Social traditions and social learning in capuchin monkeys (Cebus)

Capuchin monkeys (genus Cebus) have evolutionarily converged with humans and chimpanzees in a number of ways, including large brain size, omnivory and extractive foraging, extensive cooperation and coalitionary behaviour and a reliance on social learning. Recent research has documented a richer repertoire of group-specific social conventions in the coalition-prone Cebus capucinus than in any other non-human primate species; these social rituals appear designed to test the strength of social bonds. Such diverse social conventions have not yet been noted in Cebus apella, despite extensive observation at multiple sites. The more robust and widely distributed C. apella is notable for the diversity of its tool-use repertoire, particularly in marginal habitats. Although C. capucinus does not often use tools, white-faced capuchins do specialize in foods requiring multi-step processing, and there are often multiple techniques used by different individuals within the same social group. Immatures preferentially observe foragers who are eating rare foods and hard-to-process foods. Young foragers, especially females, tend to adopt the same foraging techniques as their close associates.     

Capuchin (Cebus apella) Tool Use in a Captive Naturalistic Environment

Captive tufted capuchins are proficient at both tool use and manufacture. However, their capacity to comprehend cause-effect relationships as they relate to tool use is a subject of debate. An ability to conceptualize task requirements in assessing the appropriateness of potential tools would be essential to efficient tool use in the wild. Observations of tool use among free-ranging populations of Cebus are extremely limited, and the importance of this behavior to capuchin feeding ecology is unclear. I tested tufted capuchins' ability to conceive solutions to a probing task in a naturalistic captive setting. Three out of 5 participants demonstrated an ability to consistently make and use tools selected from a wide variety of natural materials within a forest exhibit. Over 98% (N = 140) of the tools that they modified enabled them to successfully acquire food rewards. It is likely that wild Cebus apella shares this ability, and that tool use occurs under a highly specific set of natural conditions.     

Transfer index and mediational learning in tufted capuchins (Cebus apella)

The transfer index (TI) is a discrimination reversal paradigm that requires the achievement of a given prereversal criterion of accuracy. The mediational learning (ML) paradigm is a modification of the TI procedure that features the presentation of three different reversal conditions designed to assess whether prereversal learning is based on purely associative processes or mediated by the use of a strategy (win-stay/lose-shift). These two paradigms have been used with apes and several Old World monkey species, proving to be effective tools for the comparison of species on the basis of their transfer abilities and the nature of their learning processes. However, among New World monkeys, only the squirrel monkey has been tested. Capuchin (Cebusspp.) adaptability and their mastery in using tools have led to controversial interpretations of their cognitive and learning skills. We evaluated their mode of learning and the transfer of learning using the TI and the ML paradigms. We tested four tufted capuchins (Cebus apella)in a WGTA using a variety of stimulus object pairs. The results show that they possess rather good transfer abilities and one subject showed an associative learning mode. None of the subjects showed evidence of learning mediated by a win-stay/lose-shift strategy.     

Using Avida-ED for Teaching and Learning About Evolution in Undergraduate Introductory Biology Courses

Evolution is a complex subject that requires knowledge of basic biological concepts and the ability to connect them across multiple scales of time, space, and biological organization. Avida-ED is a digital evolution educational software environment designed for teaching and learning about evolution and the nature of science in undergraduate biology courses. This study describes our backward design approach to developing an instructional activity using Avida-ED for teaching and learning about evolution in a large-enrollment introductory biology course. Using multiple assessment instruments, we measured student knowledge and understanding of key principles of natural selection before and after instruction on evolution (including the Avida-ED activity). Assessment analysis revealed significant post-instruction learning gains, although certain evolutionary principles (most notably those including genetics concepts, such as the genetic origin of variation) remained particularly difficult for students, even after instruction. Students, however, demonstrated a good grasp of the genetic component of the evolutionary process in the context of a problem on Avida-ED. We propose that: (a) deep understanding of evolution requires complex systems thinking skills, such as connecting concepts across multiple levels of biological organization, and (b) well designed use of Avida-ED holds the potential to help learners build a meaningful and transferable understanding of the evolutionary process. An erratum to this article can be found at     

Hands-on training about overfitting

Overfitting is one of the critical problems in developing models by machine learning. With machine learning becoming an essential technology in computational biology, we must include training about overfitting in all courses that introduce this technology to students and practitioners. We here propose a hands-on training for overfitting that is suitable for introductory level courses and can be carried out on its own or embedded within any data science course. We use workflow-based design of machine learning pipelines, experimentation-based teaching, and hands-on approach that focuses on concepts rather than underlying mathematics. We here detail the data analysis workflows we use in training and motivate them from the viewpoint of teaching goals. Our proposed approach relies on Orange, an open-source data science toolbox that combines data visualization and machine learning, and that is tailored for education in machine learning and explorative data analysis.     

