and ecological variables. High growth rates in gorillas compared to Pan are most consistent with this model. Variation between chimpanzees and pygmy chimpanzees (especially females) also seem to fit predictions of this model. © 1996 Wiley-Liss, Inc.     

Coexistence in a sea urchin guild and its implications to coral reef diversity and degradation

Summary Coexistence between the coral reef inhabiting sea urchins Echinometra mathaei, Diadema savignyi and D. setosum was studied by comparing differences in body morphology, distribution, diet, susceptibility to predators, intra- and interspecific competition and settlement. The three species share similar diets and broad within-habitat distributions but differ in their microspatial preferences. E. mathaei is the smallest species, has the highest settlement rates and lives territorially within small burrows or crevices. D. savignyi is intermediate in size and lives frequently in intermediate size crevices or occassionally in social groups. D. setosum is the largest species and occassionally lives in large crevices or more frequently in social groups. Both Diadema have similarily low settlement rates. Competition experiments showed that E. mathaei was consistently the top competitor for crevice space. Diadema species shared larger crevices but competition occured within smaller crevices and was frequently won by the largest individual, regardless of species. D. savignyi may be the top competitor for crevice space between the Diadema species due to a reduced spine length/test size ratio which gives it a larger test for the same crevice size requirement. Predation rates were high for E. mathaei and low for both Diadema species. Coexistence is mediated by predation on the competitive-dominant while predation coupled with different body morphologies and behavior allows spatial resource partitioning of the reef's variable topography. Consequently, the three variables of predation, topographic complexity and differing body shapes create the observed species diversity. A reduction in predators due to stochastic fluctuations or from fishing pressure can lead to E. mathaei population increases and competitive exclusion of Diadema.     

Sexual segregation in western grey kangaroos: testing alternative evolutionary hypotheses

In sexually dimorphic ungulates, sexual segregation is hypothesized to have evolved because of sex-specific differences in body size and/or reproductive strategies. We tested these alternative hypotheses in kangaroos, which are ecological analogues of ungulates. Kangaroos exhibit a wide range of body sizes, particularly among mature males, and so the effects of body size and sex can be distinguished. We tested predictions derived from these hypotheses by comparing the distribution of three sex–sex size classes of western grey kangaroos Macropus fuliginosus , in different habitats, and the composition of groups of kangaroos, across seasons. In accordance with the predation risk-reproductive strategy hypothesis, during the non-breeding season, females, which were more susceptible to predation than larger males, and were accompanied by vulnerable young-at-foot, were over-represented in secure habitats. Large males, which were essentially immune to predation, occurred more often than expected in nutrient-rich habitat, and small males, which faced competing demands of predator avoidance and feeding, were intermediate between females and large males in their distribution across habitats. During the breeding season, females continued to be over-represented in secure habitats when their newly emerged pouch young were most vulnerable to predation. All males occupied these same habitats to maximize their chances of securing mates. Consistent with the social hypotheses, groups composed of individuals of the same sex, irrespective of body size, were over-represented in the population during the non-breeding season, while during the breeding season all males sought females so that mixed-sex groups predominated. These results indicate that body size and reproductive strategies are both important, yet independent, factors influencing segregation in western grey kangaroos.     

