Fundamental problems with the cooperative breeding hypothesis. A reply to Burkart & van Schaik.

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.

Tamarins: Insights into monogamous and non-monogamous single female social and breeding systems.

Tamarins are reported to live in small multimale-multifemale groups characterized by a single breeding female. Here we present information on the composition and genetic relatedness of individuals in 12 wild-trapped groups of Weddell's saddleback tamarins (Saguinus weddelli) from northern Bolivia to determine if groups are best described as nuclear or extended families suggesting social monogamy or whether groups contain several unrelated same sex adults indicative of social polyandry/polygyny. Mean group size was 6.25 including an average of 2.16 adult males (range 1-4) and 2.08 adult females (1-3). No group contained only one adult male and one adult female and 25% of groups contained two parous females. We estimated the genetic relatedness among individuals using 13 polymorphic microsatellite markers. Across the population, mean relatedness was low and not significantly different among adult males versus among adult females, suggesting that both sexes disperse from their natal groups. Adults of both sexes also tended to have close same-sex adult relatives within their groups; relatedness among adult females of the same group averaged 0.31 and among adult males was 0.26. This suggests that tamarins of one or both sexes sometimes delay dispersal and remain as adults in their natal group or that emigration of same-sexed relatives into the same group may be common. Finally, parentage analyses indicated that, whereas the parents of juveniles generally were present in the group, this was not always the case. Based on these data, published reports of the presence of multiple breeding males and occasionally multiple breeding females in the same group, and the fact that less than 10% of groups in the wild contain a single adult male-adult female pair, we argue that social polyandry best characterizes the composition of tamarin groups and that monogamy is not a common mating pattern in Saguinus weddelli or other tamarin species.

High-throughput sequencing of fecal DNA to identify insects consumed by wild Weddell's saddleback tamarins (Saguinus weddelli, Cebidae, Primates) in Bolivia.

The genus Saguinus represents a successful radiation of over 20 species of small-bodied New World monkeys. Studies of the tamarin diet indicate that insects and small vertebrates account for ∼16-45% of total feeding and foraging time, and represent an important source of lipids, protein, and metabolizable energy. Although tamarins are reported to commonly consume large-bodied insects such as grasshoppers and walking sticks (Orthoptera), little is known concerning the degree to which smaller or less easily identifiable arthropod prey comprises an important component of their diet. To better understand tamarin arthropod feeding behavior, fecal samples from 20 wild Bolivian saddleback tamarins (members of five groups) were collected over a 3 week period in June 2012, and analyzed for the presence of arthropod DNA. DNA was extracted using a Qiagen stool extraction kit, and universal insect primers were created and used to amplify a ∼280 bp section of the COI mitochondrial gene. Amplicons were sequenced on the Roche 454 sequencing platform using high-throughput sequencing techniques. An analysis of these samples indicated the presence of 43 taxa of arthropods including 10 orders, 15 families, and 12 identified genera. Many of these taxa had not been previously identified in the tamarin diet. These results highlight molecular analysis of fecal DNA as an important research tool for identifying anthropod feeding patterns in primates, and reveal broad diversity in the taxa, foraging microhabitats, and size of arthropods consumed by tamarin monkeys.

Experimental field study of problem-solving using tools in free-ranging capuchins (Sapajus nigritus, formerly Cebus nigritus).

Some populations of capuchins are reported to use tools to solve foraging problems in the wild. In most cases, this involves the act of pounding and digging. The use of probing tools by wild capuchins is considerably less common. Here we report on the results of an experimental field study conducted in southern Brazil designed to examine the ability of wild black-horned capuchins (Sapajus nigritus) to use a wooden dowel as a lever or a probe to obtain an embedded food reward. A group of eight capuchins was presented with two experimental platforms, each housing a clear Plexiglas box containing two bananas on a shelf and four inserted dowels. Depending on the conditions of the experiment, the capuchins were required either to pull (Condition I) or push (Conditions II and III) the dowels, in order to dislodge the food reward from the shelf so that it could be manually retrieved. In Condition I, four individuals spontaneously solved the foraging problem by pulling the dowels in 25% (72/291) of visits. In Conditions II and III, however, no capuchin successfully pushed the dowels forward to obtain the food reward. During these latter two experimental conditions, the capuchins continued to pull the dowels (41/151 or 27% of visits), even though this behavior did not result in foraging success. The results of these field experiments are consistent with an identical study conducted on wild Cebus capucinus in Costa Rica, and suggest that when using an external object as a probe to solve a foraging problem, individual capuchins were able to rapidly learn an association between the tool and the food reward, but failed to understand exactly how the tool functioned in accomplishing the task. The results also suggest that once a capuchin learned to solve this tool-mediated foraging problem, the individual persisted in using the same solution even in the face of repeated failure (slow rate of learning extinction).

