Clara B. Jones

Multimodal Communication by Male Mantled Howler Monkeys (Alouatta palliata) in Sexual Contexts: A Descriptive Analysis

We analyzed continuously sampled focal and ad libitum data of male mantled howler monkeys (Alouatta palliata) observed in random order. Males resided in two groups in a Costa Rican tropical dry forest environment (riparian habitat group: 3 males, 15 females, 402 h observation; deciduous habitat group: 2 males, 8 females, 114 h observation). Samples were limited to sexual contexts, in particular, the 60-min periods before and after each copulation observed within each group for each male. Time samples for each male were distributed equally before and after their own copulations. Before statistical analyses were conducted, data were corrected for differences in time sampled for males within each group. Four types of multimodal signaling were resolved: (1) audiovisual, (2) olfactory-visual, (3) olfactory-visual-tactile and (4) tactile-gustatory. Olfactory and tactile signals were never observed in combination with auditory signals. Consistent with expectation for a Neotropical, arboreal species, audiovisual signals were the most frequently observed type of multimodal communication in both groups (riparian habitat group: n = 139; deciduous habitat group: n = 66). Our evidence strongly suggests that unimodal signals may be combined and recombined to form complex, multimodal signals. Subordinate males in each group were more likely than dominant males to emit audiovisual signals before their own copulations. Male dyads were compared to assess the relative rate of audiovisual signaling by one male before another male’s copulations. On average, the subordinate male of the riparian habitat group exhibited audiovisual signals at a higher rate before his own copulations compared to the rate of audiovisual signaling by his dominant challengers. The same comparisons are not significant for males in the deciduous habitat group. The pattern of male response that we report whereby subordinates emit some complex signals at a higher rate than dominants supports the ‘terminal investment hypothesis’ predicting that organisms should increase reproductive effort with age since, in mantled howlers, age correlates negatively with dominance rank. Additional, qualitative observations suggested that subordinates in both groups were most likely to obtain copulations when they increased rates of complex signaling and/or escalated interactions with their male challengers. Group differences were apparent, however, and we suggest factors that may account for these patterns. We assessed responses by female receivers of complex signals emitted by males in sexual contexts. In general, higher-ranking males are more attractive to females and are more successful at monopolizing them. Findings for other, less frequently displayed, multimodal signals (olfactory-visual, olfactory-visual-tactile and tactile-gustatory) are presented and discussed. We conclude with the suggestion that howlers may be a robust model for the investigation of complex signals in Neotropical primates, including research on functionally referential communication and context-dependent syntax.

Preserving Biodiversity and Ecosystems: Catalyzing Conservation Contagion

The natural world is in a chronic state of crisis and under constant threat of degradation, primarily by anthropogenic factors. In general, current conservation strategies have failed to effect long-range solutions to the rapid loss of biodiversity (Persha et al., 2011). Deforestation continues despite efforts by mainstream (top-down) conservation programs (Persha et al., 2011; Schmitt et al., 2009), and the effectiveness of large-scale protected areas has, at best, a mixed record of success (Brockington et al., 2008; Persha et al., 2011). Scientific disciplines, in particular, ecology and conservation biology, continue to emphasize threats to biodiversity (Schipper et al., 2008), to debate conservation priorities (Brooks et al., 2006), to advance unproven strategies (SSC, 2008), and to offer no more than hypothetical solutions to pressing problems (Milner-Gulland et al., 2010; Turner et al., 2007). The bulk of the scientific community remains tangential to the conservation needs of communities in habitat countries, with a critical lack of input and connectivity between the extensive scientific literature and ground-level practices (Milner-Gulland et al., 2010).

Behavioral Flexibility: Interpretations and Prospects

Phenotypic plasticity represents sets of mechanisms, including behavioral flexibility, of adjustment and adaptation to local conditions that may be components of ontogenetic processes (West-Eberhard, 2003). Slobodkin (1968) and others (Miller, 1956; Slobodkin and Rapoport, 1974; Lerner, 1970; Hochachka and Somero, 1973; Lande, 1980) have proposed a predictive theory whereby natural selection favors different mechanisms within and between species for accomodation to local environmental (abiotic and biotic, including social) variations. These authors suggest that the mechanism(s) favored will be a function of the temporal and/or spatial patterning of environmental changes (e.g., fluctuations in food supply, temperature, or rainfall) relative to the organism’s generation time (T, “environmental grain”). The proposed mechanism(s) may differ with respect to their rates of activation (i.e., relatively flexible to relatively inflexible) and their sensitivities to local conditions (i.e., relatively attentive to relatively inattentive, see Chapter 2).