Ontogeny and the evolution of adult body size dimorphism in apes

This analysis investigates the ontogeny of body size dimorphism in apes. The processes that lead to adult body size dimorphism are illustrated and described. Potential covariation between ontogenetic processes and socioecological variables is evaluated. Mixed-longitudinal growth data from 395 captive individuals (representing Hylobates lar [gibbon], Hylobates syndactylus [siamang], Pongo pygmaeus [orangutan], Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) form the basis of this study. Results illustrate heterogeneity in the growth processes that produce ape dimorphism. Hylobatids show no sexual differentiation in body weight growth. Adult body size dimorphism in Pongo can be largely attributed to indeterminate male growth. Dimorphism in African apes is produced by two different ontogenetic processes. Both pygmy chimpanzees (Pan paniscus) and gorillas (Gorilla gorilla) become dimorphic primarily through bimaturism (sex differences in duration of growth). In contrast, sex differences in rate of growth account for the majority of dimorphism in common chimpanzees (Pan troglodytes). Diversity in the ontogenetic pathways that produce adult body size dimorphism may be related to multiple evolutionary causes of dimorphism. The lack of sex differences in hylobatid growth is consistent with a monogamous social organization. Adult dimorphism in Pongo can be attributed to sexual selection for indeterminate male growth. Interpretation of dimorphism in African apes is complicated because factors that influence female ontogeny have a substantial effect on the resultant adult dimorphism. Sexual selection for prolonged male growth in gorillas may also increase bimaturism relative to common chimpanzees. Variation in female growth is hypothesized to covary with foraging adaptations and with differences in female competition that result from these foraging adaptations. Variation in male growth probably corresponds to variation in level of sexual selection. © 1995 Wiley-Liss, Inc.     

Body‐size distribution and biogeographical patterns in non‐marine ostracods (Crustacea: Ostracoda)

The idea that free‐living minute organisms have ubiquitous distributions has been recently revitalized, causing significant controversy. The ubiquitous model predicts that a threshold where ubiquity leaves room to biogeography might exist somewhere along the animal body‐size range. In the present study, such a prediction is tested by analysing body‐size frequency distribution, species distribution, and local‐to‐global species ratio at the scale of biogeographical realms in cypridoidean non‐marine ostracods, a group with a body‐size range in the ubiquity–biogeography (U‐B) boundary. Data were gathered for all described extant cypridoidean ostracod species (N = 1761), with body‐size recorded for 1134 of them. Although local‐to‐global species ratios show significant over‐dispersal of small‐body ostracods for the Palaearctic and the Australasian regions, there are explanations alternative to the ‘Everything is Everywhere’ model that can account for such a result. Indicators of taxonomic structure do not support the hypothesis of a random distribution of cypridoidean species among realms. Nevertheless, the strong biogeography signal occurring at a large scale vanishes at the local scale (country‐level within the Palaearctic), and suggests wide dispersion within biogeographical realms. Additional factors, including inconsistent taxonomic criteria for species recognition, uneven sampling effort, and an excess of ‘single‐report’ occurrences, have been identified too as potential distorters of the observed patterns. Taxonomic harmonization, open databases of biogeographical data, and better ecological information are suggested as critical goals that need to be achieved for further understanding of ostracod global distribution patterns. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 409–423.     

A comparative analysis of vigilance in birds

Individual variation in vigilance is known to vary with factors such as group size but the ecological determinants of vigilance among species have not been examined thus far in a systematic fashion. Earlier analyses suggested that vigilance should be lower in larger species and in species living in larger groups. These analyses were based on a small number of species and failed to take into account phylogenetic relationships among species. Here, I examined ecological determinants of vigilance in a large sample of bird species using a phylogenetic framework. I focused on vigilance in foraging groups of birds in the non-breeding season. Among species, vigilance by solitary foragers was not influenced by body mass. However, among species, asymptotic vigilance, the plateau reached by vigilance in larger groups, decreased with increasing group size in vegetarian clades but not in carnivorous clades. Asymptotic vigilance also increased with increasing body mass in vegetarian clades but not in carnivorous clades. Increasing group size may allow species to reduce vigilance in response to decreased predation risk. Increasing body mass may allow species to increase vigilance because more non-foraging time is available in larger species. Diet may modulate the effect of body mass and group size through factors such as within-group vigilance or foraging techniques.     

Does relaxed predation drive phenotypic divergence among insular populations?

