susanne.shultz@manchester.ac.uk Shultz | The University of Manchester (original) (raw)

Papers by susanne.shultz@manchester.ac.uk Shultz

Behavioral Ecology, Jan 1, 2010

Predation is a major force in shaping biological communities, both over ecological and evolutiona... more Predation is a major force in shaping biological communities, both over ecological and evolutionary timescales. In response to predation pressure, prey have evolved characteristics designed to mitigate predation pressure. We evaluated predator foraging biases in relation to prey characteristics across 16 vertebrate communities. We show that although predator biases vary, some prey traits are consistently associated with predator diet composition. Within their acceptable prey size range, predators show positive bias toward larger bodied prey, small-brained prey (controlling for body size), small group size, and terrestriality. Thus, whether predator foraging decisions are passive or active, predator choice exerts differential pressure on prey species according to prey characteristics. Predator biases also were positively associated with early age at maturity, supporting the role of mortality in driving life-history characteristics. These results support several theoretical models of predation including its role as a selective force driving evolutionary changes in life history, brain size and sociality, optimal diet theory, and antiapostatic predation.

Journal of Comparative Psychology, Jan 1, 2010

A persistent debate in behavioral research is whether brain size or architecture relates to cogni... more A persistent debate in behavioral research is whether brain size or architecture relates to cognitive performance. A growing body of evidence has demonstrated correlations between brain size and ecological and behavioral tasks. These studies are premised on a causal link between brain size and cognitive function, although this association has little empirical backing. We show, for a set of 46 species from 17 primate genera, that competence on a series of eight executive function cognitive tasks both correlate across tasks and with brain size and architecture across species. Our model selection approach showed that, although several measures of brain component volumes are significantly associated with performance, hippocampus size is the best predictor of overall performance. The best performing model also includes total brain size and relative neocortex size. Additionally, absolute measures are much more predictive of performance than relative measures of brain and brain component size. These results are consistent with the hippocampus' role in learning, and the executive brain (neocortex) being important for problem solving and consolidation. Our findings challenge and extend those of previous analyses by clarifying the relationship between overall brain size and specific regional volumes. They also suggest that commonly used indices of encephalization, such as residuals of brain volume regressed on body size, may confound rather than clarify matters.

Behavioral Ecology and Sociobiology, Jan 1, 2010

Female rhesus macaques exhibit matrilineal dominance structures, and high dominance rank confers ... more Female rhesus macaques exhibit matrilineal dominance structures, and high dominance rank confers fitness benefits across a lifetime and across generations. Rank effects are “inherited” through social processes that are well understood; however, biological mechanisms that might impact these processes are not well known. Recently, it has been shown that prenatal androgens appear to be implicated in supporting dominance rank hierarchies in some mammals. In humans, interindividual differences in the second (index) to fourth (ring) digit ratio (2D:4D) have been linked indirectly to variation in prenatal androgens, with low 2D:4D in both sexes associated with higher inferred prenatal androgen effects. 2D:4D has also been related to dominant social behavior and has been shown to co-vary with social systems across nonhuman primate species. Here, we investigate how 2D:4D co-varies with socially inherited dominance rank in female rhesus macaques. Low 2D:4D was associated with higher-ranking females, while higher 2D:4D was associated with lower-ranking females. Similar relationships were also shown between ranked families within matrilines. This is the first study to show such a relationship between 2D:4D and dominance rank in a nonhuman primate and suggests that prenatal androgen effects could be involved in the maintenance of dominance rank in female cercopithecine primates.

Behaviour, Jan 1, 2010

Approaches to sociality have, in the past, focused either on group typologies or on the functiona... more Approaches to sociality have, in the past, focused either on group typologies or on the functional aspects of relationships (mate choice, parental investment decisions). In contrast, the nature of the social relationships that scale from the individual-level behavioural decisions to the emergent properties represented by group typology has received almost no attention at all. We argue that that there is now a need to refocus attention on the bonding processes that give rise to social groups. However, we lack any kind of language with which to describe or classify these operationally, in part perhaps because social bonding is emotional (and, hence, 'felt'). One task for the future is, therefore, to identify suitable indices that can be used to compare the degree of bondedness between individual animals both between species and, within species, between individual dyads in such a way as to be able to test functional questions.

