The Next Direction for Primatology? A Commentary on Setchell (2013)

Primatologists were asked to submit their “ideas for the Big Questions that remain unanswered in Primatology” and, from this, Setchell (2013) grouped the 170 responses into 11 broad themes. This exercise created a valuable tool that can help primatologists identify both the “missing gaps” and current broad overarching themes within our field. In this commentary, we offer our perspective on the methodology and results of this survey. By considering the 11 themes more holistically, primatologists can more easily address a broader range of questions, methods, and outcomes for their research endeavors and conservation efforts. Ultimately, the results of this survey should enable researchers and policymakers to recognize gaps in our knowledge and plan how to proceed with new research initiatives and funding applications. The identified themes should also provide a reference point for new avenues of investigation, and we are hopeful that this list can encourage interdisciplinary research if primatologists consider the overlaps across the themes. However, as Setchell noted, as some key areas of research were omitted from the list, the 11 themes should be used as a tool for guidance in expanding our research horizons and not as a template for the minimum of what is required.     

Place,Practice and Primatology: Clarence Ray Carpenter,Primate Communication and the Development of Field Methodology, 1931–1945

Place, practice and status have played significant and interacting roles in the complex history of primatology during the early to mid-twentieth century. This paper demonstrates that, within the emerging discipline of primatology, the field was understood as an essential supplement to laboratory work. Founders argued that only in the field could primates be studied in interaction with their natural social group and environment. Such field studies of primate behavior required the development of existing and new field techniques. The practices and sites developed by American primatologist Clarence Ray Carpenter were used to demonstrate that scientific standards could be successfully applied to the study of primates in the field. In an environment in which many field biologists fought for higher scientific status, Carpenter gradually adopted increasingly interventionist techniques. These techniques raised epistemological problems for studies whose value rested on the naturalness of the behaviors observed. Thus, issues of status shaped field practices and subsequently altered Carpenter’s criteria for what constituted natural primate behavior. This article is part of a doctoral dissertation (in progress). This research was supported in part by a Doctoral Dissertation Research Grant and Doctoral Dissertation Fellowship from the University of Minnesota. Georgina (Hoptroff) Montgomery presented earlier versions of this paper at the ISHPSSB conference held in Vienna in July 2003 and at the HSS conference in Boston in November 2003.     

Researchers' ethical concerns regarding habituating wild-nonhuman primates and perceived ethical duties to their subjects: Results of an online survey

While the process of habituation is essential for researchers to observe primates in their natural habitats, ethical dilemmas may arise from its consequences. We collected data from 286 participants via an online survey to investigate: (a) how primatologists perceive their ethical duties toward their subjects; (b) the extent to which primatologists are concerned about the potential ethical consequences of habituation; and (c) the methods primatologists use to reduce potential harms caused by habituation. Overall, primatologists felt an extremely strong duty to mitigate harms that they may cause (e.g., to not stress individuals during observation, treat injuries, and reunite separated individuals) and expressed very high concern for habituation's potential to increase the vulnerability of their subjects to poaching and disease transfer. Ratings for those items were so high that they could not be included in subsequent exploratory factor analyses that were designed to reveal constructs underlying respondents’ ratings of their ethical duties and concerns. Factor analysis of ratings of ethical duties revealed that primatologists reported a strong duty to mitigate harms caused by other humans and a lower perceived duty to mitigate naturally occurring harmful events. Factor analysis on ethical concern ratings revealed that respondents were concerned about harms during the habituation process, the presence of unhabituated behavior after habituation had been established, and indirect harms of habituation. Concerns for unhabituated behavior and indirect harms were rated slightly higher than concern for harms during the habituation process. To mitigate potential harms, primatologists primarily reported engaging in strategies to reduce stress in their subjects. Our findings reveal a disconnect between primatologists' ratings of their ethical concerns and their reported mitigation practices that may, in part, stem from gaps in knowledge about the true impacts of habituation. We suggest areas of discussion and research in the field necessary to address those gaps.     

Explanatory unification and natural selection explanations

The debate between the dynamical and the statistical interpretations of natural selection is centred on the question of whether all explanations that employ the concepts of natural selection and drift are reducible to causal explanations. The proponents of the statistical interpretation answer negatively, but insist on the fact that selection/drift arguments are explanatory. However, they remain unclear on where the explanatory power comes from. The proponents of the dynamical interpretation answer positively and try to reduce selection/drift arguments to some of the most prominent accounts of causal explanation. In turn, they face the criticism raised by statisticalists that current accounts of causation have to be violated in some of their core conditions or otherwise used in a very loose manner in order to account for selection/drift explanations. We propose a reconciliation of both interpretations by conveying evolutionary explanations within the unificationist model of scientific explanation. Therefore, we argue that the explanatory power in natural selection arguments is a result of successful unification of individual- and population-level facts. A short case study based on research on sympatric speciation will be presented as an example of how population- and individual-level facts are unified to explain the morphological mosaic of bill shape in island scrub jays (Aphelocoma insularis).     

