Dynamics of population growth by Cebus capucinus in Costa Rica

Leakey Foundation Final Report Fernando A. Campos, University of Calgary

1.1 Brief summary The central aim of my research is to understand the effects of environmental change on behavioral flexibility and adaptation in the white-faced capuchin (Cebus capucinus), a medium-sized Neotropical primate, across a range of spatial and temporal scales. I collected behavioral data during 18 months of field work in Sector Santa Rosa (SSR) of the Área de Conservación Guanacaste (ACG), a UNESCO World Heritage site in Costa Rica that comprises a complex mosaic of tropical dry forest in diverse stages of regeneration. I combined my behavioral observations with long-term census and demographic data, satellite-based assessments of landscape spatial pattern, climate records, and systematic botanical measurements to investigate several outstanding questions about how primates cope with ecological variability. Predation risk and foraging efficiency showed strong spatiotemporal variation depending on both climate and habitat structure, while capuchins’ movement patterns and population dynamics reflected these pressures at larger scales. This research contributes to our understanding of how primates adapt their behavior to thrive in changing environments.

1.2 Publication summary and plans My Leakey-funded field work has resulted in three peer-reviewed publications in journals with broad readership.

1. “Drivers of home range characteristics across spatiotemporal scales in a neotropical primate, Cebus capucinus” published in Animal Behaviour: doi:10.1016/j.anbehav.2014.03.007.

2. “Spatial ecology of perceived predation risk and vigilance behavior in white-faced capuchins” published in Behavioral Ecology: doi:10.1093/beheco/aru005.

3. “Urine-washing in white-faced capuchins: a new look at an old puzzle” published in Behaviour: doi:10.1163/1568539X-000030800.

I have completed two additional manuscripts that I plan to submit for publication in the coming weeks. The first is titled “A multi-decade investigation of primate population dynamics: the effects of climatic oscillations and forest regeneration” and the second is titled “Energy returns on foraging in white-faced capuchins, Cebus capucinus.”

1.3

Detailed Summary

1.3.1 Introduction and relevance to the study of human origins One of the major goals of paleoanthropology is to understand the role of environmental factors in shaping the course of human evolution. Most prevailing hypotheses that attempt to link the envi1

ronment with human evolution ascribe central importance to landscape change and heterogeneity (Vrba, 1980; Potts, 1996; Kingston, 2007). A growing body of evidence suggests that many early hominins exploited a variety of habitats within mosaic landscapes, and that many of these habitats experienced strong shifting or oscillating climatic conditions (reviewed by Reed et al., 2005; Elton, 2008). Potts (1998) argues further that the appearances of many important hominin adaptations coincide with periods of substantial habitat diversity and environmental remodeling. However, there are significant limitations on what can be learned about human evolution from archeological and paleoenvironmental data alone. For example, the fitness landscapes associated with individual foraging strategies, ranging behaviors, daily activity patterns, and habitat and resource utilization depend critically on interactions between individuals and the particular biotic and abiotic elements of their local surroundings and can probably never be fully contextualized within a reconstructed ancient environment based on archeological data.

One approach to dealing with these limitations is to use living nonhuman primates as models (Whiten et al., 2010). Capuchins (Cebus and Sapajus spp.) show many behavioral and anatomical convergences with great apes and humans, including a large brain-to-body size ratio, long life spans, violent coalitionary aggression, the capacity for tool use, and social traditions. Like early hominins, C. capucinus possess a remarkable ability to exploit varied and varying environments: they are generalists in both habitat and diet, and they thrive in a broad range of environmental conditions (Fragaszy et al., 2004). The landscape at SSR and the numerous convergences that capuchins share with hominins makes this population an excellent model system for exploring some of the ecological and demographic pressures that may have shaped humans’ evolutionary trajectory. My field observations and my broad analytical approach—integrating landscape ecology, spatial statistics, and GIS/remote sensing— provide a comprehensive examination of a primate population’s responses to its changing environment. The results of this research provide valuable information that may help to deconstruct and quantify the key components of the “habitat heterogeneity” paradigm in human evolution, which remains central but vaguely-defined in current anthropological theory.