American Journal of Physical Anthropology, Jan 1, 2009

The second-to-fourth digit ratio (2D:4D) has been proposed as a biomarker reflecting prenatal and... more The second-to-fourth digit ratio (2D:4D) has been proposed as a biomarker reflecting prenatal androgen effects (PAE), such that individuals with lower ratios have experienced higher PAE than those with higher ratios. 2D:4D has been correlated with a number of sex-linked traits in humans such as aggression, promiscuity, and competitiveness. In addition, polygynous societies reportedly have lower 2D:4D (higher PAE) than more monogamous populations. This evidence suggests that PAE may be implicated in the development of sexually selected behaviors in humans. To place 2D:4D research into a broader context, we test the relationship between digit ratios and behavior across nonhuman anthropoids; polygynous species, with higher levels of intrasexual competition, should have more pronounced markers of PAE (lower 2D:4D) than pair-bonded species. Our results accord with those found in humans: 2D:4D is lower in polygynous species and higher (lower PAE) in pair-bonded species. Old World monkeys have low, and relatively invariant 2D:4D (high PAE), which is coupled with high levels of intrasexual competition. This contrasts with higher and more variable ratios in both great apes and New World monkeys. In addition, both male and female ratios decrease with increasing levels of intrasexual competition. Human ratios are intermediate between pair-bonded and more promiscuous hominoids. We propose that PAE may be involved in promoting species characteristic social behavior in anthropoids. Am J Phys Anthropol, 2010. © 2009 Wiley-Liss, Inc.

Behavioral Ecology and Sociobiology, Jan 1, 2003

Although much is known about the relationship between vigilance, group size and predation risk, b... more Although much is known about the relationship between vigilance, group size and predation risk, behavioural responses to predation risk and their resultant costs are less clear. We investigated the response of Diana monkeys to increased predation risk by looking at behavioural changes associated with male long-distance calls, which are reliably given to certain predators. After male long-distance calls, group spread and nearest-neighbour distance decreased whilst travel and association rates for the group increased. The average height and exposure level of individuals in the group did not change after calls. Individual Diana monkeys changed their behaviour and were more likely to be vigilant or travel and less likely to engage in social or resting behaviours after long-distance calls. In addition, movement rates increased with the number of species the Diana monkeys were associated with. Diana monkey long-distance calls facilitate the joining of groups of other species. Black and white colobus and lesser spot-nosed monkeys were more likely to be in an association following a long-distance call than before. Behavioural responses, such as increased travel or association rates, that reduce foraging efficiency are interpreted as evidence of a non-lethal impact of increased predation risk.

Biology Letters, Jan 1, 2006

Prey use a wide variety of anti-predator defence strategies, including morphological and chemical... more Prey use a wide variety of anti-predator defence strategies, including morphological and chemical defences as well as behavioural traits (riskmodulated habitat use, changes in activity patterns, foraging decisions and group living). The critical test of how effective anti-predator strategies are is to relate them to relative indices of mortality across predators. Here, we compare biases in predator diet composition with prey characteristics and show that chimpanzee (Pan troglodytes) and felid show the strongest and the most consistent predator bias towards smallbrained prey. We propose that large-brained prey are likely to be more effective at evading predators because they can effectively alter their behavioural responses to specific predator encounters. Thus, we provide evidence for the hypothesis that brain size evolution is potentially driven by selection for more sophisticated and behaviourally flexible anti-predator strategies.