Variability Is Not the Villain: Finding Patterns in Complex Natural Images

Everyone needs strong observational skills to solve challenging problems and make informed decisions. However, many students expect to find exact answers to their questions by using the internet and do not understand the role of uncertainty, especially in decision making and scientific research. Humans and other animals choose among many options by using information about their environment. During this activity, students use their observational skills to analyze data from images of grass shrimp and a highly variable salt-marsh habitat as case studies for prioritizing different pieces of information. They gain an increased appreciation of natural variability and learn to build a consensus in a scenario that has no correct answer.     

An academic genealogy on the history of American field primatologists

In this paper, we present the academic genealogy of American field primatologists. The genealogy has been compiled to formally document the historical record of this young field. Data have been collected from three main sources: 1) e-mail surveys, 2) library and Internet research, and 3) verbal communication through forums such as American Association of Physical Anthropology meetings. Lineages of primatologists have been graphically displayed using Microsoft Visio. As of September 2005, 672 names and 239 affiliated universities, organizations and institutions have been recorded in 19 lineages. Five hundred and thirty-eight of the 672 names, 80.1%, are field primatologists. The Hooton/Washburn lineage is the largest; 60.6% of the recorded field primatologists are linked to this lineage. In addition, four of the five professors who have mentored a comparable number of field primatologists at American universities since Washburn are linked to the Hooton/Washburn lineage; and the school where Washburn mentored a majority of his students, UC-Berkeley, continues to have the highest overall graduation record for this subdiscipline. However, the field of primatology has been diversifying since the 1960s, and different universities are now responsible for graduating a substantial number of primatologists. We conclude that while the Hooton/Washburn lineage has remained remarkably homogenous in its anthropological focus, the field is also becoming increasingly enriched by primatologists who have had training in fields such as zoology, psychology, and ecology both in the United States and abroad.     

Methods in Primate Nutritional Ecology: A User’s Guide

An important goal of primatology is to identify the ecological factors that affect primate abundance, diversity, demography, and social behavior. Understanding the nutritional needs of primates is central to understanding primate ecology because adequate nutrition is a prerequisite for successful reproduction. Here, we review nutritional methods and provide practical guidelines to measure nutrient intake by primates in field settings. We begin with an assessment of how to estimate food intake by primates using behavioral observations. We then describe how to collect, prepare, and preserve food samples. Finally, we suggest appropriate nutritional assays for estimating diet nutritional quality and point to the merits and limitations of each. We hope this review will inspire primatologists to use nutritional ecology to answer many unresolved questions in primatology.     

Can the site conditions required for successful natural regeneration of juniper (Juniperus communis L.) be determined from a single species survey?

Background: Ecological surveys often aim to inform biodiversity conservation policy and practice. Survey types differ; all require clear aims and good design. A survey in Scotland was carried out to measure the distribution and health of juniper (Juniperus communis) and potential for its natural regeneration.

Aims: Explore if one-off national surveys can inform conservation action by examining, as an example, the Scottish juniper data set to: (1) determine site conditions favourable for juniper regeneration, (2) provide recommendations for site management for regeneration.

Methods: Associations between site conditions and juniper occurrence were investigated with principal component analysis (PCA) and using species distribution modelling (SDM). To identify changes in site conditions over time, we compared degree of site suitability for natural regeneration (PCA distance) and population age structure.

Results: Twenty-one per cent of the sites showed juniper regeneration. Compared to all juniper sites, conditions at regenerating sites were different (e.g. climatically wetter, lower site fertility). Change over time in conditions was suggested by patterns in population age structure.

Conclusions: Following the establishment of a juniper population, site conditions may change, becoming unsuitable for natural regeneration. Historical site information to confirm this is lacking. We cannot answer fundamental questions about the causal mechanisms of the natural regeneration of juniper and question whether one-off survey data can inform conservation management.     

Searching for the origins of musicality across species

In the introduction to this theme issue, Honing et al. suggest that the origins of musicality—the capacity that makes it possible for us to perceive, appreciate and produce music—can be pursued productively by searching for components of musicality in other species. Recent studies have highlighted that the behavioural relevance of stimuli to animals and the relation of experimental procedures to their natural behaviour can have a large impact on the type of results that can be obtained for a given species. Through reviewing laboratory findings on animal auditory perception and behaviour, as well as relevant findings on natural behaviour, we provide evidence that both traditional laboratory studies and studies relating to natural behaviour are needed to answer the problem of musicality. Traditional laboratory studies use synthetic stimuli that provide more control than more naturalistic studies, and are in many ways suitable to test the perceptual abilities of animals. However, naturalistic studies are essential to inform us as to what might constitute relevant stimuli and parameters to test with laboratory studies, or why we may or may not expect certain stimulus manipulations to be relevant. These two approaches are both vital in the comparative study of musicality.     

