Abstract: Predictors of male residence patterns in groups of black howler monkeys (Jones et al)

Jones CB, Milanov V, Hager R (2008) Predictors of male residence patterns in groups of black howler monkeys. Journal of Zoology 275: 72-78.

Abstract: Males may share access to fertilizable females (polygynandry) in one environment while, under other conditions, polygynous (one-male or "harem") mating is the norm [in mammals]. However, few studies in mammals have empirically investigated the factors predicting when males will oexist in bisexual reproductive units rather than live in one-male associations with females. We examined patterns of male group membership in a population of black howler monkeys, Alouatta pigra, residing in two habitats (deciduous and riparian of a tropical moist forest environment in Belize, Central America. Using general linear and logistic regression modeling, we evaluated nine variables as possible predictors of male residence patterns (one-male groups or multimale groups). Our results suggest that adult sex ratio and group size are the best predictors of male residence patterns in both habitats. Our findings provide empirical support for theoretical expectations that male reproductive strategies will be a function of habitat-related demographic patterns and the subsequently varying potential of males to monopolize females in heterogeneous regimes. This study may have important implications for our understanding of features of mammalian societies in which males compete directly for access to females.

Summary: An exploratory analysis of developmental plasticity... [CB Jones]

Jones CB (2005) An exploratory analysis of developmental plasticity in Costa Rican mantled howler monkeys (Alouatta palliata palliata Gray). In A. Estrada, PA Garber, MSM Pavelka, LeA Luecke (eds.), New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer, New York.

Summary: The topic of developmental plasticity is fundamentally related to life-history evolution (West-Eberhard 2003), in particular, patterns of survival and reproduction. Jones (1997b) employed matrix analysis (see Alberts & Altmann 2003) of Scott's census data with age structure for mantled howlers at Hacienda La Pacifica to estimate life-history parameters including survivorship, fecundity, and mortality. The suite of life-history traits described by this author (e.g., low survivorship in more than one age class, iteroparity, relatively small reproductive effort) is consistent with the view that mantled howlers, and, possibly other members of the genus, express tactics and strategies minimizing costs to fecundity. Since changes in CC [Chest Circumference] and/or CC:P [Chest Circumference : Pubis Width] are irreversible morphological changes, it is proposed that female mantled howlers are capable of responding to local conditions with mechanisms of developmental plasticity, a within-individual strategy compatible with the life-history strategy of mantled howlers (Meyers & Bull 2002; Table 1; see Ravosa et al. 1993). Further research is required to test alternate hypotheses for the present results (e.g., natural selection [C.P. Groves, pers. comm.; F. Nihout, pers. comm.]) and to examine the possibility that there is a threshold of response to locally stressful conditions in irrigation habitat exhibited by female howlers and manifested as developmental plasticity in CC and CC:P.

The present report is consistent with the program of Stearns et al. (2003: 311) expressed in the following statement: "Alternative explanations for characteristic male and female growth schedules, and the consequences of the patterns seen in each species...all call for investigation across the spectrum of primate social systems." The study of the functional ecology, including physiological ecology and developmental plasticity, of primates is in its early stages (Milton 1998; also see Strier 1992; Ravosa et al. 1993; Crockett 1998; Reader & Laland 2003: 20-21; Jones 2005), investigations which are likely to occupy laboratory and field investigators for many years. This body of research will have important implications on primate and other mammalian development, energetics, life history evolution, and conservation, as it involves an understanding of growth, survival, and reproduction relative to environmental regimes.

References

Alberts SC, Altmann J (2003) Matrix models for primate life history analysis. In PM Kappeler, ME Pereira (eds.), Primate life histories and socioecology. University of Chicago Press, pp 66-102.

Crockett CM (1998) Conservation biology of the genus Alouatta. Int. J. Primatol. 19: 549-578.

Jones CB (2005) Behavioral flexibility in primates: causes and consequences. Springer, New York.

Meyers LA, Bull JJ (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17: 551-557.

Milton K (1998) Physiological ecology of howlers (Alouatta): energetic and digestic considerations and comparison with the Colobinae. Int J Primatol 19: 513-548.

