Fundamental Problems with the Cooperative Breeding Hypothesis. A reply to Burkart & Van Schaik

This is the final version of the article. Available from Wiley via the DOI in this record.The cooperative breeding hypothesis (CBH) states that cooperative breeding, a social system in which group members help to rear offspring that are not their own, has important socio-cognitive consequences. Thornton & McAuliffe (2015; henceforth T&M) critiqued this idea on both conceptual and empirical grounds, arguing that there is no reason to predict that cooperative breeding should favour the evolution of enhanced social cognition or larger brains, nor any clear evidence that it does. In response to this critique, Burkart & van Schaik (2016 henceforth B&vS) attempt to clarify the causal logic of the CBH, revisit the data and raise the possibility that the hypothesis may only apply to primates. They concede that cooperative breeding is unlikely to generate selection pressures for enhanced socio-cognitive abilities, but argue instead that the CBH operates purely through cooperative breeding reducing social or energetic constraints. Here, we argue that this revised hypothesis is also untenable because: (1) it cannot explain why resources so released would be allocated to cognitive traits per se rather than any other fitness-related traits, (2) key assumptions are inconsistent with available evidence and (3) ambiguity regarding the predictions leaves it unclear what evidence would be required to falsify it. Ultimately, the absence of any compelling evidence that cooperative breeding is associated with elevated cognitive ability or large brains (indeed data suggest the opposite is true in non-human primates) also casts doubt on the capacity of the CBH to explain variation in cognitive traits.A.T. was supported by a BBSRC David Phillips Fellowship (BB/H021817/1) and a grant from the ESRC (ES/M006042/1)

Influences on gum feeding in primates

This chapter reviews the factors that may affect patterns of gum feeding by primates. These are then examined for mixed-species troops of saddleback (S. fuscicollis) and mustached (S. mystax) tamarins. An important distinction is made between gums produced by tree trunks and branches as a result of damage and those produced by seed pods as part of a dispersal strategy as these may be expected to differ in their biochemistry. Feeding on fruit and Parkia seed pod exudates was more prevalent in the morning whereas other exudates were eaten in the afternoon. This itinerary may represent a deliberate strategy to retain trunk gums in the gut overnight, thus maximising the potential for microbial fermentation of their β-linked oligosaccharides. Both types of exudates were eaten more in the dry than the wet season. Consumption was linked to seasonal changes in resource availability and not the tamarins’ reproductive status pro-viding no support for the suggestion that gums are eaten as a pri-mary calcium source in the later stages of gestation and lactation. The role of availability in determining patterns of consumption is further supported by the finding that dietary overlap for the trunk gums eaten was greater between species within mixed-species troops within years than it was within species between years. These data and those for pygmy marmosets (Cebuella pygmaea) suggest that patterns of primate gummivory may reflect the interaction of prefer-ence and availability for both those able to stimulate gum production and those not

Forest chimpanzees (Pan troglodytes verus) remember the location of numerous fruit trees

It is assumed that spatial memory contributes crucially to animal cognition since animals’ habitats entail a large number of dispersed and unpredictable food sources. Spatial memory has been investigated under controlled conditions, with different species showing and different conditions leading to varying performance levels. However, the number of food sources investigated is very low compared to what exists under natural conditions, where food resources are so abundant that it is difficult to precisely identify what is available. By using a detailed botanical map containing over 12,499 trees known to be used by the Taï chimpanzees, we created virtual maps of all productive fruit trees to simulate potential strategies used by wild chimpanzees to reach resources without spatial memory. First, we simulated different assumptions concerning the chimpanzees’ preference for a particular tree species, and, second, we varied the detection field to control for the possible use of smell to detect fruiting trees. For all these assumptions, we compared simulated distance travelled, frequencies of trees visited, and revisit rates with what we actually observed in wild chimpanzees. Our results show that chimpanzees visit rare tree species more frequently, travel shorter distances to reach them, and revisit the same trees more often than if they had no spatial memory. In addition, we demonstrate that chimpanzees travel longer distances to reach resources where they will eat for longer periods of time, and revisit resources more frequently where they ate for a long period of time during their first visit. Therefore, this study shows that forest chimpanzees possess a precise spatial memory which allows them to remember the location of numerous resources and use this information to select the most attractive resources