Seriation in paleontological data using markov chain Monte Carlo methods

Given a collection of fossil sites with data about the taxa that occur in each site, the task in biochronology is to find good estimates for the ages or ordering of sites. We describe a full probabilistic model for fossil data. The parameters of the model are natural: the ordering of the sites, the origination and extinction times for each taxon, and the probabilities of different types of errors. We show that the posterior distributions of these parameters can be estimated reliably by using Markov chain Monte Carlo techniques. The posterior distributions of the model parameters can be used to answer many different questions about the data, including seriation (finding the best ordering of the sites) and outlier detection. We demonstrate the usefulness of the model and estimation method on synthetic data and on real data on large late Cenozoic mammals. As an example, for the sites with large number of occurrences of common genera, our methods give orderings, whose correlation with geochronologic ages is 0.95.     

Large net cage for captive breeding and behavioural studies of damselfly Lestes sponsa (Hansemann, 1823) (Odonata: Lestidae): submerged oviposition as a model behaviour

Odonata have a strong potential as model organisms for testing ecological and evolutionary hypotheses because of their short life history, relative ease and cost-effectiveness of care. Unfortunately, very few studies have examined how to create a semi-natural environment for odonates, limiting the biological validity of laboratory manipulation. To better study odonate life cycle and behaviour under controlled conditions, we designed a large net cage that imitated the natural terrestrial as well as aquatic habitat of the damselfly Lestes sponsa (Hansemann, 1823). This species is thought to be capable of submerged oviposition, an unusual behaviour in odonates. We compared multiple variables across natural conditions and the net cage. We demonstrated that between-year variability under natural conditions was generally greater than variability between natural and artificial environments. Overall, semi-natural conditions did not substantially change the L. sponsa life cycle (including the unique behaviour of submerged oviposition), suggesting that results from the net cage are likely generalisable to the field.     

Criteria for release of genetically-improved phytoseiids: an examination of the risks associated with release of biological control agents

Biological control of agricultural pests by phytoseiid predators has been achieved through classical introductions, conservation of indigenous and established foreign species, and augmentation of both introduced and indigenous species. Laboratory selection of phytoseiids has produced several strains that have been mass reared and released for pest management programs in glasshouses and agricultural cropping systems. Concerns over risks of classical biological control have developed recently. The development of recombinant DNA (rDNA) techniques for the genetic manipulation of crops and microorganisms also has inaugurated a debate on the safety of releasing transgenic organisms into the environment. This debate will extend to the release of phytoseiids that have been manipulated with rDNA techniques. Risks associated with releasing phytoseiids for augmentation or classical biological control programs are minimal and the benefits are great. Research initiated to answer questions about the risks of releasing transgenic phytoseiids into the environment provides opportunities to expand our understanding of the ecological impact of phytoseiids in agricultural and natural environments and could lead to improved pest management tactics.     

Increasing the Understanding of Plant Invasions in Southern South America: First Symposium on Alien Plant Invasions in Chile

The first symposium on Alien Plant Invasions in Chile was held in southern Chile in November of 2002. Chile represents an interesting setting to study biological invasions because of its long history of introductions, and its high rate of endemisms that makes it more prone to invasions. However, little is known about plant invasions in Chile and the country lacks a clear policy on alien species. The speakers at the symposium discussed their research on several aspects of alien plant invasions in southern Chile and Argentina. They also elaborated a list of future challenges of plant invasion ecology for the area. The package of recommendations may be useful for other developing countries with similar state of knowledge of their flora and similar environmental and economic issues. We expect that this type of meeting will help to stimulate the scientific debate about invasion ecology and the development of coordinated research to answer local questions, while contributing to find generalities in plant invasion patterns and processes.     

Modelling density-dependent fish shoal distributions in the laboratory and field

Density-dependent variables have long been established as an important area of ecological research, but the effects of the local density of conspecifics on grouping behaviour are less well-studied. We compared the influence of the density of conspecifics on the shoal size distribution of killifish, Fundulus diaphanus , in the laboratory and the field. In both environments we observed an increase in shoal size and shoal number with the density of individuals present. The increase in shoal size was markedly steeper in the field than in the laboratory, but direct comparison of the two was complicated by the fact that the absolute numbers of fish present at the field site were considerably higher than those used in the laboratory trials. We developed an individual-based model that was first used as a null model of shoal formation (defined by proximity to others) in fish with no shoaling tendency over the same range of densities used in the laboratory. Group size increased much more rapidly with increasing density in the laboratory than predicted by the null model. When we incorporated shoaling behaviour into our model, the laboratory results could be reproduced with high accuracy. However, when extrapolated to match conditions in the field, the model predicted smaller, more numerous shoals than were actually observed. We suggest this is due to heterogeneity of the field environment because fish were found to be highly aggregated in certain areas of our field site. The predictive power of laboratory studies for the field is discussed with regards to using individual-based modelling as a tool for deriving such predictions.     

