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: 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: 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.

Alouatta [howler monkeys] spp: unstable "temporal division-of-labor" [Clara B. Jones, 1996]

Jones CB (June, 1996) Temporal Division-of-Labor In A Primate: Age-Dependent Foraging Behavior. Neotropical Primates 4(2): 50-53. [with minor edits from the original]

Introduction
Division of labor based on age or size ["polyethism"] may reflect the reproductive condition of individuals in social groups. In 1967, West proposed the general hypothesis that hierarchical relations may be advantageous to both dominants and subordinates and that individuals of low rank may be inferior reproductives who benefit genetically from associations with and contributions to reproductively superior individuals. Since increasing age or size eventually entails decreasing reproductive value (Vx), several authors have noted that the display of social behavior, such as foraging behavior that benefits all members of a group, especially kin, should increase with age as the benefits from individual (selfish) reproduction decline (e.g., West-Eberhard 1975; Hrdy & Hrdy 1996). As individual reproductive value decreases, benefits (genetic or other) from assisting the reproduction of conspecifics (social behavior [cooperation, altruism as per W.D. Hamilton 1964]) may increase because costs (genetic or other [including, delayed costs or benefits] of social behavior) decrease with decreased benefits from individual reproduction. In order to test this hypothesis, I studied the relationship between adult female age, dominance rank, reproductive value, and social foraging behavior (food search and pursuit) for adult female mantled howler monkeys (Alouatta palliata Gray). [Author's note, 1/20/2020: "Temporal division-of-labor" (TDL) may, also, be termed, "age-polyethism" or "primitive" (totipotent) eusociality or Totipotent Eusociality (TE); see blogpost on General Mammalian Patterns, #28]

Subjects and Methods
During an extended period of study at Hacienda La Pacifica, Canas, Guanacaste, Costa Rica, I studied two marked, aged groups of mantled howler monkeys in two tropical dry forest habitats [Riparian, Group 5, and Deciduous, Group 12: see Jones 1980, Table 1]. For this species [and others of the genus], age and dominance rank are negatively correlated [Jones 1978, Jones 1980].

Social foraging was operationally defined as the behavioral series: feed-rest-move [at least 100 m]-feed, by a unit of more than three adults. These criteria were adopted in order to standardize measurement and to eliminate periods of food search within unusually large patches and by consort pairs. I identified which females in the primary study groups initiated foraging sequences and analyzed these observations by age.

My null hypothesis held that the frequency of foraging by females of any age class would be proportional to the total number of females who foraged in an age class. Two of the 15 [adult] females in one group [both young adults--Riparian Habitat Group 5] were never observed to direct foraging sequences and are excluded from analysis. Three [adult] females were aged on the basis of physical and behavioral traits other than tooth wear, and assignment to age classes for these females was made independent of the present analysis. Two of these females were observed from sub-adult through adult growth and classified as young adults; a third [adult] female, classified as middle-aged, was the mother of a sub-adult and a juvenile offspring, a highly unlikely combination for any other age class [see Glander 1980]. In my analysis of the second group [eight adult females--Deciduous Habitat Group 12], two young adult immigrant females were never observed to forage socially and were excluded from analysis. The pattern of results reported here would remain unaffected by alternative treatments of the raw data.

A monthly foraging rate for each forager was computed by dividing the frequency of foraging by the female's number of months resident in a group, a period of time varying from 10-14 months since some females emigrated during the study. These rates were compared with a female's age class, on the one hand, and dominance rank, on the other, to assess the relationship between the display of social foraging behavior and rank, and reproductive value [Vx, for her age class, (computed from) population data in Malmgren 1979, Table 23; equation after Wilson & Bossert 1971; c.f. Jones 1997] where relative contribution to future generations of an individual of a given age is quantified.

Results and Discussion
Table 1 [below--scroll down] presents the results of my analysis for the first group [Group 5] of foraging frequency as a function of female age, including, expected frequencies, and Chi Square. Computing "goodness of fit" led to an unequivocal rejection of the null hypothesis [P <- 0.001, X2= 107.64, df= 3]. Thus, old age and foraging frequency are significantly related. Young adult females initiate foraging significantly less than expected on the basis of their numbers [in Group 5: P <- 0.001], suggesting that such individuals are relatively "selfish" or are conserving time [T] and energy [E], possibly for reproduction and/or competition. Table 1 also shows that the middle-aged to old female foraged more than expected by chance [P <- 0.01], and this female succeeded the oldest and lowest-ranking female as the most frequent [social] forager when the old female emigrated in 1977 [personal observation*].