Mammal Review, Jan 1, 2002

Evolution, Jan 1, 2007

As the brain is responsible for managing an individual's behavioral response to its environment, ... more As the brain is responsible for managing an individual's behavioral response to its environment, we should expect that large relative brain size is an evolutionary response to cognitively challenging behaviors. The “social brain hypothesis” argues that maintaining group cohesion is cognitively demanding as individuals living in groups need to be able to resolve conflicts that impact on their ability to meet resource requirements. If sociality does impose cognitive demands, we expect changes in relative brain size and sociality to be coupled over evolutionary time. In this study, we analyze data on sociality and relative brain size for 206 species of ungulates, carnivores, and primates and provide, for the first time, evidence that changes in sociality and relative brain size are closely correlated over evolutionary time for all three mammalian orders. This suggests a process of coevolution and provides support for the social brain theory. However, differences between taxonomic orders in the stability of the transition between small-brained/nonsocial and large-brained/social imply that, although sociality is cognitively demanding, sociality and relative brain size can become decoupled in some cases. Carnivores seem to have been especially prone to this.

American Journal of Physical Anthropology, Jan 1, 2006

Understanding the initial processes of deposition can help with interpretations of fossil assembl... more Understanding the initial processes of deposition can help with interpretations of fossil assemblages. Here we discuss the taphonomy of primate remains collected under 16 nests of African crowned eagles (Stephanoaetus coronatus) in the Tai Forest, Ivory Coast. From 1,200 bones collected, including 669 primate bones, we calculated minimum number of individuals (MNI), survivability profiles, and damage profiles using methods identical to those employed by Sanders et al. (2003 J. Hum. Evol. 44:87–105) in their analysis of bones from eagle nests in Uganda. Crowned eagles leave a consistent taphonomic signature on their prey remains; hence, results from our analysis of the Tai assemblage are similar to those from the Ugandan sample. Hindlimb and cranial bones are relatively abundant in the sample, while ribs, vertebrae, carpals, and tarsals do not survive well. Primate crania typically display puncture marks around the eye, long bones remain largely intact, and scapulae exhibit raked breakage. These data have implications for understanding the dynamic between extant primates and one of their principle predators, as well as the taphonomy of hominid-bearing caves in South Africa. We concur with Berger and Clarke (1995 J. Hum. Evol. 29:275–299) that a large raptor could have been responsible for the death of the Taung child, Australopithecus africanus. Am J Phys Anthropol 131:151–165, 2006. © 2006 Wiley-Liss, Inc.