Ravosa MJ, Meyers DM, Glander KE (1993) Relative growth of the limbs and trunk in sifakas: heterochronic, ecological, and functional considerations. Am J Phys Anthropol 92: 499-520.

Reader SM, Laland KN (2003) Animal innovation: an introduction. In SA Reader and KN Laland (eds.), Animal innovation, Oxford University Press, Oxford, pp 3-35.

Stearns SC, Pereira ME, Kappeler PM (2003) Primate life histories and future research. In PM Kappeler, ME Pereira (eds.), Primate life histories and socioecology. University of Chicago Press, pp 301-312.

Strier KB (1992) Ateline adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88: 515-524.

Abstract: Multi-modal communication by male mantled howler monkeys [Jones & Van Cantfort]

Jones CB, Van Cantfort TE (2007) Multimodal communication by male mantled howler monkeys ( Alouatta palliata palliata Gray) in sexual contexts: a descriptive analysis. Folia Primatol 78: 166-185.

Abstract: We analyzed continuously sampled focal and ad libitum data of male mantled howler Cmonkeys (Alouatta palliata palliata Gray) observed in random order. Males resided in two groups in a Costa Rican tropical dry forest environment (riparian habitat group: 3 adult males, 15 adult females, 402 h observation; deciduous habitat group: 2 adult males, 8 adult 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 adult 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.

Abstract: Population structure and group productivity...female socioecology [CB Jones]

Horwich RH, Brockett RC, James RA, Jones CB (November 2001) Population structure and group productivity of the Belizean black howling monkey (Alouatta pigra): implications for female socioecology. Primate Report 61: 47-65.

Abstract: The assembly and architecture of populations are functions of decisions made by individuals for the optimization of lifetime survival and reproductive success. We analyzed the results of 12 longitudinal surveys (209 group counts) of Belizean black howling monkeys (Alouatta pigra) at the Community Baboon Sanctuary (CBS) in an attempt to describe population structure and group productivity over time. Similar to previous reports of black howlers at several sites, modal group size was found to be one adult male and 2 adult females. Group size ranged from 2 to 16 and maximum female group size* was 4 as reported for other species of polygynous Alouatta. Population density ranged from 8.14 - 178.19 individuals per km^2, one of the highest densities ever recorded for A. pigra. Group size was significantly positively correlated with population density, and 52% of the variance in group size was explained by population density. Female group size and number of immatures [J+I+ sub-adults] per group were positively correlated. An analysis of the least squares regression line for female group size and the number of immatures per group found 9 of 12 surveys experiencing density-dependent conditions. Relative reproductive success [RRS], the mean number of immatures : females per female group size, decreased with increasing female group size suggesting that females in larger groups are at a disadvantage due to decreases in survivorship and/or fecundity [i.e., no Allee Effect]. Again, density-dependent conditions appeared to be operating. Our analysis of gains and losses to 19 groups from 1995-1997 suggests that the black howler population at the CBS is at equilibrium or slightly increasing, primarily as a result of recruitment of immatures (infants, juveniles, and/or sub-adults). If female black howlers at the CBS experience density-dependent conditions, they may undergo significant food competition contrary to predictions of the "ecological model" for folivorous primates. The different conditions predicted by the least squares regression analysis (density-dependence, density-independence, or an advantage to large groups [see method used on page 54: "An indirect test of female survivorship and/or fecundity]) may define the domains of selective pressures generating variations in group size as a function of decisions made by individuals optimizing inclusive fitness. These and other findings have important implications for female social relations Alouatta. At present we cannot distinguish between competition for limiting food resources and infanticide as the proximate mechanism [or, both?] limiting female group size in Belizean black howlers and other polygynous howlers.

*Related Reference
Jones CB, Milanov V, Hager R (2008) Predictors of male residence patterns in groups of black howler monkeys. J Zool 275: 72-78.

Relative Reproductive Success... [Methodology]... (CB Jones)

Jones CB (March, 1996) Relative Reproductive Success [RRS] in the mantled howler monkey: implications for conservation. Neotropical Primates 4(1): 21-23.