My principle findings are summarized below.

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1.3.2 Perceived predation risk and vigilance behavior Predation pressure is believed to be a fundamental evolutionary driver in primate socioecology, yet our understanding of how fine-scale variation in perceived predation risk affects primates’ shortterm space use patterns and predator avoidance strategies remains limited. Perceived predation risk can be estimated relatively easily in some nonhuman primates due to their distinct and easily recognizable alarm-call responses to different predator guilds (Seyfarth et al., 1980; Digweed et al., 2005; Fichtel et al., 2005). I calculated encounter frequencies with different predator guilds— raptors, snakes, and terrestrial quadrupeds—based on alarm calls and direct observation, and I characterized these encounters using a range of ecological variables. Alarm-calling bouts directed at birds were more likely to originate in high forest strata, whereas alarm-calling bouts at snakes and terrestrial quadrupeds were more likely to originate near the ground. Using an analytical approach introduced by Willems and Hill (2009), I related the spatial distribution of alarm calls to the spatial distribution of systematically collected ranging data to create predator guild-specific estimates of perceived predation risk, and I explored the distribution of these perceived risk functions across the heterogeneous landscape. The relative risk maps revealed that high-risk areas for birds and for all guilds combined consisted of more mature forest, whereas low-risk areas for these predators consisted of relatively younger forest (fig. 1.1).

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Figure 1.1: Log-relative risk functions for each predator guild based on alarm-calling data and given the underlying pattern of habitat

usage, with asymptotic tolerance contours showing zones of heighted risk (solid) and reduced risk (dashed). Small gray crosses indicate the locations of recorded alarm-calling bouts. The “combined” guild includes the other 3 guilds as well as all alarm-calling bouts that could not be confidently assigned to a guild.

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Finally, I analyzed the spatiotemporal occurrence of a putative antipredator behavior, vigilance, to determine whether the perceived risk functions were informative for predicting vigilance behavior relative to null models of uniform risk or habitat-specific risk. Capuchins were most vigilant near the ground, which may reflect greater perceived exposure to snakes and terrestrial predators in lower forest strata. Incorporating the combined (bird + snake + terrestrial quadruped) risk function into a predictive model of vigilance behavior improved prediction relative to null models of uniform risk or habitat-specific risk (fig. 1.2).

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Figure 1.2: Estimated coefficients for models for the occurrence of vigilance behavior that include vertical level, one guild or habitat

risk scenario, and no interaction effects. Estimates are relative to the baseline categories “Low” for vertical level and “Early Forest” for habitat. Vigilance was coded as 1 (vigilant) or 0 (not vigilant). All models include the random effects focal sample number and focal animal. Thick lines show ±1 standard deviation; thin lines show ±2 standard deviations. Model m12 received greatest empirical support.

The results of this study demonstrate that my study animals perceived reduced predation risk in the high and middle forest layers, and they adjust their vigilance behavior to small-scale spatial variation in perceived risk. My findings suggest a possible benefit to C. capucinus from exploiting young, disturbed habitats: perceived predation risk from aerial predators and overall predator encounter rates are reduced in younger habitats. Thus, the ability to exploit disturbed buffer or edge habitats, which are often given low conservation priority, may provide unexpected advantages to adaptable species, such as refuge from some types of predators.

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1.3.3 Small-scale energetic returns on foraging behavior Natural selection should strongly favor efficiency in individual foraging behavior (Emlen, 1966; Pyke et al., 1977). Using brief foraging bouts as the unit of analysis, I quantified energy intake rate using the measured energy content of ingested food items, and I quantified energy expenditure using estimates of basal and locomotor energy costs based on continuous changes in activity and time-matched movement trajectories. Capuchins’ small-scale foraging behavior shifted along with changes in their energetic resource base. Energy expenditure rates during foraging bouts were inversely proportional to food abundance, and travel velocities slowed as they incorporated a greater fraction of less-predictable invertebrates in their diet (fig. 1.3). a)

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Figure 1.3: Concurrent changes in the energetic resource base and travel velocities, separated by season and habitat type. a) Propor-

tion of the total energy ingested from insects and invertebrates. The proportions do not sum to one because of the small contributions of seeds, owers, and other animal food items. b) Violin plots and box plots of overall travel velocities during focal samples, each of which contributes one point to the plot.