Proceedings of The Royal Society B: Biological Sciences, Jan 1, 2002

Journal of Applied Ecology, Jan 1, 2004

1Rapid population declines of the vultures Gyps bengalensis, Gyps indicus and Gyps tenuirostris h... more 1Rapid population declines of the vultures Gyps bengalensis, Gyps indicus and Gyps tenuirostris have recently been observed in India and Pakistan, continuing at least up to 2003. Surveys indicate annual rates of decline of 22–50% for G. bengalensis and G. indicus during 2000–03. Previous studies in Pakistan have shown that the non-steroidal anti-inflammatory drug diclofenac causes renal failure and is lethal to G. bengalensis when it feeds on the carcass of a domestic animal that received a normal veterinary dose shortly before death. In Pakistan, diclofenac poisoning was found to be by far the most frequent cause of death.2A simulation model of vulture demography, described in this paper, demonstrated that the observed rates of population decline could be caused by contamination with a lethal level of diclofenac in a small proportion (between 1 : 130 and 1 : 760) of ungulate carcasses available to vultures.3Proportions of adult and subadult vultures found dead or dying in the wild that had signs of diclofenac poisoning were similar to the proportions of deaths expected from the model if the observed population decline was due entirely to diclofenac poisoning. The proportion of the excess mortality required to cause the observed population declines that could be attributable to diclofenac was estimated to be between 71% and 100%, depending on model assumptions. However, across all or most of the plausible range of assumed values for adult survival, the upper 95% confidence limit for the proportion of excess mortality due to diclofenac was 100%. Hence, available data are consistent with diclofenac poisoning being at least the major cause, and possibly the only cause, of rapid population declines of Gyps vultures across the Indian subcontinent.4Synthesis and applications. We recommend that urgent action is taken in the range states of the three currently threatened vulture species to prevent the exposure of vultures to livestock carcasses contaminated with diclofenac. Research is also needed to identify alternative drugs that are effective in livestock and safe for vultures. Efforts should also be made to raise awareness, among veterinarians, pharmacists, livestock owners and the general public, of the problem of diclofenac contamination and the availability of safe alternatives. Captive holding and breeding of vultures until diclofenac is controlled is recommended as a precaution to ensure the long-term survival of the threatened species and to provide a stock of birds for future reintroduction programmes.Rapid population declines of the vultures Gyps bengalensis, Gyps indicus and Gyps tenuirostris have recently been observed in India and Pakistan, continuing at least up to 2003. Surveys indicate annual rates of decline of 22–50% for G. bengalensis and G. indicus during 2000–03. Previous studies in Pakistan have shown that the non-steroidal anti-inflammatory drug diclofenac causes renal failure and is lethal to G. bengalensis when it feeds on the carcass of a domestic animal that received a normal veterinary dose shortly before death. In Pakistan, diclofenac poisoning was found to be by far the most frequent cause of death.A simulation model of vulture demography, described in this paper, demonstrated that the observed rates of population decline could be caused by contamination with a lethal level of diclofenac in a small proportion (between 1 : 130 and 1 : 760) of ungulate carcasses available to vultures.Proportions of adult and subadult vultures found dead or dying in the wild that had signs of diclofenac poisoning were similar to the proportions of deaths expected from the model if the observed population decline was due entirely to diclofenac poisoning. The proportion of the excess mortality required to cause the observed population declines that could be attributable to diclofenac was estimated to be between 71% and 100%, depending on model assumptions. However, across all or most of the plausible range of assumed values for adult survival, the upper 95% confidence limit for the proportion of excess mortality due to diclofenac was 100%. Hence, available data are consistent with diclofenac poisoning being at least the major cause, and possibly the only cause, of rapid population declines of Gyps vultures across the Indian subcontinent.Synthesis and applications. We recommend that urgent action is taken in the range states of the three currently threatened vulture species to prevent the exposure of vultures to livestock carcasses contaminated with diclofenac. Research is also needed to identify alternative drugs that are effective in livestock and safe for vultures. Efforts should also be made to raise awareness, among veterinarians, pharmacists, livestock owners and the general public, of the problem of diclofenac contamination and the availability of safe alternatives. Captive holding and breeding of vultures until diclofenac is controlled is recommended as a precaution to ensure the long-term survival of the threatened species and to provide a stock of birds for future reintroduction programmes.

Proceedings of The Royal Society B: Biological Sciences, Jan 1, 2006

Among mammals, the members of some Orders have relatively large brains. Alternative explanations ... more Among mammals, the members of some Orders have relatively large brains. Alternative explanations for this have emphasized either social or ecological selection pressures favouring greater informationprocessing capacities, including large group size, greater foraging efficiency, higher innovation rates, better invasion success and complex problem solving. However, the focal taxa for these analyses (primates, carnivores and birds) often show both varied ecological competence and social complexity. Here, we focus on the specific relationship between social complexity and brain size in ungulates, a group with relatively simple patterns of resource use, but extremely varied social behaviours. The statistical approach we used, phylogenetic generalized least squares, showed that relative brain size was independently associated with sociality and social complexity as well as with habitat use, while relative neocortex size is associated with social but not ecological factors. A simple index of sociality was a better predictor of both total brain and neocortex size than group size, which may indicate that the cognitive demands of sociality depend on the nature of social relationships as well as the total number of individuals in a group.

Folia Primatologica, Jan 1, 2001

African crowned eagles (Stephanoaetus coronatus) are widely recognised as the most important pred... more African crowned eagles (Stephanoaetus coronatus) are widely recognised as the most important predator for arboreal primates throughout sub-Saharan Africa. Due to the difficulty of observing eagles, few interactions between monkeys and eagles have been documented [but see 1, ...