First Paragraph of Brief Communication: The structure of primate groups is thought to result from the tendency of females to select rich patches of food and that of males to select large aggregations of females (Wittenberger 1980; Emlen & Oring 1977). Because patch richness and the consequent number and quality of females may vary, the relative reproductive success (RRS) of females may also vary over space and time. RRS is a population parameter, since it is one characteristic of demographic or life history traits describing subunits of a species within and between environmental regimes (see Vehrencamp & Bradbury 1984). RRS is important to the field of conservation biology since an increase in the variance of reproductive success in a population reduces effective population size (Primack 1993). Information about RRS facilitates viability analysis of population fluctuations required for recovery from environmental perturbations.

Methods: This report analyzes relative reproductive success (RRS--Method via Sandy Vehrencamp, Cornell University, ~1976) of mantled howler monkeys (Alouatta palliata palliata Gray) in two Central American forests as the mean number of juveniles plus infants (J+I) per female group size per site. This report uses data from several studies...at two research sites where mantled howler monkeys have been studied most intensively....Mantled howler monkeys, large cebids [n.b., now classified Atelidae]....

References
Emlen ST, Oring L (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197: 215-223.
Primack RB (1993) Essentials of conservation biology. Sinauer Associates, Sunderland, MA.
Vehrencamp SL, Bradbury JW (1984) Mating systems and ecology. In Behavioural ecology: an evolutionary approach. JR Krebs, NB Davies (eds.). pp. 251-278. Sinauer Associates, Inc., Sunderland, MA.
Wittenberger JF (1980) Group size and polygyny in social mammals. Am Nat. 115: 197-222.

Abstract: Ethology, neuroethology, and evolvability in vertebrates... (CB Jones)

Jones CB (February, 2008) Ethology, neuroethology, and evolvability in vertebrates: a brief review and prospectus. Primate Report 75: 41-61.

Abstract: The implications of recent developments in cellular and developmental biology are discussed for vertebrate ethology, describing behavior as neuromuscular elements with the potential to generate non-lethal phenotypic novelty induced by environmental stimuli (evolvability). I present a modified schema of a recent model for the origin of adaptive phenotypic novelties. Behavioral accommodation is hypothesized to lead to genetic accommodation if recurrence of environmental effects upon biochemical pathways of novel genetically correlated neuromuscular elements enhances survival and/or reproduction, I review, discuss, and interpret findings which have been implicated in neural plasticity and subsequent reorganization of the phenotype (e.g., "trial-and-error" learning), emphasizing, in particular, the importance of hypervariable exploratory systems. It is suggested that hypervariable neuromuscular elements and subsequent phenotypic plasticity may be induced by long-term potentiation (LTP), potentially deconstraining conserved action patterns and exposing novel patterns of response to selection. The idea that the phenotype is a heterogeneous landscape of neuromuscular elements varying in function from selfish, including parasitic, to mutualistic is proposed, and I suggest that conflict may be ubiquitous, enhancing the potential for deconstraint. A simple theoretical treatment is applied to my proposal that semi-autonomous, antagonistic transposable behavioral elements (TBE) may parasitize one another within and between individuals, inducing hypervariability. I suggest topics for future research, in particular, the role of environmental stressors as inducers of hypervariability and evolutionary adaptability.

Background Reference
Kirschner M, Gerhart J (1998) Evolvability. Proc. Natl. Acad. Sci., USA 95: 8420-8427.

Abstract: Allouatta palliata politics... [CB Jones]

Jones CB (April, 2000) Alouatta palliata politics: Empirical and theoretical aspects of power. Primate Report 56: 3-21.