Hand-Holding by Belizean Black Howler Monkeys: Intentional Communication in a Neotropical Primate

[Crockett and Eisenberg, 1987]), large, arboreal, herbivorous primates of the Neotropics, inhabit societies characterized by reciprocal communication [Carpenter, 1934; Wilson, 1975; Crockett, 1987; Crockett and Eisenberg, 1987; Brockett et al., 2000]. Com-munication among howlers is primarily vocal [Carpenter, 1934; Wilson, 1975; Baldwin and Baldwin, 1976], but little is known about the functions of signals em-ployed by these monkeys. The investigation of intentional communication among New World monkeys is in an early stage compared to these studies in Old World monkeys and apes [Cheney and Seyfarth, 1982; Maestripieri, 1997; Nakamura, 2002]. The purpose of this brief report is to present preliminary data on hand-holding behavior by Beliz-ean black howler monkeys

Are Humans Cooperative Breeders? A Call for Research

Manyattemptshavebeenmadetodocumentandtoclassifyhuman sociosexualsystems,andcurrenttreatmentsconcludethat, thougha ‘‘strange’’taxon (Crespi, 2009), humans are‘‘cooperative breeders’’(Hrdy, 2009). Hrdy devotes an impressive number of pages in an attempt to support the idea that humans are preadapted evolutionarily to allocare (care of young by individuals other than their mothers) and that these behaviors are beneficial in modern times. In cooperatively breeding societies, one or a few dominant females coexist with ‘‘helpers,’’usually daughters or other female kin, who demonstrate reproductive restraint that may be self-imposed or imposed by a dominant breeder, usually a female (e.g., Abbott, Digby, & Saltzman, 2009). Cooperative breeding and eusociality (extreme sociality) are the highest grades of sociality recognized by social biologists. Both of these sociosexual systems are characterized by overlapping generations and subordinate helpers. Eusocial taxa exhibit, in addition, a reproductive division of labor that may, in cases of advanced eusociality found in some social insect taxa, be permanently non-reproductive with individual workers or helpers demonstrating morphological specializations for division of labor. It is generally acknowledged that, among mammals, some species of naked mole rats (Bathyergidae) represent the only known examples of eusociality in the class. However, the idea that humans are eusocial has been proposed by several authors employing femalemenopauseand its consequent sterility (apparently unique to humans and other apes among primates) to support their conceptual models (e.g., Foster & Ratnieks, 2005). These and other authors argue that post-menopausal women gain more genetic benefitsby assisting relatives (especially daughters) in child-rearing than they would by continued selfish reproduction(inclusivefitness),allother thingsbeingequal. Iamnotaware of rigorous empirical tests of this hypothesis for humans, a research program with a high priority for an understanding of sociosexual evolution in Homo sapiens. It will be important to study not only potential benefits, but, also, potential costs (e.g., ‘‘elder abuse’’) for post-menopausal females and possible sexual dimorphisminvulnerability torelatives’exploitationoftheelderly. On the other hand, offspring may sometimes be the victims of violence or other deleterious responses by elder female caretakers. These fields of investigation may yield important qualifications to current assumptions about the advantages to younger kin of interactions with post-reproductive females. It would, in addition, be useful for primatologists, including students of humans, to adopt a classification system for sociosexual behaviors and their evolutionary trajectories in order to permit arrangement of populations or species from solitary to advanced eusocial. Vehrencamp (1979) argued that the evolutionofadvancedsociality inmammals is limitedwhereparental, almostalwaysmaternal, care terminates subsequent toweaning. Inotherwords, in theseconditions, therewouldbenocontext for elaborate helping behaviors to evolve and, indeed, the social architecture of most mammals is solitary. Vehrencamp goes on to point out that cooperative breeding and eusociality have evolved in some mammals (e.g., some rodents, some carnivores, and some primates), arguing convincingly that these evolutionary transitions have arisen via the ‘‘familial route’’ (Solitary?Subsocial? Intermediate subsocial?Eusocial) rather than the ‘‘parasocial route’’ (Solitary?Communal? Quasisocial?Semisocial?Eusocial). Infamilial systems, theIntermediate subsocial stage is characterized by related individuals in a group dividing labor (e.g., defense of a refugium, sharing information about food or other resources) except reproductive divisionof labor thatcharacterizes thefinal, eusocial, stage.Vehrencamp’s (1979) templates, based upon the schema advanced by C. B. Jones (&) Theoretical Phenogroup Project, 22 School Road, Asheville, NC 28806, USA e-mail: theoreticalphenogroup06@yahoo.com