Proceedings of The Royal Society B: Biological Sciences, Jan 1, 2007

The social brain hypothesis argues that large brains have arisen over evolutionary time as a resp... more The social brain hypothesis argues that large brains have arisen over evolutionary time as a response to the social and ecological conflicts inherent in group living. We test predictions arising from the hypothesis using comparative data from birds and four mammalian orders (Carnivora, Artiodactyla, Chiroptera and Primates) and show that, across all non-primate taxa, relative brain size is principally related to pairbonding, but with enduring stable relationships in primates. We argue that this reflects the cognitive demands of the behavioural coordination and synchrony that is necessary to maintain stable pairbonded relationships. However, primates differ from the other taxa in that they also exhibit a strong effect of group size on brain size. We use data from two behavioural indices of social intensity (enduring bonds between group members and time devoted to social activities) to show that primate relationships differ significantly from those of other taxa. We suggest that, among vertebrates in general, pairbonding represents a qualitative shift from loose aggregations of individuals to complex negotiated relationships, and that these bonded relationships have been generalized to all social partners in only a few taxa (such as anthropoid primates).

Proceedings of The Royal Society B: Biological Sciences, Jan 1, 2004

Although predation avoidance is the most commonly invoked explanation for vertebrate social evolu... more Although predation avoidance is the most commonly invoked explanation for vertebrate social evolution, there is little evidence that individuals in larger groups experience lower predation rates than those in small groups. We compare the morphological and behavioural traits of mammal prey species in the Taï forest, Ivory Coast, with the diet preferences of three of their non-human predators: leopards, chimpanzees and African crowned eagles. Individual predators show marked differences in their predation rates on prey species of different body sizes, but clear patterns with prey behaviour were apparent only when differences in prey habitat use were incorporated into the analyses. Leopard predation rates are highest for terrestrial species living in smaller groups, whereas eagle predation rates are negatively correlated with group size only among arboreal prey. When prey predation rates are summed over all three predators, terrestrial species incur higher predation rates than arboreal species and, within both categories, predation rates decline with increasing prey group size and decreasing density of groups in the habitat. These results reveal that it is necessary to consider anti-predator strategies in the context of a dynamic behavioural interaction between predators and prey.

Philosophical Transactions of The Royal Society B: Biological Sciences, Jan 1, 2007

We present a detailed reanalysis of the comparative brain data for primates, and develop a model ... more We present a detailed reanalysis of the comparative brain data for primates, and develop a model using path analysis that seeks to present the coevolution of primate brain (neocortex) and sociality within a broader ecological and life-history framework. We show that body size, basal metabolic rate and life history act as constraints on brain evolution and through this influence the coevolution of neocortex size and group size. However, they do not determine either of these variables, which appear to be locked in a tight coevolutionary system. We show that, within primates, this relationship is specific to the neocortex. Nonetheless, there are important constraints on brain evolution; we use path analysis to show that, in order to evolve a large neocortex, a species must first evolve a large brain to support that neocortex and this in turn requires adjustments in diet (to provide the energy needed) and life history (to allow sufficient time both for brain growth and for 'software' programming). We review a wider literature demonstrating a tight coevolutionary relationship between brain size and sociality in a range of mammalian taxa, but emphasize that the social brain hypothesis is not about the relationship between brain/neocortex size and group size per se; rather, it is about social complexity and we adduce evidence to support this. Finally, we consider the wider issue of how mammalian (and primate) brains evolve in order to localize the social effects.

Proceedings of The Royal Society B: Biological Sciences, Jan 1, 2005

Large-scale population declines have been documented across many faunal assemblages. However, the... more Large-scale population declines have been documented across many faunal assemblages. However, there is much variation in population trends for individual species, and few indications of which specific ecological and behavioural characteristics are associated with such trends. We used the British Common Birds Census to identify specific traits associated with long-term abundance trends in UK farmland birds. Two factors, resource specialization and relative brain size, were significantly associated with population trend, such that species using atypical resources and with relatively small brains were most likely to have experienced overall declines. Further analyses of specific brain components indicated that the relative size of the telencephalon, the part of the brain associated with problem solving and complex behaviours, and the brain stem might be better predictors of population trend than overall brain size. These results suggest that flexibility in resource use and behaviour are the most important characteristics for determining a species' ability to cope with large-scale habitat changes.