Tool use in Cebus

This paper summarizes early anecdotal information and systematic studies of tool use in capuchin monkeys (Cebus spp.). Tool use in capuchins is neither context specific nor stereotyped. The success of capuchins in using tools and in exploiting a variety of food resources in the wild derives from several factors: their manipulative abilities, interest in external objects and a tendency to explore the environment. In using tools, capuchins are similar to apes and more proficient than other monkey species. A cognitive approach indicates, however, that (in contrast with chimpanzees) they never develop an understanding of the requirements of the tool tasks presented.     

Comparative anatomical analyses of the forearm muscles of Cebus libidinosus (Rylands et al. 2000): manipulatory behavior and tool use

The present study describes the flexor and extensor muscles in Cebus libidinosus' forearm and compares them with those from humans, chimpanzees and baboons. The data is presented in quantitative anatomical indices for similarity. The capuchin forearm muscles showed important similarities with chimpanzees and humans, particularly those that act on thumb motion and allow certain degree of independence from other hand structures, even though their configuration does not enable a true opposable thumb. The characteristics of Cebus' forearm muscles corroborate the evolutionary convergence towards an adaptive behavior (tool use) between Cebus genus and apes.     

Performing Evolution: Role-Play Simulations

By simulating evolution through performance, students become physically, as well as mentally, engaged in thinking about evolutionary concepts. This instructional strategy redirects tension around the subject toward metacognitive reflection. Non-verbal performances like those presented here also avoid the pitfalls of relying on difficult-to-use language. This paper describes a teachable unit including the learning goals and outcomes as well as rubrics to aid assessment. Through two performance-based activities, the unit introduces the fundamental evolutionary concepts that evolution lacks forethought and that natural selection is a sorting process. By reflecting on the performances, students learn other sophisticated evolutionary concepts like hitchhiking, the effects of environmental change, and the extinction of traits. They also become aware of the scientific process, articulating hypotheses about the outcome of the simulations, collecting data, and revising their hypotheses. Discussions and homework about the performances reveal how learning progresses, and detailed rubrics help both instructors and students assess conceptual learning. This unit concludes with the opportunity for students to transfer what they have learned to new concepts: they design new performances to simulate other mechanisms of evolution, such as genetic drift, mutation, and migration.     

Using the Tools at Hand: Manual Laterality and Elementary Technology in Cebus spp. and Pan spp.

Cebus and Pan appear to be a remarkable example of evolutionary convergence in behavioral ecology. We examine their apparently analogous solutions to problems posed by laterality of hand function and elementary technology. We scrutinize appropriate published data in a meta-analysis, focusing on Cebus apella and C. capucinus and on Pan paniscus and P. troglodytes. We compare behavioral data in terms of captive versus wild, and tool use versus non-tool use, but notable gaps exist in the data, especially for bonobos. Cebus and Pan spp. are equivalent tool users in captivity, but chimpanzees are notably more extensively so in nature. For hand preference, captive bonobos and wild and captive chimpanzees show ambipreference for non-tool-use patterns. For both Cebus spp. and Pan spp., there is a tendency for individuals to be committed exclusively to one hand or the other for tool use. The data for laterality of hand function fit consistently into the five-level model proposed by McGrew and Marchant (1996).     

Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli.     

Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients

Many ecological dynamics occur over time-scales that are well beyond the duration of conventional experiments or observations. One useful approach to overcome this problem is extrapolation of temporal dynamics from spatial variation. We review two complementary variants of this approach that have been of late increasingly employed: the use of natural gradients to infer anthropogenic effects and the use of anthropogenic gradients to infer natural dynamics. Recent studies have considered a variety of naturally occurring gradients associated with climate, CO2, disturbance and biodiversity gradients, as well as anthropogenic gradients such as those created by biological invasions, habitat fragmentation and land abandonment. These studies show that natural gradients are useful in predicting long-term consequences of human-induced environmental changes, whereas anthropogenic gradients are helpful in inferring the mechanisms behind natural dynamics because covarying factors are often more clearly understood in anthropogenic gradients than in natural gradients. We classify these studies into several categories, each with different strengths and weaknesses, and outline how the limitations can be overcome by combining the gradient-based approach with other approaches. Overall, studies reviewed here demonstrate that the development of basic ecological concepts and the application of these concepts to environmental problems can be more effective when conducted complementarily than when pursued separately.     

Using contextual and lexical features to restructure and validate the classification of biomedical concepts

Background  

Biomedical ontologies are critical for integration of data from diverse sources and for use by knowledge-based biomedical applications, especially natural language processing as well as associated mining and reasoning systems. The effectiveness of these systems is heavily dependent on the quality of the ontological terms and their classifications. To assist in developing and maintaining the ontologies objectively, we propose automatic approaches to classify and/or validate their semantic categories. In previous work, we developed an approach using contextual syntactic features obtained from a large domain corpus to reclassify and validate concepts of the Unified Medical Language System (UMLS), a comprehensive resource of biomedical terminology. In this paper, we introduce another classification approach based on words of the concept strings and compare it to the contextual syntactic approach.     

Euclidean distance matrix analysis: a coordinate-free approach for comparing biological shapes using landmark data.

