Quantification of invertebrate predation and herbivory in food chains of low complexity

Zooplankton grazing impact on algae, heterotrophic flagellates and bacteria, as well as invertebrate predation on herbivorous zooplankton, were investigated in two sub-Antarctic lakes with extremely simple food chains. The two species of herbivorous zooplankton present in the lakes (the copepods boeckella michaelseni and Pseudoboeckella poppei) exerted substantial grazing pressure on algae. However, the dominant algal species exhibited properties that enabled them to avoid (large size or extruding spines, e.g. Staurastrum sp., Tribonema sp.) or compensate (recruitment from the sediment, Mallomonas sp.) grazing. There are only two potential invertebrate predators on the herbivorous copepods in the two lakes: the copepod Parabroteas sarsi and the diving beetle Lancetes claussi. Vertebrate predators are entirely abscent from sub-Antarctic lakes. Based on our experiments, we estimated that the predators would remove at most about 0.4% of the herbivorous copepods per day, whereas planktivorous fish, if present in the lakes, would have removed 5–17% of the zooplankton each day. Consequently, the invertebrate predators in these high-latitude lakes had only a marginal predation impact compared to the predation pressure on zooplankton in the presence of vertebrate predators in temperate lakes. The study of these simple systems with only two quantitatively functionally important trophic links, suggests that high grazing pressure foreces the algal community towards forms with grazer resistant adaptations such as large size, recruitment from another habitat, and grazer avoidance spines. We propose that due to such adaptations, predictions from food web theory are only partly corroborated, i.e. algal biomass actually increases with increasing productivity, although the grazer community is released from predation. In more species-rich and complex systems, e.g temperate lakes with three functionally important links, such adaptations are likely to be even more important, and, consequently, the observable effects of trophic interactions from top predators on lower trophic levels even more obscured.     

Can the Patterns of Sexual Swelling Cycles in Female Taï Chimpanzees be Explained by the Cost-of-Sexual-Attraction Hypothesis?

Chimpanzee females of East and West African populations differ in the average number of cycles per interbirth interval. Whereas females in Gombe, Mahale, and Kibale (eastern chimpanzees, Pan troglodytes schweinfurthii) average <9 cycles before they conceive, females at Taï (western chimpanzees; Pan troglodytes verus) average 29 cycles. We examined data from 2 different study groups (North and South) at Taï. By showing that Taï females interrupt cyclic activity for, on average, 7.4 mo between the end of the postpartum amenorrhea period (PPA) and the subsequent conception, and by calculating the number of cycles to conception based on a probability distribution of cycles over the interbirth interval, we show that Taï females average 19.4 cycles (North Group) and 11.7 cycles (South Group) to conception; therefore, the earlier calculation of 29 cycles was an overestimate. Further, at Taï young parous females have a significantly shorter PPA than those of older females, but the number of cycles to conception does not differ significantly between primiparous and nulliparous females. Some of our results are therefore not in line with the predictions of the cost-of-sexual-attraction hypothesis, which proposes that the factor ultimately responsible for the intensity of female sexual attractiveness is female intragroup scramble competition. We discuss an alternative hypothesis—the social passport hypothesis—which is compatible with the results of the study.     

Role of Nonbehavioral Factors in Adjusting Long Bone Diaphyseal Structure in Free-ranging <Emphasis Type="Italic">Pan troglodytes</Emphasis>