Additional observations support the reliability of the above patterns. The oldest female in the second group [Group 12] foraged more frequently than any other adult female [P <- 0.001, X2= 17.29, df= 2; c.f. Jones 1998]. Similarly, the relationship between foraging rate and age class [Fig. 1] yields a significant positive correlation [rs= +0.629, P <- 0.05]. Related to this, the correlation between foraging rate and dominance rank [Fig. 2] is significant but negative [i.e., the higher the foraging rate, the lower the dominance rank, rs= -0.63, P <- 0.05]. Thus, the initiation of [social] foraging is significantly associated with female age and dominance rank.

It was hypothesized above that the expression of social behavior would increase with increasing age since reproductive value [Vx, Fig. 3] decreases with age and with it the benefits from selfish reproduction [i.e., adult females have less to lose and more to gain in fitness as they age]. Figure 3 shows the reproductive value curve for the population of mantled howler monkeys at Hacienda La Pacifica [after Jones 1997]. Comparing Fig. 3 with Figs. 1 and 2, consistent with expectation, a strong negative association appears to exist between reproductive value and rate of foraging. Reproductive value in the four adult age classes is negatively, and significantly correlated with social foraging rate/month [rs= -0.95, P <- 0.02]. These results support the view that increasing age or size eventually entails decreasing reproductive value and that the display of social behavior should increase with age as the benefits from individual [selfish] reproduction decline.

What features of the howlers' environment might favor temporal division-of-labor? On 52 occasions, I was able to record the specific resource upon which foraging sequences terminated. Forty-four [85%] of these sequences terminated on ephemeral food [i.e., fruit, flowers, or new leaves: see Jones 1996], while eight [15%] sequences terminated with feeding on mature leaves [P <- 0.001, X2= 49, df= 1]. Thus, the initiation of social foraging sequences appears to be associated with food, the local distribution of which is temporally uncertain; new leaves, flowers, and fruit. The old female initiated 21 of the 52 [foraging] bouts, 20 of these for ephemeral food [c.f. Jones 1998].

An old female's presumed experience with the mosaic of her home range might enhance her efficiency as a forager so that her foraging activity may yield an energetic and nutritional gain to other group members. Temporal uncertainty of preferred food resources [see Jones 1996] may favor individuals that are the beneficiaries of the foraging activity of others, particularly, kin, when reproductive value is low. Division-of-labor through differential social roles may be a function of relative reproductive value, and behavioral roles may be understood within the context of life history patterns. [------>across Social Mammals** & other Social Vertebrates**? across Social Animals**?].

Acknowledgments
I appreciate the comments of R.C. Lewontin, E.O. Wilson, M.J. West-Eberhard, I.S. Bernstein, W.C. Dilger, and K.E. Weber on an earlier draft of this note. I thank the W. Hagnauer family for permission to work on their property, Hacienda La Pacifica, and for logistic assistance. My gratitude to Norman J. Scott, Jr. [USFWS], for expert introductions to the conduct of fieldwork and for imparting a variety of skills, is immeasurable. The work was supported by grants from the National Fellowships Fund and the National Research Council.

Clara B. Jones, Institute of Animal Behavior, Rutgers University-Newark, 101 Warren Street, Newark, New Jersey 07102, U.S.A.