For problems of classification and comparison in biological research, the primary focus is on the similarity of forms. A biological form can be conveniently defined as consisting of size and shape. Several approaches for comparing biological shapes using landmark data are available. Lele (1991a) critically discusses these approaches and proposes a new method based on the Euclidean distance matrix representation of the form of an object. The purpose of this paper is to extend this new methodology to the comparison of groups of objects. We develop the statistical versions of various concepts introduced by Lele (1991a) and use them for developing statistical procedures for testing the hypothesis of shape difference between biological forms. We illustrate the use of this method by studying morphological differences between normal children and those affected with Crouzon and Apert syndromes and craniofacial sexual dimorphism in Cebus apella.     

Capuchin monkey (Cebus apella) grips for the use of stone tools

This research examined capuchin monkey (Cebus apella) grips for the use of throwing, nut-cracking, and cutting tools. We provided subjects with stones and apparatus that accommodated the use of stones as tools. Our subjects exhibited five grips, two of which the animals used when force was the primary consideration (power grips) and three of which the animals use when accuracy of sensory judgment and instrumentation was required (precision grips). We believe that the range of contexts in which capuchins use stone tools, combined with the ability of capuchins to employ both power and precision grips as part of their tool repertoire, indicate that Cebus apella can be used to identify grips that facilitated hominid lithic technology. Am J Phys Anthropol 103:131–135, 1997. © 1997 Wiley-Liss, Inc.     

Schistosoma haematobium: experimental infection in capuchin monkey, Cebus apella

South American capuchin monkeys (Cebus apella) have been included in a series of nonhuman primates under evaluation for their potential use as models in a study of the basic biology of Schistosoma haematobium. Emphasis has been given to involvement of the urogenital system, a prominent feature of infection in man. Preliminary observations on Cebus apella with moderate numbers of S. haematobium from Iran showed that there may be serious involvement of the urogenital system with development of pronounced hydronephrosis accompanied by pathobiological alteration of the urinary bladder, ureters, and kidneys. There were heavy deposits of parasite eggs in the major viscera.     

A Communicative Approach to Using Computers for Cultivating Cognitive Skills and Communication in Young Children

An analysis of a child's cognitive activity in the use of computers may be carried out with respect to the child's verbalization of the objective world in the presence of one other person or several people. This approach [1-3] also includes the dialogic nature of learning, and thus differs fundamentally from investigations that examine development only in individual problem solving. In contrast to the approach of Soviet investigators, who stress the role of social situations in the formation of individual concepts in a person, the dominant approach in the USA has, until quite recently, been child-oriented in all areas of learning and in child psychology.     

In situ hybridization of an acetylaminofluorene-modified probe recognized by Z-DNA antibodies in vitro

An in situ hybridization procedure, based on the chemical modification of DNA by acetylaminofluorene (AAF), followed by a specific immunoreaction was used to localize a Z-DNA sequence isolated from the satellite DNA of Cebus appella. The AAF probe is localized on the R-band-positive heterochromatic segments of Cebus chromosomes, which strongly react with Z-DNA antibodies. The use of a nonradioactive single-stranded labeled probe confirms the reliability and the rapidity of immunochemical methods for the detection of DNA sequences on chromosomes.     

Maximizing farm-level uptake and diffusion of biological control innovations in today’s digital era

When anthropologists interviewed Honduran and Nepali smallholders in the mid-1990s, they were told that “Insects are a terrible mistake in God’s creation” and “There’s nothing that kills them, except for insecticides”. Even growers who maintained a close bond with nature were either entirely unaware of natural pest control, or expressed doubt about the actual value of these services on their farm. Farmers’ knowledge, beliefs and attitudes towards pests and natural enemies are of paramount importance to the practice of biological control, but are all too often disregarded. In this study, we conduct a retrospective analysis of the extent to which social science facets have been incorporated into biological control research over the past 25 years. Next, we critically examine various biological control forms, concepts and technologies using a ‘diffusion of innovations’ framework, and identify elements that hamper their diffusion and farm-level uptake. Lastly, we introduce effective observation-based learning strategies, such as farmer field schools to promote biological control, and list how those participatory approaches can be further enriched with information and communication technologies (ICT). Although biological control scientists have made substantial technological progress and generate nearly 1000 papers annually, only a fraction (1.4%) of those address social science or technology transfer aspects. To ease obstacles to enhanced farmer learning about biological control, we describe ways to communicate biological control concepts and technologies for four divergent agricultural knowledge systems (as identified within a matrix built around ‘cultural importance’ and ‘ease of observation’). Furthermore, we describe how biological control innovations suffer a number of notable shortcomings that hamper their farm-level adoption and subsequent diffusion, and point at ways to remediate those by tactical communication campaigns or customized, (ICT-based) adult education programs. Amongst others, we outline how video, smart phones, or tablets can be used to convey key ecological concepts and biocontrol technologies, and facilitate social learning. In today’s digital era, cross-disciplinary science and deliberate multi-stakeholder engagement will provide biocontrol advocates the necessary means to bolster farmer adoption rates, counter-act surging insecticide use, and restore public trust in one of nature’s prime services.