Limb bones deform during locomotion and can resist the deformations by adjusting their shapes. For example, a tubular-shaped diaphysis best resists variably-oriented deformations. As behavioral profiles change during adulthood, patterns of bone deformation may exhibit age trends. Habitat characteristics, e.g., annual rainfall, tree density, and elevation changes, may influence bone deformations by eliciting individual components of behavioral repertoires and suppressing others, or by influencing movements during particular components. Habituated chimpanzee communities provide a unique opportunity to examine these factors because of the availability of morphological data and behavioral observations from known-age individuals inhabiting natural habitats. We evaluated adult femora and humeri of 18 female and 10 male free-ranging chimpanzees (Pan troglodytes) from communities in Gombe (Tanzania), Mahale Mountains (Tanzania), and Taï Forest (Côte d’Ivoire) National Parks. We compare cross sections at several locations (35%, 50%, 65% diaphyseal lengths). Community comparisons highlight different diaphyseal shapes of Taï females relative to Mahale and Gombe females, particularly in humeral diaphyses. Age trends in diaphyseal shapes are consistent with reduced activity levels in general, not only reduced arboreal activity. Age-related bone loss is apparent among community females, but is less striking among males. Community trends in diaphyseal shape are qualitatively consistent with ranked annual rainfall at localities, tree density, and elevation change or ruggedness of terrain. Habitat characteristics may contribute to variation in diaphyseal shape among chimpanzee communities, much like among modern human groups, but verification awaits further rigorous experimental and comparative analyses.     

How feeding competition determines female chimpanzee gregariousness and ranging in the Taï National Park, Côte d'Ivoire

Socioecological theory suggests that feeding competition shapes female social relationships. Chimpanzees (Pan troglodytes) live in fission–fusion societies that allow them to react flexibly to increased feeding competition by forming smaller foraging parties when food is scarce. In chimpanzees at Gombe and Kibale, female dominance rank can crucially influence feeding competition and reproductive success as high‐ranking females monopolize core areas of relatively high quality, are more gregarious, and have higher body mass and reproductive success than low‐ranking females. Chimpanzee females in Taï National Park do not monopolize core areas; they use the entire territory as do the males of their community and are highly gregarious. Although female chimpanzees in Taï generally exhibit a linear dominance hierarchy benefits of high rank are currently not well understood. We used a multivariate analysis of long‐term data from two Taï chimpanzee communities to test whether high‐ranking females (1) increase gregariousness and (2) minimize their travel costs. We found that high‐ranking females were more gregarious than low‐rankers only when food was scarce. During periods of food scarcity, high rank allowed females to enjoy benefits of gregariousness, while low‐ranking females strongly decreased their gregariousness. High‐ranking females traveled more than low‐ranking females, suggesting that low‐rankers might follow a strategy to minimize energy expenditure. Our results suggest that, in contrast to other chimpanzee populations and depending on the prevailing ecological conditions, female chimpanzees at Taï respond differently to varying levels of feeding competition. Care needs to be taken before generalizing results found in any one chimpanzee population to the species level. Am. J. Primatol. 73:305–313, 2011. © 2010 Wiley‐Liss, Inc.     

Buttress drumming by wild chimpanzees: Temporal patterning, phrase integration into loud calls, and preliminary evidence for individual distinctiveness

Wild chimpanzees (Pan troglodytes) generate low-frequency sounds that are audible to humans from a distance of at least 1 km away by hitting the buttresses of trees with their hands and feet. This buttress drumming occurs in discrete bouts of rapidly delivered beats that usually accompany “pant hoots,” the species-specific long-distance vocalization. Individual differences in male chimpanzee (P.t. verus) drumming were investigated during a 6-month field study in the Taï National Park, Ivory Coast. Analysis of drumming bouts recorded from six adult males revealed significant differences between individuals in three acoustic features: (1) mean duration of inter-beat interval; (2) mean number of beats per bout; and (3) mean bout duration. Preliminary analysis indicated that individuals differ in their tendency to deliver drum beats in temporally close pairs separated by longer interbeat intervals. Qualitative examination also suggested that individuals may differ in the temporal integration of drumming into the pant hoot vocalization. These results suggest that there may be acoustic cues available for chimpanzees to recognize unseen males by their drumming performances alone. Drumming by Taï chimpanzees was also compared to drumming by chimpanzees (P.t. schweinfurthii) from the Kanyawara study group in Kibale National Park. Uganda. The Kanyawara chimpanzees appeared to drum more often without vocalizing than did the Taï chimpanzees. When they did drum and vocalize together, the Kanyawara chimpanzees appeared to integrate their drumming later into the associated pant hoots than did the Taï chimpanzees. These results suggest the possibility that interpopulation variation exists in chimpanzee buttress drumming.     