Abstract: Social scientists have studied social influence, in particular, aspects of power, for more than 50 years. Social influence in two groups of the mantled howling monkey (Alouatta palliata palliata Gray) was investigated. Dyadic aggressive interactions were observed 131 times in 516 h of observation. Ritualized aggression (the "branch-break" display), primarily exhibited by males, accounted for 40% of the observed aggression, while fighting and chasing comprised the remainder. Females exhibited fighting proportionately more than males, but the sexes were equally likely to chase. No aggression was observed between males in the 2-male deciduous forest group. A class (socioeconomic) effect was noted in dyadic aggressive interactions among females since aggressors and victims were usually of similar rank. Females may "disrupt" one another's sexual activities, suggesting that female-female competition is intense. There was little evidence for female bonding. Male-female aggression occurred infrequently, almost always in sexual contexts. Females often used the submissive "bared-teeth display" to rebuff males and appear to be significantly "emancipated" from male control. Aggression by adults toward immatures was rare. High-ranking individuals were observed to harass low-ranking individuals, the primary tactic of group expulsion in both sexes. Males were observed to intervene in the aggressive interactions of females, a form of "policing." Coalitions were observed in the 3-male riparian forest group within both sexes and, for females, appeared to be opportunistic. Post-conflict behavior was analyzed to test the hypothesis that submissive behaviors are expressed more frequently after conflict. No significant differences in the exhibition of submissive behavior occurred post-conflict compared with matched controls. Specific behavior patterns occurred more frequently during post-conflict or matched-control periods, however. In particular, "approach" and "vocalize" were more frequent post-conflict, the latter possibly representing "reconciliation" to repair or to stabilize relationships. The lowest-ranking male in the three-male riparian forest group was experimentally translocated to assess the effects of changes in proximity as a function of male identity and dominance rank. The presence or absence of individuals appeared to affect competitive relations among males. French & Raven's (1959) "bases of power" were identified in A. palliata, but mechanisms of social influence are not necessarily "cognitive-based" as they may be for chimpanzees and humans. French & Raven's paradigm may provide a useful framework for comparative studies.

"Power is a general matrix of force relations at a given time, in a given society." Dreyfus & Rabinow, 1982, p 186

References
Dreyfus JL, Rabinow P (1982) Michel Foucault: beyond structuralism and hermeneutics (2nd edition). University of Chicago Press, Chicago, IL, USA..

French, Jr., JRP, Raven, B (1959) The bases of power. In: Cartwright D (ed.). Studies in social power. Institute for Social Research, Ann Arbor, MI, USA.

Abstract: The number of adult females in groups of polygynous howling monkeys... (CB Jones)

Jones CB (January, 2004) The number of adult females in groups of polygynous howler monkeys (Alouatta spp.): theoretical inferences. Primate Report 68: 7-25.

Abstract: Several reports have documented that adult female group size in polygynous howler monkeys (Alouatta spp.) rarely exceeds 4. This paper evaluates three schemas for the interpretation of this phenomenon: (1) a simple game theoretical model; (2) the resource dispersion hypothesis; and, (3) certain models of reproductive skew. Similarities among these schemas are noted, and their possible utility in explaining differences between the typically polygynandrous A. palliata and typically polygynous species of the genus is discussed. Suggestions for future research are proposed, including, data required to test each schema. 

Abstract: Life history patterns of howler monkeys in a time-varying environment. CB Jones

Jones CB (1997) Life-history patterns of howler monkeys in a time-varying environment. Biol. Primatol. Lat. 6(1): 1-8.

Abstract: This report examines the relationship between life-history characteristics and environmental predictability for mantled howler monkeys (Alouatta palliata palliata Gray) at Hacienda La Paccifica, Guanacaste Province, Costa Rica. A census with age structure was employed to estimate life-history parameters [calculations of life table after Wilson & Bossert, 1971] including survivorship, fecundity, and mortality, [& generation time]. A time-series analysis of yearly rainfall at La Pacifica was conducted to test inferences from life-history theory whereby variations in mortality across the lifespan [across age stages] are a function of environmental predictability. La Pacifica was found to be a relatively predictable environment, and, consistent with theory, howlers exhibit life-history traits expected for their regime. These include low survivorship during more than one age class, iteroparity, a relatively small reproductive effort, a single young per litter, relatively few young across a lifetime, and relatively long lifespan. The predictable environment of howlers at La Pacifica appears to favor adult over juvenile (including infant) survival, and howler life history is consistent with that for other large mammalian herbivores whose females may time reproductive investment to reduce the [deleterious] effects of environmental heterogeneity ("bet-hedging"). [A moving average model of the rainfall data is provided in the paper.]

Reference
Wilson EO, Bossert WH (1971) A primer of population biology. Sinauer Associates, Stamford, CT.