Spatial memory in the grey mouse lemur (Microcebus murinus)

Wild animals face the challenge of locating feeding sites distributed across broad spatial and temporal scales. Spatial memory allows animals to find a goal, such as a productive feeding patch, even when there are no goal-specific sensory cues available. Because there is little experimental information on learning and memory capabilities in free-ranging primates, the aim of this study was to test whether grey mouse lemurs (Microcebus murinus), as short-term dietary specialists, rely on spatial memory in relocating productive feeding sites. In addition, we asked what kind of spatial representation might underlie their orientation in their natural environment. Using an experimental approach, we set eight radio-collared grey mouse lemurs a memory task by confronting them with two different spatial patterns of baited and non-baited artificial feeding stations under exclusion of sensory cues. Positional data were recorded by focal animal observations within a grid system of small foot trails. A change in the baiting pattern revealed that grey mouse lemurs primarily used spatial cues to relocate baited feeding stations and that they were able to rapidly learn a new spatial arrangement. Spatially concentrated, non-random movements revealed preliminary evidence for a route-based restriction in mouse lemur space; during a subsequent release experiment, however, we found high travel efficiency in directed movements. We therefore propose that mouse lemur spatial memory is based on some kind of mental representation that is more detailed than a route-based network map

Vigilance in a Cooperatively Breeding Primate

Collective vigilance is considered a major advantage of group living in animals. We investigated vigilance behavior in wild mustached tamarins (Saguinus mystax), small, arboreal, cooperatively breeding New World primates that form stable mixed-species groups with saddleback tamarins (Saguinus fuscicollis). We aimed 1) to investigate whether vigilance patterns change according to individual activity and 2) to examine whether there is a social component of vigilance in their cooperative and nonaggressive society. We studied 11 factors that may influence vigilance and used this data to interpret the possible functions of vigilance. We observed 44 individuals in 3 mixed-species and 2 single-species groups of 2 populations that differed in population density and home range sizes. Vigilance changed greatly when individuals were engaged in different activities and individual vigilance was affected by different sets of factors depending on the activity. As vigilance decreased in proximity of conspecifics and heterospecifics when feeding, and in larger mixed-species groups when resting, we conclude that the predominant function of vigilance in mustached tamarins is predator related. However, the absence of the group size effect in very large single-species groups suggests that it may also function to maintain group cohesion. In the population with higher density and smaller home ranges individuals also increased their vigilance in home range overlap areas. We found no evidence that mustached tamarins monitor group mates to avoid food stealing or aggression. The effect of heterospecifics on individual vigilance suggests that collective vigilance might have been an important incentive in the evolution of tamarin mixed-species groups

Functions of Intermittent Locomotion in Mustached Tamarins (Saguinus mystax)

Many animals interrupt their moving with brief pauses, which appear to serve several different functions. We examined the function of such intermittent locomotion in wild living mustached tamarins (Saguinus mystax), small arboreal New World primates that form mixed-species groups with saddleback tamarins (Saguinus fuscicollis). We investigated how different environmental and social factors affect pausing during locomotion and used these data to infer the function of this behavior. As measures of intermittent locomotion, we used percentage of time spent pausing and pause rate. We considered 3 possible functions that are not mutually exclusive: increased endurance, route planning, and antipredator vigilance. Mustached tamarins spent on average (mean ± SE) 55.1 ± 1.0% of time pausing, which makes effective resource exploitation more time consuming and needs to be outweighed by correspondingly large benefits. Percentage of time spent pausing decreased in larger mixed-species groups vs. smaller mixed-species groups and decreased with height and in monkeys carrying infants. It was not affected by sex, age, spatial arrangement, or single-species group size. Pause rate increased in individuals traveling independently compared to those traveling in file, but was not affected by other factors. The group size effect in mixed-species groups lends support to the notion that pausing during locomotion is an antipredator tactic that can be reduced in the increased safety of larger groups, but other results suggest that additional functions, particularly route planning, are also of great importance. Benefits in terms of predator confusion and group movement coordination are also likely to play a role and remain a topic for further research