Behavioral and physiological adjustments to new predators in an endemic island species,the Galápagos marine iguana

For the past 5 to 15 million years, marine iguanas (Amblyrhynchus cristatus), endemic to the Galápagos archipelago, experienced relaxed predation pressure and consequently show negligible anti-predator behavior. However, over the past few decades introduced feral cats and dogs started to prey on iguanas on some of the islands. We investigated experimentally whether behavioral and endocrine anti-predator responses changed in response to predator introduction. We hypothesized that flight initiation distances (FID) and corticosterone (CORT) concentrations should increase in affected populations to cope with the novel predators. Populations of marine iguanas reacted differentially to simulated predator approach depending on whether or not they were previously naturally exposed to introduced predators. FIDs were larger at sites with predation than at sites without predation. Furthermore, the occurrence of new predators was associated with increased stress-induced CORT levels in marine iguanas. In addition, age was a strong predictor of variation in FID and CORT levels. Juveniles, which are generally more threatened by predators compared to adults, showed larger FIDs and higher CORT baseline levels as well as higher stress-induced levels than adults. The results demonstrate that this naive island species shows behavioral and physiological plasticity associated with actual predation pressure, a trait that is presumably adaptive. However, the adjustments in FID are not sufficient to cope with the novel predators. We suggest that low behavioral plasticity in the face of introduced predators may drive many island species to extinction.     

Morphological variation in adult chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d'Ivoire

Twenty five adult chimpanzee skeletons (Pan troglodytes verus) of known age and sex (15 females, 10 males) from a long‐term study site in Taï National Park, Cote d'Ivoire present new data on variation. These skeletons provide a rare opportunity to measure the cranium and postcranium from the same individuals. We compare measurements and indices of the Taï sample with those of relatively complete Pan troglodytes schweinfurthii skeletons from Gombe National Park, Tanzania. Measurements of Pan paniscus are included as an outside comparison. The Taï and Gombe samples are analyzed by sex; combined sex samples are compared between the two groups, and the two sexes to each other. Taï females and males do not differ in most long bone lengths or in pelvic dimensions, but do differ significantly in cranial capacity, facial measurements, clavicle length, scapular breadth, and femur length. Gombe females and males differ significantly in some facial measurements and in scapular breadth. In combined sex samples, Taï individuals have lower cranial capacity, longer palate and mandible, and greater dimensions in the trunk and limb lengths. Taï females account for most of the variation; males differ from each other only in greater length of humerus and femur. The Taï skeletons provide new data for assessing individual variation and sexual dimorphism within and between populations and species. The combination of cranial and postcranial data provides a clearer picture of chimpanzee intraspecific and interspecific variation than can be gained from either data set alone. Am J Phys Anthropol, 2008. © 2007 Wiley‐Liss, Inc.     

The Predator Deterrence Function of Primate Alarm Calls

It is generally assumed that alarm calls function in intraspecific communication, for example to warn close relatives about the presence of a predator. However, an alternative hypothesis suggests that, in some cases, signallers may also gain fitness benefits in directly communicating to the predator, for example by advertising perception and unprofitability to predators that depend on unprepared prey. In this study, we show that six monkey species in Taï forest, Ivory Coast, produce significantly more alarm calls to leopards than to chimpanzees, although both are notorious monkey predators. The conspicuously high vocalization rates to leopards had adaptive consequences for the monkeys. By following a radio-collared leopard, we found that after detection and high alarm call rates the leopard gave up its hiding location and left the group significantly faster than would be expected by chance. We discuss these data with respect to the various functional hypothesis of alarm call behaviour and conclude that the high alarm call rates to leopards are part of an anti-predator strategy in primates that may have evolved to deter predators that depend on surprise.     