The evolution of striking phenotypes on islands is a well‐known phenomenon, and there has been a long‐standing debate on the patterns of body size evolution on islands. The ecological causes driving divergence in insular populations are, however, poorly understood. Reduced predator fauna is expected to lower escape propensity, increase body size and relax selection for crypsis in small‐bodied, insular prey species. Here, we investigated whether escape behaviour, body size and dorsal coloration have diverged as predicted under predation release in spatially replicated islet and mainland populations of the lizard species Podarcis gaigeae. We show that islet lizards escape approaching observers at shorter distances and are larger than mainland lizards. Additionally, we found evidence for larger between‐population variation in body size among the islet populations than mainland populations. Moreover, islet populations are significantly more divergent in dorsal coloration and match their respective habitats poorer than mainland lizards. These results strongly suggest that predation release on islets has driven population divergence in phenotypic and behavioural traits and that selective release has affected both trait means and variances. Relaxed predation pressure is therefore likely to be one of the major ecological factors driving body size divergence on these islands.     

Relative growth of the limbs and trunk in the African apes

Examination of relative growth and allometry is important for our understanding of the African apes, as they represent a closely related group of species of increasing body size. This study presents a comparison of ontogenetic relative growth patterns of some postcranial dimensions in Pan paniscus, Pantroglodytes, and Gorilla gorilla. Interspecific proportion differences among the three species are also analyzed. It is stressed that reliable ontogenetic information can only be obtained if subadults are examined-growth data cannot be inferred from static adult scaling. Results indicate that some postcranial relative growth patterns are very similar in the three species, suggesting differential extrapolation of a common growth pattern, whereas for other proportion comparisons the growth trends differ markedly among the species, producing distinct shape differences in the adults Interspecific shape changes among the three species are characterized by positive allometry of chest girth and negative allometry of body height and leg length. It is suggested that relative decrease of leg length with increasing body size among the African pongids might be expected on biomechanical grounds, in order to maintain similar locomotor abilities of climbing arborealism and quadrupedal terrestrialism. Relative to body weight or trunk length, the limbs of the bonobo (Pan paniscus) are longer than in the common chimpanzee or the gorilla, with a lower intermembral index. This may most closely resemble the primitive condition for the African apes.     

Effect of energetic constraints on distribution and winter survival of weasel males

1. The absolute energy needs of small animals are generally lower than those of larger animals. This should drive higher mortality of larger animals, when the environmental conditions deteriorate. However, demonstration of the effect of energy constraints on survivals proved difficult, because the range of body mass within species is generally too small to produce enough variation for studying such an effect. An opportunity for an intraspecific study comes from weasels inhabiting the Bia?owie?a Forest (north-eastern Poland), which are characterized by a threefold variation in body mass. 2. We assumed that in summer larger weasel males are favoured by sexual selection, because they are more successful when competing for mates. We then tested whether they suffer higher mortality in winter, because they have difficulty finding sufficient food to satisfy their energy needs and/or because the additional foraging time would result in increased exposure to predation. 3. We measured daily energy expenditures (DEE) of overwintering weasel males using the doubly labelled water (DLW) technique. We constructed an energetic model predicting how individuals of different size are able to balance their energy budgets feeding on large and small prey while minimizing time spent hunting, thereby reducing their own exposure to predation. 4. The range of body mass in overwintering weasels predicted by our model corresponded very well with the distribution of prey body mass in three different habitats within our study area. Larger individuals were able to compensate for higher food requirements by using habitats with larger prey species than those available to smaller male weasels. This effectively offset the expected negative association between body mass and winter survival predicted from considerations of energy balance. 5. Our results show how energetic constraints affect body mass and spatial segregation of a species at the intra-specific level not only across large geographical ranges, but also within a relatively small area.     

Gorilla ecology and behavior

Many factors influence the evolution of primate grouping patterns, including phylogeny, demographic and life-history variables, and ecological factors such as access to food, predation pressure, and avoidance of infanticide. The interaction between these factors determines social organization.¹ Because western lowland and mountain gorillas differ so dramatically in their habitats and foraging strategies, they provide a valuable opportunity to assess how changes in ecology influence this balance. Mountain gorillas live in high-altitude montane forests, are herbivorous, and live in stable and cohesive groups. Western lowland gorillas live in lowland rainforest and are much more frugivorous than mountain gorillas. It is not yet clear to what extent incorporating significant quantities of fruit in the diet influences western lowland gorilla sociality because they have been studied much less than have mountain gorillas. However, what is known about their behavior hints that there may also be considerable differences in their social organization, including changes in group size and cohesion and in the frequency and type of intergroup encounters. Gorillas thus provide a unique opportunity to reevaluate proposed models of ecological influences on social organization in African apes.© 1998 Wiley-Liss, Inc.     