Reply to Lawler: feeding competition, cooperation, and the causes of primate sociality.

This is a reply to Richard Lawler's commentary on our previous work [Lawler, 2011; this issue] in which he develops a set of operational models to test socioecological theories of the evolutionary importance of feeding competition. We strongly agree that we need to critically re-evaluate the basic assumptions of all models of primate sociality, and to verify the explanatory power of alternative models. We also feel Lawler's commentary provides an important opportunity to broaden the debate concerning the fundamental roles of cooperation, competition, and aggression in understanding primate social systems. Lawler provides a number of suggestions as to how models developed in primate socioecology might be tested. We agree with these suggestions, make further suggestions, and call for specific operational definitions so that researchers might begin to develop and test various methodologies. However, we also call for testing alternative theories. Current socioecological theory is based on the assumption that competition and positive selection is always in operation and has driven the evolution of living organisms. We believe that this "explanation of choice" often is treated as an assumed truth to which data are forced to fit, rather than being seen as a theory to be tested. Furthermore, we agree with Weiss and Buchanan [2009. The Mermaid's Tale: Four Billion Years of Cooperation in the Making of Living Things] that on ecological and developmental scales, where organisms actually live out their lives, cooperation may play a more fundamental role than competition.

Putting the community back in community ecology and education: the role of field schools and private reserves in the ethical training of primatologists.

In 1993 and 1999, with the assistance of a Nicaraguan family, we founded La Suerte Biological Research Station in northeastern Costa Rica and Ometepe Biological Research Station in southern Nicaragua as a privately owned conservation-oriented business. Our goal was to develop a program of sustainable community ecology focused on education, research, and the conservation of primates and tropical forests. In order to accomplish this we developed field courses in which undergraduate and graduate students conduct scientific research, experience local cultures, and learn about conservation. Over 120 of these students have received doctoral degrees or are currently in graduate programs. Four doctoral dissertations, several MA theses, and some 20 scientific articles have been published based on research conducted at our field stations. In order to achieve our long-term goals of preserving the environment, we also needed to engage directly with local communities to address their needs and concerns. To this end, we developed a series of community-based initiatives related to health care, bilingual education, and conservation education using traditional and on-line teaching tools. In this article, we describe our efforts in Costa Rica and Nicaragua teaching conservation-oriented field courses and working with the local human communities. Building upon these experiences, we outline a set of ethical considerations and responsibilities for private reserves, conservation-oriented businesses, NGOs, and conservancies that help integrate members of the local community as stakeholders in conservation.

Experimental field study of hand preference in wild black-horned (Cebus nigritus) and white-faced (Cebus capucinus) capuchins: evidence for individual and species differences.

In this experimental field investigation, we compare the degree to which wild capuchins in Brazil (Cebus nigritus) and Costa Rica (Cebus capucinus) exhibit individual- and population-level handedness during three visually-guided tasks. These tasks required reaching to remove a large leaf covering a hidden food reward, seizing the food reward, and manipulating a tool (pulling a wooden dowel) in order to obtain access to an embedded food reward. Studies in some populations of captive capuchins indicate evidence for both individual hand preferences and population-level handedness. In this study, six of eight wild C. capucinus and six of seven wild C. nigritus exhibited a significant hand preference during individual tasks, but no individual exhibited a consistent preference across all three tasks. Task-specialization, or the tendency for most individuals in the same group or population to use the same hand to accomplish a particular task, also was evaluated. Cebus nigritus showed a significant bias toward the use of the right hand in removing the leaf. Although the number of individual capuchins in both species that manipulated the dowels was limited (N = 7), each individual that manipulated the dowels in eight or more instances had a positive handedness index, suggesting a greater use of the right hand to accomplish this task. Overall, our results provide preliminary support for individual- and population-level handedness in wild capuchin monkeys.

Wild capuchins (Cebus capucinus) fail to use tools in an experimental field study.

From September through November 2000 we conducted an experimental field study of tool use in a group of 15 wild white-faced capuchins (Cebus capucinus) in Costa Rica. The problem presented to the capuchins involved the use of wooden dowels as probes to obtain a food reward (two bananas) located inside a clear Plexiglas box. Specifically, the task required the capuchins to manually insert a dowel into any of six holes drilled into the box in order to push the bananas off a shelf. The banana could then be retrieved through a large opening at the bottom of the box. The capuchins visited the tool-use platform 702 times over the course of 55 consecutive days and under several experimental conditions. During the first 21 days of the study, they explored the box but made no attempt to touch or pick up the dowels. Even after we placed the dowels in the holes, the capuchins only occasionally manipulated them. Overall, the results indicate that the capuchins did not use a tool to solve this novel foraging problem.