Bird predation as a selective pressure on the immature stages of the cabbage butterflies, Pieris rapae and P. brassicae

The importance of bird predation as a selective pressure on the eggs, larvae and pupae of the cabbage butterflies, Pieris rapae L. and P. brassicae L. has been investigated in a rural garden and an allotment. Birds are the main predators of all stages in a well-tended garden whereas in a field the eggs and young larvae are mainly preyed upon by arthropods. The species of avian predators vary according to the stage of development and species of prey. Consequently the relative survival rate of P. rupae and P. brussicue varies with stage of development. This changing pattern of survival has in turn acted as a selective pressure on their two main braconid parasites. Many aspects of the size, shape, colour and behaviour of the larvae and pupae of both species of Pieris appear to be adaptations to the selective pressures exerted by bird predation.     

Predator–prey naïveté, antipredator behavior,and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non‐consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non‐native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non‐native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non‐consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non‐native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter‐related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non‐native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non‐native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.     

Leopard predation and primate evolution

Although predation is an important driving force of natural selection its effects on primate evolution are still not well understood, mainly because little is known about the hunting behaviour of the primates' various predators. Here, we present data on the hunting behaviour of the leopard (Panthera pardus), a major primate predator in the Tai; forest of Ivory Coast and elsewhere. Radio-tracking data showed that forest leopards primarily hunt for monkeys on the ground during the day. Faecal analyses confirmed that primates accounted for a large proportion of the leopards' diet and revealed in detail the predation pressure exerted on the eight different monkey and one chimpanzee species. We related the species-specific predation rates to various morphological, behavioural and demographic traits that are usually considered adaptations to predation (body size, group size, group composition, reproductive behaviour, and use of forest strata). Leopard predation was most reliably associated with density, suggesting that leopards hunt primates according to abundance. Contrary to predictions, leopard predation rates were not negatively, but positively, related to body size, group size and the number of males per group, suggesting that predation by leopards did not drive the evolution of these traits in the predicted way. We discuss these findings in light of some recent experimental data and suggest that the principal effect of leopard predation has been on primates' cognitive evolution.     

Diet,feeding behavior,and jaw architecture of Taï monkeys: Congruence and chaos in the realm of functional morphology

We review feeding and mandibular anatomy in a community of West African monkeys. We use field observations, food material property data, and skeletal specimens from the Ivory Coast's Taï Forest to explore the factors that shape mandibular architecture in colobines and cercopithecines. Despite excellent geographic control across our sample, the fit between bone form (as conventionally described) and functional activity (as we perceive it) is not spectacular. We present a thought experiment to assess how well we could reconstruct diet in the Taï monkeys if we only had skeletons and teeth to study. This exercise indicated that we would be correct about half the time. Our analyses reinforce the notion that diet is anything but a monolithic variable and that better success at relating mandibular form to food must incorporate information on ingestive and processing behavior, geometric and material properties of foods, and both material and structural data on jaws themselves.     

Behavioral and physiological adjustments to new predators in an endemic island species, the Galápagos marine iguana