Vigilance of mustached tamarins in single-species and mixed-species groups—the influence of group composition

Species that participate in mixed-species groups (MSG) may have complementary roles in antipredator strategies. We studied vigilance in mustached tamarins (Saguinus mystax), small arboreal primates that form stable mixed-species groups with saddleback tamarins (Saguinus fuscicollis), in order to examine how the direction of vigilance changes with different species group compositions and whether the division of labor between the two species can be confirmed. We did so by comparing quantitative and qualitative differences in vigilance behavior between same individuals in and out of association (case A); MSG and single-species groups of the same total group size from two different populations (case B); and MSG of the same group size but with a different ratio of conspecifics to heterospecifics (case C). We predicted that individuals would increase downward scanning when heterospecifics are absent or their percentage is low, but total vigilance would increase only in case A due to the group size effect. However, mustached tamarins increased total vigilance due to horizontal scanning in cases A and C, and the predictions were confirmed only in small-sized groups in case B. Thus, we found indications that associating tamarin species in MSG might complement each other in the direction of vigilance, but the division of labor alone does not satisfactorily explain all the findings. There appear to be other mechanisms at work that define how direction of vigilance changes with group size and species composition. Complementarity of species probably occurs due to species vertical stratification rather than differences in the direction of vigilance

Effect of Resting Patterns of Tamarins (Saguinus fuscicollis and Saguinus mystax) on the Spatial Distribution of Seeds and Seedling Recruitment

The spatial distributions of dispersed seeds have important evolutionary consequences for plants. Repeated defecations in sites frequently used by seed dispersers can result in high seed concentrations. We observed the resting behavior of a mixed-species group of tamarins in Peru and recorded the occurrence of seed dispersal (over 8 mo) and seed fate (over 11–22 mo) to determine whether the location and use of resting sites influenced the spatial distribution of dispersed seeds and seedlings. The tamarins rested mostly on trees (Saguinus fuscicollis: 60.6%, S. mystax: 89.2%) and dead trunks (S. fuscicollis: 24.4%) and used 61% of their resting sites repeatedly. During both the dry and wet seasons, tamarins dispersed significantly more seeds within resting areas (0.00662 and 0.00424 seeds/m2, respectively) than outside them (0.00141 and 0.00181 seeds/m2). Seed survival and seedling recruitment did not differ significantly between resting and other areas, resulting in a higher seedling concentration around the resting sites. Seed density did not increase with the duration or the frequency of use of the resting sites but did increase when we pooled the seasonal resting sites together in 50 m × 50 m quadrats, ultimately causing a clumped distribution of dispersed seeds. The use of resting sites in secondary forest, particularly during the dry season, allows the creation of seedling recruitment centers for species coming from the primary forest. Our findings show that tamarin resting behavior affects the spatial distribution of dispersed seeds and seedlings, and their resting sites play an important role in plant diversity maintenance and facilitate forest regeneration in degraded areas

The bashful and the boastful : prestigious leaders and social change in Mesolithic Societies

The creation and maintenance of influential leaders and authorities is one of the key themes of archaeological and historical enquiry. However the social dynamics of authorities and leaders in the Mesolithic remains a largely unexplored area of study. The role and influence of authorities can be remarkably different in different situations yet they exist in all societies and in almost all social contexts from playgrounds to parliaments. Here we explore the literature on the dynamics of authority creation, maintenance and contestation in egalitarian societies, and discuss the implications for our interpretation and understanding of the formation of authorities and leaders and changing social relationships within the Mesolithic