Patterns of positional behavior in mixed-species troops of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in northwestern Brazil.

We present the results of a 4-month field investigation of positional behavior, vertical ranging, and species differences in limb proportions and body mass in a mixed-species troop of Saguinus fuscicollis, Saguinus labiatus, and Callimico goeldii in northwestern Brazil. Despite certain similarities in overall positional repertoire, patterns of positional behavior varied significantly between species. Travel in Callimico occurred principally in the lowest levels of the canopy, and was characterized by an exaggerated form of hindlimb-dominated bounding (bounding-hop), and leaping to and from vertical trunks (55.1% of leaps). In contrast, saddle-back tamarins traveled in the lower and middle levels of the canopy, and engaged in a range of leaping behaviors, including stationary leaps (37.3%), acrobatic leaps (31.3%), and trunk-to-trunk leaps (20%). Red-bellied tamarins exploited the highest levels of the arboreal canopy. Travel in this species was dominated by quadrupedal bounding and acrobatic leaps (67% of leaps) that began and ended on thin, flexible supports. Species differences in positional behavior correlated with species differences in limb proportions and locomotor anatomy, and provide a framework for understanding niche partitioning in mixed-species troops of Saguinus and Callimico.

The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus).

Prehensile tails appear to have evolved at least twice in platyrrhine evolution. In the atelines, the tail is relatively long and possesses a bare area on the distal part of its ventral surface that is covered with der-matoglyphs and richly innervated with Meissner's corpuscles. In contrast, the prehensile tail of Cebus is relatively short, fully haired, and lacks specialized tactile receptors. Little is currently known regarding tail function in capuchins, and whether their prehensile tail serves a greater role in feeding or traveling. In this paper we examine patterns of positional behavior, substrate preference, and tail use in wild white-faced capuchins (Cebus capucinus) inhabiting a wet tropical forest in northeastern Costa Rica. Observational data were collected over the course of 3 months on adult capuchins using an instantaneous focal animal time sampling technique. Differences in the frequency and context of tail use, and the estimated amount of weight support provided by the tail relative to other appendages during feeding/foraging and traveling were used as measures of the ecological role of this specialized organ in capuchin positional behavior. During travel, quadrupedal walking, leaping, and climbing dominated the capuchin positional repertoire. The capuchin tail provided support in only 13.3% of travel and was principally employed during below branch locomotor activities. In contrast, tail-assisted postures accounted for 40.6% of all feeding and foraging records and occurred primarily in two contexts. The tail was used to suspend the individual below a branch while feeding, as well as to provide leverage and weight support in above-branch postures associated with the extraction of prey from difficult to search substrates. A comparison of tail use in Cebus, with published data on the atelines indicates that both taxa possess a grasping tail that is capable of supporting the animal's full body weight. In capuchins and howling monkeys, the tail appears to be used more frequently and serves a greater weight-bearing role during feeding than during traveling. In Ateles, and possibly Brachyteles, and Lagothrix, however, the prehensile tail serves a dual role in both feeding and forelimb suspensory locomotion. Additional relationships between white-faced capuchin feeding, positional behavior, extractive foraging techniques, and prehensile tail use are discussed.

Evolutionary and ecological implications of primate seed dispersal.

In this paper, we evaluate patterns of fruit eating and seed dispersal in monkeys and apes and draw an important distinction between 1) the ecological consequences of primates as seed dispersers and 2) the evolutionary implications of primates on the seed and fruit traits of the plant species they exploit. In many forest communities, primates act as both seed predators and seed dispersers and are likely to have an important ecological impact on patterns of forest regeneration and tree species diversity. Evidence from Kibale National Park, Uganda, and Manu National Park, Peru, as well as several other South American sites indicates that monkeys and apes display a wide range of fruit-processing behaviors, including spitting seeds, dropping seeds, masticating seeds, and swallowing seeds. Differences in consumer body size, diet, ranging patterns, and oral and digestive morphology result in different patterns in the distance and distribution of seeds from the parent plant. In the case of South American monkeys, for example, despite their relatively small body size, platyrrhines were found to exploit larger fruits and swallow larger seeds on average than did Old World monkeys and apes of the Kibale forest. We found little evidence to support the existence of a coevolutionary relationship between a single or set of primate dispersers and the particular plant species they disperse. This is due to variability in the manner in which monkeys and apes select fruits and treat seeds, the fact that many species of primates and nonprimates exploit and disperse the same fruit species, and the fact that extremely high levels of postdispersal seed, seedling, and sapling mortality serve to dilute the influence that any primate species may have on the recruitment of the next generation of adult trees. It is apparent that many primate lineages exhibit dental, digestive, and/or sensory adaptations that aid in the exploitation of particular food types and that many lineages of flowering plants have evolved characteristics of fruits and seeds that facilitate seed dispersal. However, in light of currently available data, we argue that these represent evolutionary rather than more strictly defined coevolutionary relationships.

Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care.

This paper explores relations of ontogeny, life history strategies and patterns of infant care in 11 species of small-bodied New World monkeys. Analysis of these data suggests that differences in the social systems of Aotus, Callicebus, Saimiri, Callimico, Saguinus, Leontopithecus, Cebuella and Callithrix are closely tied to both the costs of reproduction and to the ontogenetic requirements of maturing young. In Saimiri, both rapid prenatal body weight and perinatal brain growth result in relatively high metabolic costs to breeding females. These costs, coupled with minimal nonmaternal assistance in caregiving, appear to favor a reproductive strategy that limits offspring production to a single birth at 2-year intervals. In contrast, tamarins and marmosets are capable of producing twins twice in the same year. Prenatal investment in each offspring is relatively low, and the potentially high postnatal costs of nursing 2 infants are minimized by the evolution of a social system involving extensive extramaternal care-giving. Cooperative infant care in callitrichins (tamarins and marmosets) serves to distribute the metabolic costs of infant ontogeny among several group members. Callimico is also characterized by a high reproductive output, with females capable of producing a single infant twice during the year. Infants continue to grow rapidly after weaning. Patterns of infant development in Callimico are similar to those found in tamarins and marmosets and support a close phylogenetic relationship among these taxa. Aotus and Callicebus are characterized by an alternative strategy. In these taxa, a monogamous mating system is associated with paternal certainty, male parental care, and provisioning of the young. The transfer of male energetic resources to a single offspring allows night and titi monkeys to maintain a comparatively short interbirth interval (1 year). Ecological and social factors, such as predation and feeding competition, do not appear to adequately explain much of the observed variation in infant development and preadult growth rates in these platyrrhines. Instead, reproductive strategies are strongly linked to ontogenetic patterns and life histories.

Experimental field study of spatial memory and learning in wild capuchin monkeys (Cebus capucinus).

Despite a large body of data on diet and ranging patterns in prosimians, monkeys and apes, little is known regarding the types of information that non-human primates use when making foraging decisions. In a series of controlled field experiments, we tested the ability of wild capuchins (Cebus capucinus) at La Suerte Biological Research Station in north-eastern Costa Rica to remember the spatial positions of 13 feeding platforms and use olfactory and visual cues to identify baited (real bananas) versus sham (plastic bananas) feeding sites. The results indicate that when 'place' was predictable, the capuchins learned the spatial locations of food and non-food sites rapidly (one-trial learning). In a second experiment, the positions of baited feeding sites were random. In the absence of other information, the capuchins used the presence of a local landmark cue (yellow block) placed at reward platforms to select feeding sites. In a final experiment, there was evidence that expectations regarding the amount of food available at a platform (2 bananas vs. 1/2 banana) had a significant influence on capuchin foraging decisions. Although the capuchins were sensitive to changes in experimental conditions, when they were given conflicting cues, spatial information was predominant over other information in selecting feeding sites.

Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax).

In several primate taxa there is evidence that the social and physical environment can exert a significant effect on reproductive behavior and biology. In this paper we examine social and physiological factors influencing group composition and reproduction in free-ranging moustached tamarin monkeys (Saguinus mystax mystax). This species is characterized by cooperative care of the young and a breeding system that includes both polyandrous and polygyandrous matings. Body measurements collected on adult males residing in multimale groups indicate marked within-group differences in testes volume. In 12 of 17 groups examined, testes volume of at least two resident adult males differed by 21-174%. Among these males, testes volume was not correlated with either body weight or adult age class. We also examine whether factors such as time of year had an effect on reproductive condition. An analysis of body measurements of 128 adult male and 127 adult female moustached tamarins, wild-trapped and released in northeastern Peru, indicates cyclic changes in genital size. For males, mean monthly testes volume in July (712 mm3) was twice that recorded in June (351 mm3). Females exhibited a similar pattern. Although endocrine information on intra- and intersexual social effects on fertility are unavailable for S. mystax, given the high degree of social cooperation and lack of overt aggression among adult male group members, we offer the possibility that resident male moustached tamarins compete for access to the groups' lone breeding female through socially induced reproductive suppression and sperm competition. © 1996 Wiley-Liss, Inc.

Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems.

In this paper we address a series of questions concerning reproductive opportunities, kinship, dispersal, and mating patterns in free-ranging moustached tamarin monkeys (Saguinus mystax). Between 1980 and 1990 information on group size, composition, and migration patterns was collected on marked groups of moustached tamarins inhabiting Padre Isla, an island in the Amazon Basin of northeastern Peru. In 1990, 86% of 114 animals residing in 16 social groups were trapped, examined, and released. Mean group size was 7.0, including 2.2 adult males and 2.0 adult females. None of these groups was characterized by a single adult male-female pair. In groups with more than one adult female, only the oldest female produced offspring. An examination of dispersal patterns indicates that transfers between groups were common and fell into several categories, including immigration of individual males and females, simultaneous transfer of pairs of subadult and/or adult males (sometimes relatives) into the same social groups, and group fissioning in which males and females of the splinter group join another small social group. We have no unambiguous cases of 2 adult/subadult females migrating together into the same social group. All 6 groups for which reproductive data were available were characterized by either a polyandrous or polygynous (polygyandrous) mating pattern. The results of this study indicate that moustached tamarins reside in small multimale multifemale groups that are likely to contain both related and unrelated adult group members. Kinship and social ties among males appear to be stronger and more longlasting than kinship and social ties among females. We contend that the modal mating system of moustached and many other tamarins is not monogamous, and offer the possibility that cooperative infant care and mating system flexibility in callitrichines evolved from a polygynous mating pattern. © 1993 Wiley-Liss, Inc.

Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae.

Primates of the subfamily Callitrichinae (Callimico, Callithrix, Leontopithecus, and Saguinus) are small-bodied New World monkeys (105-700 g) possessing clawlike nails on all manual and pedal digits excluding the hallux. Specialized nails in these genera serve a critical function in feeding by enabling tamarins and marmosets to cling to trunks and other large vertical supports while exploiting food resources. Within the subfamily, there is evidence of at least four distinct large-branch feeding patterns. These include (1) seasonal exudate feeding and occasional trunk foraging (many Saguinus spp.); (2) exploitation of bark surface insects and the use of trunks as a platform to locate terrestrial prey (Saguinus fuscicollis, S. nigricollis, and Callimico); (3) manipulative foraging and bark stripping to locate concealed insects and small vertebrates (Leontopithecus); and (4) tree gouging and year-round exudate feeding (many Callithrix). Large-branch feeding and the use of vertical clinging postures appear to be a primary adaptation among virtually all callitrichines, distinguishing them ecologically from other platyrrhine taxa. Given the anatomy and behavior of extant callitrichines, Saguinus appears to be the most ecologically generalized member of this subfamily, and species of this genus may provide useful models for reconstructing the feeding and foraging adaptations of early callitrichines.

Body weights in mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons in Amazonian Peru.

An investigation of body weights of members of mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons was conducted at the Rio Blanco Research Station in northeastern Peru. A total of 107 adult and subadult tamarin monkeys were trapped, measured, and released. Data collected indicate that mean body weights for adult male and female moustached tamarins are 564 gm and 626 gm, respectively, whereas for adult saddle-back tamarins these values are 412 gm and 411 gm. Subadults weighed 11-27% less than adults. Body weights recorded in this study are significantly greater than those previously reported for tamarins of the same species and age living in other areas of Amazonian Peru. We hypothesize that, in the case of moustached and saddle-back tamarins, advantages associated with feeding and foraging in mixed species troops facilitate greater efficiency in resource monitoring and result in the maintenance of larger body weights.

Ecological distinctions between sympatric species of Saguinus and Sciurus.

Tamarins are small New World monkeys that have been described as "squirrellike." Squirrels, along with bats and birds, are the taxa most likely to utilize resources similar to those used by primates in the tropical forest canopy. In this paper we compare differences in ecology, diet, locomotion, and habitat utilization between sympatric populations of tamarins (Saguinus oedipus) and tree squirrels (Sciurus granatensis) in Panama. Data presented indicate that although there is some degree of resource overlap, patterns of habitat utilization differ significantly. Rather than being "squirrellike," the Panamanian tamarin exhibits a pattern of locomotor and feeding behavior consistent with that found in other arboreal primates.