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.

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

Conducting Fieldwork Remotely (Clara B. Jones)

Conducting Field Work Remotely

I am presenting this blogpost hoping that some researchers might find it useful--especially, females who want to remain fieldworkers while assuming caretaking responsibilities. At one point [~2006], I was unable to travel far from my home base but wanted to conduct a project in Brazil. I collaborated with a Brazilian colleague--a [then] young professor, Julio Cesar Bicca-Marques, who suspected hybridization between two species of howler monkeys at one of his study sites. We brainstormed, deciding that I would write a proposal to obtain funding. My colleague commented on the first draft, I incorporated his suggestions and revised the proposal, and we were awarded funding by two conservation organizations. My colleague conducted the research with two of his graduate students, drew some amazing maps, took some amazing photographs, & collected the data. We collaborated on data analysis. I wrote the first draft of the resulting paper after which my colleague revised and submitted the final version. Our paper was accepted for publication, and we were both satisfied with the order of authorship and assignment of corresponding author.* This procedure, or, some variant of it, might work for others with limited mobility. I do not intend to suggest that one can build a career on these sorts of accommodations; however, intermittently, or, for brief periods of time, such arrangements, or, some variant of same, might work very well.

Bicca-Maarques JC, et al. (2008) Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization. Primates 49(4): 246-252.

https://link.springer.com/article/10.1007/s10329-008-0091-4

*At the time, I justified being final & corresponding author on the basis of my having designed a highly original survey method and on the basis of having written a successful proposal. However, in retrospect, I think a strong case could be made that it would have been appropriate for Bicca-Marques to have been assigned those roles. As an aside, he went on to conduct additional work on this topic and published the research that I did not participate in.