Multidisciplinarity in Microbiome Research: A Challenge and Opportunity to Rethink Causation,Variability, and Scale

This essay, written by a biologist, a microbial ecologist, a biological anthropologist, and an anthropologist‐historian, examines tensions and translations in microbiome research on animals in the laboratory and field. The authors trace how research questions and findings in the laboratory are extrapolated into the field and vice versa, and the shifting evidentiary standards that these research settings require. Showing how complexities of microbiomes challenge traditional standards of causation, the authors contend that these challenges require new approaches to inferences used in ecology, anthropology, and history. As social scientists incorporate investigations of microbial life into their human studies, microbiome researchers venture into field settings to develop mechanistic understandings about the functions of complex microbial communities. These efforts generate new possibilities for cross‐fertilizations and inference frameworks to interpret microbiome findings. Microbiome research should integrate multiple scales, levels of variability, and other disciplinary approaches to tackle questions spanning conditions from the laboratory to the field.     

In vivo biodistribution of stem cells using molecular nuclear medicine imaging

Studies on stem cell are rapidly developing since these cells have great therapeutic potential for numerous diseases and has generated much promise as well as confusion due to contradictory results. Major questions in this research field have been raised as to how and in which numbers stem cells home to target tissues after administration, whether the cells engraft and differentiate, and what their long-term fate is. To answer these questions, reliable in vivo tracking techniques are essential. In vivo molecular imaging techniques using magnetic resonance imaging, bioluminescence, and scintigraphy have been applied for this purpose in experimental studies. The aim of this review is to discuss various radiolabeling techniques for early stem cell tracking, the need for validation of viability and performance of the cells after labeling, and the routes of administration in experimental animal models. In addition, we evaluate current problems and directions related to stem cell tracking using radiolabels, including a possible role for their clinical implementation.     

Fecal steroid research in the field and laboratory: improved methods for storage, transport, processing, and analysis

Since the pioneering paper "Measurement of Excreted Steroids in Macaca nemestrina" [Risler et al., American Journal of Primatology 12:91-100, 1987] was first published, field primatologists have been using fecal extraction techniques to examine adrenal and gonadal hormones. These techniques have allowed investigators to determine reproductive conditions in wild primates without causing any disruption to the populations. Over the years, many techniques have been developed to improve the ease of analysis, transportation, and purification. More of the processing can now be done in the field. This paper describes the methodology developed or adapted at the Wisconsin National Primate Research Center, and the factors involved in preparing fecal samples for steroid analysis. We provide information on the steps involved in extracting and purifying steroids from feces for measurement. The latest methods include field processing of samples, such as drying collected material or separating steroids from the fecal material by solid phase extraction (SPE). How samples are processed in the field determines the requirements for international transportation and the methods used in the laboratory. The pros and cons of the different processing methods are discussed. We also report on recent advances in laboratory quantification, with implications for steroid isolation prior to analysis. The different processes involved in isolating and measuring fecal steroids discussed here will enable investigators to understand the components necessary to ensure accurate and reliable results.     

Changes in the colour of light cue circadian activity

The discovery of melanopsin, the non-visual opsin present in intrinsically photosensitive retinal ganglion cells (ipRGCs), has created great excitement in the field of circadian biology. Now, researchers have emphasized melanopsin as the main photopigment governing circadian activity in vertebrates. Circadian biologists have tested this idea under standard laboratory, 12h Light: 12h Dark, lighting conditions that lack the dramatic daily colour changes of natural skylight. Here we used a stimulus paradigm in which the colour of the illumination changed throughout the day, thus mimicking natural skylight, but luminance, sensed intrinsically by melanopsin containing ganglion cells, was kept constant. We show in two species of cichlid, Aequidens pulcher and Labeotropheus fuelleborni, that changes in light colour, not intensity, are the primary determinants of natural circadian activity. Moreover, opponent-cone photoreceptor inputs to ipRGCs mediate the sensation of wavelength change, and not the intrinsic photopigment, melanopsin. These results have implications for understanding the evolutionary biology of non-visual photosensory pathways and answer long-standing questions about the nature and distribution of photopigments in organisms, including providing a solution to the mystery of why nocturnal animals routinely have mutations that interrupt the function of their short wavelength sensitive photopigment gene.