Did knuckle walking evolve twice?

Although African great apes share a similar quadrupedal locomotor behaviour, there are marked differences in hand morphology and size between the species. Hence, whilst all three species (two genera) of African ape frequently knuckle walk as adults, debate remains as to whether this behaviour is derived from a common ancestor or whether it evolved in parallel in chimpanzees and gorillas. This exploratory morphometric study of the sub-adult and adult wrist of these two genera aims to contribute to this debate. A total of twenty-seven dimensions of the lunate, triquetral, hamate and capitate of sub-adult and adult Pan troglodytes and Gorilla gorilla were analysed in order to determine whether carpal dimensions are generally ontogenetically scaled, and whether differences in growth trajectories, or length of growth, and adult morphologies can be explained by behavioural differences between the two species. Only 56% of all dimensions studied were ontogenetically scaled in sub-adults and some of these dimensions exhibit differing adult proportions between the two species. In general, the dimensions analysed fell into two categories: Pan and Gorilla either follow the same growth trajectories (Pattern A) or the Pan reduced major axis (RMA) regressions were significantly transposed above those of Gorilla (Pattern B). Additionally, it was found that Gorilla carpals appear to cease growing relatively earlier than those of Pan. While a small number of differences, notably those of the lunate, can be accounted for by differences in behaviour between the species, the majority of differences indicate heterochronic modifications of development during evolution, which correspond to kinematic differences in knuckle walking between the African great apes. In light of morphological, behavioural and ecological data currently available it is parsimonious to suggest that knuckle walking has evolved in parallel in the two lineages.     

Look in the trees: Hylobatids as evolutionary models for extinct hominins

Studying extant apes is of central importance to paleoanthropology. This approach is informative in inferring how hominin skeletal morphology reflects phylogeny, behavior, development, and ecological context. Traditionally, great apes have dominated the paleoanthropological literature as extant analogs for extinct hominins, to the exclusion of their phylogenetic sister group, the hylobatids. Phylogenetic proximity, large body size, and high encephalization quotients may have contributed to decisions to use great apes as models for hominins. However, if we reexamine hylobatids as extant models for extinct hominins—using modern phylogenetic, behavioral, and ecological data—this clade is uniquely poised to inform future frameworks in paleoanthropology. The following features make hylobatids strong analogs for extinct hominins: taxonomic diversity, the timing of diversification, hybridization between species, small body size, and reduced sexual dimorphism. Based on these shared features, hylobatids offer future opportunities to paleoanthropology, and provide a much richer extant analog than is currently recognized.     

Some evidence for different ecological pressures that constrain male and female body size

The dwarf morph of the Lake Tanganyika cichlid Telmatochromis temporalis uses empty snail shells as shelters and breeding sites in shell beds, in which many empty shells exist. Here, we assessed selection forces regulating body size in this fish. Field observations showed that large males tended to have a greater number of females in their territories, suggesting that sexual selection favours large males. Nonetheless, a transplant experiment suggested that male body size was limited by the ability to hide in empty shells from large piscivorous fish. In females, the number of ovarian eggs increased with body size, suggesting that fecundity selection favours large females. However, females are smaller than males. Females spawned eggs close to the apices inside the shells. The small space there would decrease the risk of egg predation by egg predators, and small body size of females may be a result of adaptation to spawn eggs in the small, safe spaces. This study provides support for the idea that male and female body sizes have been limited by different ecological pressures (predation on adult fish in males, predation on eggs in females), which has not been reported previously in any animal.     