Expected energetic returns on foraging bouts were driven primarily by extrinsic constraints such as seasonality and habitat characteristics rather than by intrinsic constraints such as sex or social group size. I found that, from a foraging energetics standpoint, mature habitats were consistently superior to younger habitats, enabling higher energy intake rates and lower energy expenditure 5

rates for greater overall net energy returns. This mature-forest advantage varied seasonally and was most evident during the dry season, when ecological contrasts between habitat types are most pronounced (fig. 1.4). a)

Energy Expenditure Rate Group Mass Sex Male Season Wet Habitat Intermediate Habitat Mature Season Wet:Habitat Mature

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Net Energy Return Group Mass Sex Male Season Wet Habitat Intermediate Habitat Mature Season Wet:Habitat Mature

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Figure 1.4: Model-averaged regression coefficients and relative variable importance for linear mixed models of a) energy expenditure

rate, b) energy intake rate, and c) net energy return. Thick error bars show ±1 SD and thin bars show 95% confidence intervals. The predictor variables were scaled to facilitate direct comparison of their relative effects. All models included the random effects focal individual and focal group. The relative importance of each predictor variable was calculated as the sum of the Akaike weights for each model in which the variable appeared.

Thermoregulatory needs compel capuchins to increase resting time during the dry season (Campos & Fedigan, 2009), but when they do forage during the dry season, they must expend greater energy per unit of energy consumed. This finding reinforces the idea that the dry season is a challenging time for capuchins in SSR and that their long-term population dynamics are to some degree contingent on multi-year trends in dry season severity (see below). In light of my other findings that capuchins in SSR experience greater perceived predation risk in mature forest, I infer an interesting ecological dynamism in which the study animals must balance the counteracting pressures of more productive foraging conditions with greater predation risk.

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1.3.4

Differential use of space

The factors that drive within-species variation in animal space use remain poorly understood. A growing body of evidence suggests that both home range attributes and biological interpretations of the home range may depend fundamentally on the scale of analysis. I used a multi-scale mixed effects modelling framework to examine how seasonal fluctuations in climate, food resource abundance, and group mass affected variance in home range area and the maturity stage of forest used by capuchins in SSR. I combined the location data that I collected during my field work with data from several other researchers to produce an 8-year data set representing over 20,000 contact hours. I estimated home ranges for seven social groups at four nested temporal scales and three nested spatial scales using a movement-based kernel method (fig. 1.5).

Monthly

Quarterly

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Figure 1.5: Illustration of the movement-based kernel method used for estimating home ranges of white- faced capuchins in this study.

Home ranges shown are for group BH at each of four nested temporal scales. The upper panels show the recorded location points (small dots) and the inferred movement paths (black line segments) of BH group during the relevant period. The colored shading represents the utilization distribution. The lower panels show the three home range zones delineated for each home range: core zone (50% isopleth, solid line); primary ranging zone (70% isopleth, dashed line); and total home range zone (95% isopleth; dotted line).

Group mass was consistently the most important predictor of home range size in the models for monthly and quarterly ranges, and its effects were relatively insensitive to spatial or temporal scale. Mean daily maximum temperature was an influential factor in shaping monthly range area, with hotter weather favoring smaller home range area. Greater fruit availability was also associated with smaller monthly range area. The effects of temperature and fruit availability were both scale dependent: the impact of both variables was greatest on the core zone (fig. 1.6). The different study groups showed marked variation in the habitat composition of their home ranges, but in all groups, higher-use zones consisted of older, more evergreen forest. The habitat composition of different home range zones was driven primarily by climatic seasonality, with hotter temperatures predicting increased use of mature evergreen forest (fig. 1.7).