References
Glander KE [1980] Reproduction and population growth in free-ranging mantled howling monkeys. Am J Phys Anthropol 53: 25-36.
Hamilton WD [1964] The genetical theory of social behavior. J Theor Biol 7: 1-52.
Hrdy SB, Hrdy DB [1976] Hierarchical relations mong female hanuman langurs (Primates: Colobinae, Presbytis entellus]. Science 197: 913-915.
Jones CB [1978] Aspects of reproduction in the mantled howler monkey, Alouatta palliata Gray. Ph.D. Dissertation, Cornell University, Ithaca, NY.
Jones CB [1980] The functions of status in the mantled howler monkey, Alouatta palliata Gray: intraspecific competition for group membershi in a folivorous Neotropical primate. Primates 21: 389-405.
Jones CB [December, 1996] Predictability of plant food resources for mantled howler monkeys at Hacienda La Pacifica, Costa Rica: Glander's dissertation revisited. Neotropical Primates 4(4): 147-149.
Jones CB [1997] Life history patterns of howler monkeys in a time-varying environment. Bol. Primatol. Lat. 6(1): 1-8.
Jones CB [March-Dec, 1998] A broad-band contact call by female mantled howler monkeys: implications for heterogeneous conditions. Neotropical Primates 6(2): 38-40.
Malmgren LA [1979] Empirical population genetics of golden mantled howling monkeys (Alouatta palliata) in relation to population structure, social dynamics, and evolution. Ph.D. Dissertation, University of Connecticut, Storrs.
West MJ [1967] Foundress associations in polistine wasps: dominance hierarchies and the evolution of social behavior. Science 157: 1584-1585.
West-Eberhard MJ [1975] The evolution of social behavior by kin selection. Quart Rev Biol 50: 1-33.
Wilson EO, Bossert WH [1971] A primer of population biology. Sinauer Assoc., Stanford, CN.

*  The last time I saw Group 5's D4 female, she was seated alone and immobile on a tree limb; her face impaled with quills of the prehensile-tailed porcupine [or, coendou: Coendou]. I never encountered this female again.
**EO Wilson's 2019 book, Genesis, advances the idea that many Mammals, including, humans, may be "eusocial." Where "temporal division-of-labor" is demonstrated, taxa can be classified, "primitively eusocial;" this classification would apply, also, to any other Vertebrates or, indeed, to any other Animals, where "age polyethism" is identified. If "tradeoffs" [e.g., energetic, reproductive, survivval] are most likely to be observed in "poor" conditions [e.g., heterogeneous regimes where "fitness" is compromised; recurrent drought, unpredictable food or water supply], "age polyethism" may evolve to minimize energetic costs in time and space. While females are expected to be most sensitive to energetic effects, males, also, may benefit, under some conditions, from age-dependent responses. Furthermore, there  may be energetic [reproductive] benefits in coordinating many maturational [age-dependent] and developmental [age-dependent] milestones or markers with one another as genetic and physiological energy-savings tactics and strategies.
-----------------------------------------------------------------------------------------------
Table 1. Age class, estimated age in years, number of females in each age class (N), observed (O), and expected (E) frequencies of social foraging, and chi square (X2) for a test of the null hypothesis. In “Age Class” column, YA= Young Adult; M-a= Middle-aged Adult; M-a-O= Middle-age to Old Adult; O= Old Adult.

Age Class	N	O	E	(O-E)2/E (X2)
YA (5-7)	5	15	42.4	17.71
M-a (7-10)	5	35	42.4	1.29
M-a-O (10-15)	1	18	8.1	12.11
O (15+)	1	33	8.1	76.54
Total	12	101	101	107.65

Experiment...Food Dispersion...Hacienda La Pacifica [1976] (Clara B. Jones)

Experiment: Hacienda La Pacifica, Cañas, Costa Rica [1976] (Clara B. Jones, Ph.D.)

WHO: This post describes an unsuccesful attempt to manipulate food dispersion (distribution of food in time and space) using a Neotropical primate. The target species was the mantled howler monkey (Alouatta palliata Gray), a predominately arboreal monkey that is exclusively herbivorous, preferring new leaves, flowers, and fruit. The diet of mantled howlers, also, includes mature leaves of many plant species (mostly tree and some shrubs and vines); as well, old leaves may be eaten in due course as well as "fallback" foods, eaten when preferred food items are not available, rare in time and space, or dispersed in a manner making foraging for them energetically and/or temporally expensive, ceteris paribus. As described by Milton in her 1980 book, the foraging behavior of mantled howlers is "rule-governed", and the method described here is probably most useful with animals whose foraging behavior is tactical and strategic (e.g., animals following particular routes depending upon distribution, abundance, and/or quality of food) rather than opportunistic or "random". The method described herein should apply to animals feeding on food occurring in discrete packages (e.g., trees, termite mounds, carcasses) and/or in patches. In general, the method has utility with non-volant and non-aquatic animals.