Explaining adaptive shifts in body size on islands: a life history approach

The tendency for island populations to differ in body size from their mainland relatives has been well documented, but the mechanisms for these size changes remain speculative. Explanations have typically been based on ecological interactions that directly favor either an increase or decrease in body size. While it is clear that direct ecological interactions can influence body size, life history shifts present an alternative explanation for observed insular size trends across phylogenetic groups and trophic levels. Here I describe how decreased resource availability and reduced predation pressure, the same selective forces invoked by previous hypotheses, can operate to produce body size changes via the evolution of life history traits. This mechanism is more generally applicable than previous explanations and is consistent with much of the available data.     

Body size and the division of niche space: food and predation differentially shape the distribution of Serengeti grazers

1. Theory predicts that small grazers are regulated by the digestive quality of grass, while large grazers extract sufficient nutrients from low-quality forage and are regulated by its abundance instead. In addition, predation potentially affects populations of small grazers more than large grazers, because predators have difficulty capturing and handling large prey. 2. We analyse the spatial distribution of five grazer species of different body size in relation to gradients of food availability and predation risk. Specifically, we investigate how the quality of grass, the abundance of grass biomass and the associated risks of predation affect the habitat use of small, intermediate and large savanna grazers at a landscape level. 3. Resource selection functions of five mammalian grazer species surveyed over a 21-year period in Serengeti are calculated using logistic regressions. Variables included in the analyses are grass nitrogen, rainfall, topographic wetness index, woody cover, drainage lines, landscape curvature, water and human habitation. Structural equation modelling (SEM) is used to aggregate predictor variables into 'composites' representing food quality, food abundance and predation risk. Subsequently, SEM is used to investigate species' habitat use, defined as their recurrence in 5 × 5 km cells across repeated censuses. 4. The distribution of small grazers is constrained by predation and food quality, whereas the distribution of large grazers is relatively unconstrained. The distribution of the largest grazer (African buffalo) is primarily associated with forage abundance but not predation risk, while the distributions of the smallest grazers (Thomson's gazelle and Grant's gazelle) are associated with high grass quality and negatively with the risk of predation. The distributions of intermediate sized grazers (Coke's hartebeest and topi) suggest they optimize access to grass biomass of sufficient quality in relatively predator-safe areas. 5. The results illustrate how top-down (vegetation-mediated predation risk) and bottom-up factors (biomass and nutrient content of vegetation) predictably contribute to the division of niche space for herbivores that vary in body size. Furthermore, diverse grazing assemblages are composed of herbivores of many body sizes (rather than similar body sizes), because these herbivores best exploit the resources of different habitat types.     

Sex- and concentration-dependent effects of predator feces on seasonal regulation of body mass in the bank vole Clethrionomys glareolus

Increased perception of predation risk can cause changes in activity, feeding and reproductive behavior in a wide range of taxa. Many small mammals in the temperate zone exhibit fluctuations in body mass in response to changing photoperiod. Bank voles lose body mass in winter which they regain when photoperiod increases in the spring. To determine if predation risk affects seasonal changes in body mass (BM), bank voles were exposed to two concentrations (low: LC and high: HC) of weasel feces. Food intake (FI) and daily energy expenditure (DEE) were measured to establish if differences in body mass were due to adjustment in energy intake or expenditure. Fecal corticosterone (CORT) was measured to assess whether the voles had detected and responded to predator feces as a physiological stressor. Voles of both sexes had higher levels of fecal CORT in the groups exposed to weasel feces compared to controls. Voles responded to the predator feces in a sex- and concentration-dependent manner. Males responded to LC feces by gaining less mass following the change in photoperiod. This was mediated by reduced FI and higher DEE. Female voles also gained less BM in response to HC feces, but increased both FI and DEE. We hypothesize that males may gain a short-term advantage by lowering BM in response to predation risk, which may be regained without affecting reproductive success. The consequences of mass loss in females may be more significant as this may delay the onset of breeding or reduce the size or number of young, thereby negatively affecting breeding success.