For the past 5 to 15 million years, marine iguanas (Amblyrhynchus cristatus), endemic to the Galápagos archipelago, experienced relaxed predation pressure and consequently show negligible anti-predator behavior. However, over the past few decades introduced feral cats and dogs started to prey on iguanas on some of the islands. We investigated experimentally whether behavioral and endocrine anti-predator responses changed in response to predator introduction. We hypothesized that flight initiation distances (FID) and corticosterone (CORT) concentrations should increase in affected populations to cope with the novel predators. Populations of marine iguanas reacted differentially to simulated predator approach depending on whether or not they were previously naturally exposed to introduced predators. FIDs were larger at sites with predation than at sites without predation. Furthermore, the occurrence of new predators was associated with increased stress-induced CORT levels in marine iguanas. In addition, age was a strong predictor of variation in FID and CORT levels. Juveniles, which are generally more threatened by predators compared to adults, showed larger FIDs and higher CORT baseline levels as well as higher stress-induced levels than adults. The results demonstrate that this naive island species shows behavioral and physiological plasticity associated with actual predation pressure, a trait that is presumably adaptive. However, the adjustments in FID are not sufficient to cope with the novel predators. We suggest that low behavioral plasticity in the face of introduced predators may drive many island species to extinction.     

Stable nitrogen isotope analysis of dentine serial sections elucidate sex differences in weaning patterns of wild chimpanzees (Pan troglodytes)

Offspring provisioning is one of the most energetically demanding aspects of reproduction for female mammals. Variation in lactation length and weaning strategies between chimpanzees (Pan troglodytes), our closest living relative, and modern human societies have been reported. When and why these changes occurred is frequently debated. Our study used stable nitrogen isotope data of tooth root dentine from wild Western chimpanzees (Pan troglodytes verus) in Taï National Park, Côte d'Ivoire, to quantify weaning in these chimpanzees and explore if infant sex plays a role in maternal investment. We analyzed serial sections of deciduous lateral incisor root dentine from four Taï chimpanzees to establish the δ¹⁵N signal of nursing infants; we then analyzed serial sections of first permanent mandibular molar root dentine from 12 Taï chimpanzees to provide quantitative δ¹⁵N data on weaning in this population. Up to 2 years of age both sexes exhibited dentine δ¹⁵N values ≈2–3‰ higher than adult female Taï chimpanzees, consistent with a nursing signal. Thereafter a steady decrease in δ¹⁵N values consistent with the onset, and progression, of weaning, was visible. Sex differences were also evident, where male δ¹⁵N values decreased at a significantly slower rate compared to females. Confirmation of sex differences in maternal investment among Taï chimpanzees, demonstrates the viability of using isotope analysis to investigate weaning in non‐human primates. Additionally, assuming that behaviors observed in the Taï chimpanzees are illustrative of the ancestral pattern, our results provide a platform to enable the trajectory of weaning in human evolution to be further explored. Am J Phys Anthropol 153:635–642, 2014. © 2013 Wiley Periodicals, Inc.     

Handedness in wild chimpanzees

The debate over nonhuman primate precursors to human handedness is unsettled mainly due to lack of data, particularly on apes. Handedness in wild chimpanzees at the Taï National Park Côte d'Ivoire, has been monitored in four tasks. For the simple unimanual ones, reaching and grooming, adults use both hands equally (ambidextrous), while for the more complex unimanual wadge-dipping and the complex bimanual nut-cracking, adults are highly lateralized. These results support the hypothesis that lateralization increases with the complexity of the task. The lateralization is constant for years for each task but may vary in an individual with respect to different tasks. For nutcracking females are more lateralized than males. The ontogeny of handedness for nut-cracking shows many variations in the tendency to use one hand and in the side preferred, until at about 10 years of age, the individual achieves her adult handedness. No population bias toward one side exists in Taï chimpanzees. No heritability of handedness between mother and offspring was observed. Human and chimpanzees handedness are compared.     