WHAT: Foraging behavior of one mantled howler group in Costa Rican tropical dry forest was followed before manipulation for 3 d in dry season. Dry season was selected as the time of year when many preferred foods are most likely to flower and fruit, and the particular procedure employed (see below), required the absence of rain. A medium-sized, relatively abundant tree (Tabebuia neocrysantha: see image) was flowering at its peak during the study week and was selected as the target food item for logistic and practical reasons. In addition, the manipulation was performed in a relatively small patch of forest on the monkeys' home range (see below) to allow for selected post-manipulation data collection. The 3 d window of observation was selected to minimize the chance that flower quality would deteriorate, decreasing salience of the food item for the animals.

DESIGN AND APPARATUS: Two T. neocrysantha trees were selected for experimental manipulation. Close observation of the animals' foraging behavior in the days prior to the manipulation permitted confident knowledge of the group's location relative to the test site and relatively confident prediction that the group would utilize the trees selected as well as the approximate time of day of feeding. The objective of this field experiment was to record group movement(s), including routes taken, and feeding behavior(s) before and after manipulation, in particular, "decisions" regarding food type (flowers, fruit, new leaves, and/or mature leaves), distance traveled from feeding site of origin, route taken to next feeding station, etc. The manipulation entailed spraying the target trees with a liquid substance gustatorially, and, possibly, olfactorily, aversive to the animals. Based upon the suggestion of a rancher, quinine (Qualaquin, see link) was selected as the substance employed because of its low cost, because of the low likelihood that it would harm the animals, and because it was water-soluble. Furthermore, in Costa Rica, quinine is available "across the counter". The particular ratio of quinine to water should be as high as possible to ensure its effectiveness as a deterrent/avoidant substance to the animals from the food source; however, the particular ratio of aversive substance to water will be a function of body size, type of aversive product, and, possibly, other factors. The vehicle for delivery of the liquid substance was an inexpensive, plastic spray container generally employed for delivery of insecticide.

OUTCOME: The success of the project descrtbed was limited as a completed study primarily because of the small number of field assistants used with whom to divide tasks, an obvious contingency unfortunately not considered in sufficient detail before beginning what must be termed a pre-test.

BENEFITS AND COSTS: Each researcher must determine for her/himself the relative benefits and costs of the design described here. However, inherent to any experiment, whether field or laboratory, is the requirement to stress organisms in order to obtain veridical results/data. This principle applies, also, to human research.

ADDITIONAL QUESTIONS THAT MIGHT BE ADDRESSED WITH DESCRIBED METHOD:

1. travel efficiency/costs pre- and post-manipulation

2. movements in relation to cognitive complexity requiring evaluation of foraging tactics/strategies

3. assesment of possible decision hierarchy regarding food selectivity and is pre- and post-manipulation foraging "rule-governed

4. assessment of consequences of manipulation as ecological constraint (e.g., does manipulation induce fissioning or other changes in social organization)

5. does manipulation increase/decrease competition/aggression

6. which, if any subject, emerges as leader to alternative food station(s) (e.g., topics related to coordination and control at individual, sub-group, and group levels)

7. do temporal and/or spatial (e.g., detours, alternate routes) patterning of movements change from pre- to post-manipulation

8. do animals continue to utilize or reject food item(s); if reject, for how long; if reject, what stimuli salient (color, food type, etc.); do they generalize these cues to other food items

http://en.wikipedia.org/wiki/Quinine

The attached link displays a published report of a foraging experiment using two baboon groups as subjects:

http://www.sciencedirect.com/science?_ob=MImg&_imagekey=B6VRT-4TYRF97-8-2&_cdi=6243&_user=10&_pii=S0960982208014176&_coverDate=12%2F09%2F2008&_sk=%23TOC%236243%232008%23999819976%23754050%23FLA%23display%23Volume_18,_Issue_23,_Pages_1815-1898_(9_December_2008)%23tagged%23Volume%23first%3D18%23Issue%23first%3D23%23date%23(9_December_2008)%23&view=c&_gw=y&wchp=dGLbVzz-zSkzk&md5=a894712af9df80a816fab318298a585e&ie=/sdarticle.pdf