Female Primates as “Energy-Maximizers” in Heterogeneous Regimes

The problem of any sexual organism is the optimization of genotypic and phenotypic benefits, and the problem of the female is to do her best reproductively within the energetic constraints of her local regime. All other things being equal, a female will be selected to invest the largest possible share of her total energy budget into reproductive activities (especially, for female mammals, parenting effort), rather than on growth and survival or mating effort. It is for these reasons that in many environmental conditions it will benefit females to exhibit highly selective tactics and strategies that are not energetically wasteful.

The Costs and Benefits of Behavioral Flexibility to Inclusive Fitness: Dispersal as an Option in Heterogeneous Regimes

The current worldwide biodiversity crisis (Myers et al., 2000; Pimm and Raven, 2000) provides a natural laboratory for the study of behavioral flexibility (Tilman, 1999). Increasing temporal and spatial environmental variability and the effects of anthropogenic factors, in particular, habitat destruction, and subsequent habitat fragmentation and patchiness ( Jones, 1999a; Fukuda, 2004) are well documented for numerous primate species (Cowlishaw and Dunbar, 2000; Jones, 1983b, 1995b, 1996b, 1997c, 1999a; Harcourt et al., 2002; Clarke et al., 2002; Fukuda, 2004). This book relies heavily upon theoretical and empirical work on the causes and consequences of biodiversity from the fields of conservation biology and community ecology in an attempt to formulate and suggest tests of ideas appropriate for research at the individual level of analysis. From an evolutionary perspective, dispersal is of fundamental importance since it may counteract the effects of genetic drift by maintaining the connection between subpopulations and populations, preventing isolation.

Social Cognition and Behavioral Flexibility: Categorical Decision-Making as a Primate Signature

Social cognition may be incorporated within the Triversian (Trivers, 1985) meaning of sociality whereby interindividual interactions are classified as selfish, cooperative, altruistic, or spiteful. Like all social behavior (Frank, 1998; Trivers, 1985), I assume that social cognition has evolved to optimize fitness where the (genetic and/or phenotypic) interests of individuals competing for limiting resources are not equivalent. These interests might be compromised, however, where cognitive responses have been manipulated or exploited so that individuals behave in the interests of others (e.g., as victims of social parasitism; see Frith and Frith, 1999; Whiten and Byrne, 1988; Chapter 3).

Primate Signatures and Behavioral Flexibility in Heterogeneous Regimes

Scientists are trained to generalize, and many primatologists have attempted to characterize those traits diagnostic of the Primate Order (Vaughan, 1978; Eisenberg, 1966, 1981; Fleagle, 1999; Jones, 2001; Kappeler et al., 2003; Lee and Kappeler, 2003). Of course, the traits that one considers significant will often depend upon one’s questions, and the goals and assumptions of research have not been the same in all of these research programs. Thus, although large brain to body ratio and a capacity for learning, in particular, social learning, and cognition are mentioned by many investigators as signatures of primates (e.g., Mazur, 2002; Fragaszy and Perry, 2003a), few of the other traits appear in all schemas (e.g., specializations in dentition or cranial anatomy). This chapter will propose several traits displayed by primates that appear to this author to have received little attention as possible primate signatures and which may facilitate and/or represent behaviorally flexible responses associated with the success of primates in temporally and spatially heterogeneous regimes.

Sociosexual Organization and the Expression of Behavioral Flexibility

Most vertebrate populations are structured, and population structure will be an emergent property of decisions made by individuals concerning where to reside and where to reproduce. Individuals of mammalian species, then, are generally not organized randomly with respect to features of the habitat or to one another (but see Caughley, 1964). Students of social organization seek to explain patterns of interindividual organization within the framework of organismic and evolutionary biology and to identify and measure the causes and effects of population dispersions. For most species of mammals, including primates, the determinants of population distribution and abundance are poorly understood. However, most investigators assume that these patterns are a function of the dispersion and quality of limiting resources (e.g., food, mates), dispersal costs ( Johnson et al., 2003), as well as pressures from predation (Dunbar, 1988; Sterck et al., 1997; Nunn, 2003; also see Smuts et al., 1987).