Anti-predator adaptations in nesting Marsh Tits Parus palustris: the role of nest-site security

A proposal that nest predation is the most important selective pressure shaping nest-site use of Marsh Tits Parus palustris was checked in a long-term study (almost 500 nests) carried out in the Białowieża National Park (eastern Poland) in primeval conditions, where the birds breed in natural holes and their nests are at risk from a variety of predators. It was predicted that predation rates would depend on hole attributes, so that Marsh Tits should use the most secure holes. Predation was responsible for 70% of total nest losses. Predation risk depended on hole attributes. Nests in dead wood were predated significantly more often than those in live wood. Nests in old woodpecker holes were predated more frequently than nests in holes of other origin, and nests situated closer to the entrance were more at risk than ones further from it. The entrance size did not influence overall predation risk, but small entrance size was important in preventing access by larger predators. These differences can account for the very rare use of holes in dead wood or of woodpecker holes, the fact that they nest in holes with small entrances and relatively far from the entrance. It is concluded that the patterns of nest-site use found in this species are best explained as anti-predator adaptations, which have evolved and are maintained by the pressure of nest predators. This study also indicates the possible limits of, and constraints on, these adaptations.     

Lack of anti-predator recognition in a marine isopod under the threat of an invasive predatory crab

Biological Invasions - The prey naïveté hypothesis suggests that the failure of prey to recognize novel predators as a threat is caused by a lack of anti-predator adaptations. We tested...     

Winning the biodiversity arms race among freshwater gastropods: competition and coexistence through shell variability and predator avoidance

Explanations for the coexistence of many closely related species in inland waters continue to be generated more than 50 years after Hutchinson’s question: why are there so many kinds of animals? This review focuses on the hypothesis that high species diversity of freshwater gastropods results, in part, from predators maintaining biodiversity across a range of deep- and shallow-water habitats. Invertebrate predators, such as aquatic insects, and leeches consume soft tissue of pulmonate snails by penetrating shells of various shapes and sizes. Crayfish and large prawns chip around the shell aperture to enter thick shells and crush small shells with their mandibles. Crabs use their strong chelae to crush thin and thick shells. Fishes with pharyngeal teeth are major shell-breaking predators that combine with other vertebrate predators such as turtles and wading birds to increase the diversity of gastropod communities by regulating the abundance of dominant species. Although the generalized diets of most freshwater predators preclude tight co-evolutionary patterns of responses, there are combinations of predators that modify gastropod behavior and shell morphology in aquatic assemblages of different ages and depths. This combination of invertebrate and vertebrate predatory impacts led to competitive advantages among individual gastropods with different adaptations: (1) less vulnerable shell morphologies and sizes; (2) predator-avoidance behaviors; or (3) rapid and widespread dispersal with variable life histories. Some individuals develop thicker and/or narrow-opening shells or shells with spines and ridges. Other thin-shelled species crawl out of the water or burrow to lower their risk to shell-breaking or shell-entering predators. Some alter their age at first reproduction and grow rapidly into a size refuge. Fluctuations in water levels and introductions of non-native species can change competitive dominance relationships among gastropods and result in major losses of native species. Many different gastropod predators control species that are human disease vectors. Most snails and their predators provide other ecosystem services such as nutrient cycling and transfer of energy to higher trophic levels. Their persistence and diversity of native species require adaptive management and coordinated study.     

Impact of Commercial Hunting on Monkey Populations in the Taï region,Côte d'Ivoire1

We studied the impact of hunting on monkey species in the Taï National Park and adjacent forests in Côte d'Ivoire. The average wild meat consumption per capita per year was assessed from market surveys and interviews. We determined that the amount of primate wild meat being extracted in the Taï National Park and surrounding forests was 249 t in 1999. Hunting pressure was the highest on the larger primate species such as red colobus, Procolobus badius, black and white colobus, Colobus polykomos, and the sooty mangabey, Cercocebus torquatus atys. Estimates of population densities were based on line transect surveys. The maximum annual production of each species was calculated using the Robinson and Redford model (1991) and assuming unhunted conditions. Comparing current harvest levels with the maximum sustainable yield suggests that harvest of red colobus monkeys (Procolobus badius) is sustainable, whereas current off‐take of the black and white colobus (Colobus polykomos), the sooty mangabey (Cercocebus atys), diana monkeys (Cercopithecus diana), and Campbell's monkeys (Cercopithecus campbelli) exceeds sustainability by up to three times.