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Core

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Figure 1.6: Model-averaged regression coefficients and relative variable importance for linear mixed models of home range size. Thin

error bars show 95% confidence intervals, and thick bars show ±1 SD.

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Figure 1.7: Model-averaged regression coefficients and relative variable importance for linear mixed models of mean forest maturity

index contained within the home range.

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1.3.5

Long-term population dynamics in relation to forest regeneration and climate change

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Long-term monitoring is necessary for understanding the extent to which small or threatNumber of Groups (a) ened animal populations can cope with chang40 ing environmental conditions (Sinclair & By35 rom, 2006; Clutton-Brock, 2012). Most studies 30 of long-lived nonhuman primates have not been long enough in duration to investigate Mean Group Size (b) 18 these important questions, and consequently, 16 there have been few studies on the long-term 14 dynamics of primate populations in relation to 12 quantitative data on ecosystem change. DrawTotal Population Size (c) ing together various long-term data sets, I ex600 amined how climatic fluctuations and land500 scape structural dynamics have affected the 400 natural recovery process of a population of white-faced capuchins over a 30-year period in Immature:Female Ratio (d) 1.9 relation to quantitative information on how 1.8 1.7 the landscape and climate changed during the 1.6 1.5 same period. The population’s rapid initial 1.4 1.3 growth and later stabilization suggests that it Census year was below the habitat’s carrying capacity at the time of the conservation area’s establishment Figure 1.8: Trends in the capuchin population from 1983 to 2013, (fig. 1.8). Most of the population growth in including (a) the total number of groups, (b) mean group size, (c) recent decades has occurred in a sub-region of total population size, and (d) immature to adult female ratio. Loess smoothers added to aid visual interpretation of the trends.

SSR that experienced greater gains in forest cover with medium- to high-degree of evergreenness, which is an important resource for primates during the severe dry season (fig. 1.9). The availability evergreen habitats varied with the strength of the previous wet season, which in turn was strongly coupled with global climatic and oceanic cycles. Following extreme drought periods, population growth slowed, mean group size decreased, and reproductive rate declined. If drought years become increasingly common as the global climate warms, many animals in seasonally dry forests may be negatively affected. These findings suggest that extreme drought years may challenge small capuchin populations by disrupting tree phenology cycles and reducing the availability of favorable habitat during critical times of year.

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Figure 1.9: Landsat-derived maps of the study area during peak dry season in March 1985 (top) and March 2011 (bottom) showing

topography, vegetation greenness, MODIS transects, and sub-regions of relatively high capuchin density. The uniformly dark area in the foreground is the PaciďŹ c Ocean. The elevation data are exaggerated by a factor of four, and they come from the ASTER Global Digital Elevation Model, Version 2, a product of METI and NASA.

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1.3.6 Population health and genetic diversity genetic diversity The population genetics project described in my original proposal to the Leakey Foundation has not been completed, but this research is well underway. The project’s goal is to quantify genetic diversity in three Neotropical primate species and to assess the landscape’s permeability to gene flow along an ecological gradient from sea level to 1,100 m in the ACG. We have collected fecal samples for genetic analysis from unhabituated groups of capuchins (89 samples), howler monkeys (109 samples), and spider monkeys (56 samples) all across the ACG (fig. 1.10). My collaborators at the University of Tokyo are currently genotyping these samples. I expect the results of this research to provide unique insights into landscape-scale ecological and behavioral processes related to primate population health, life history, community ecology, and conservation.

El Hacha (272 m)

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Figure 1.10: Map of DNA sample collection sites for three primate species in the Área de Conservación Guanacaste.

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References

Campos, F. A. & Fedigan, L. M. (2009). Behavioral adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in santa rosa national park, costa rica. American Journal of Physical Anthropology, 138(1), 101–111. doi:10.1002/ajpa.20908 Clutton-Brock, T. (2012). Long-term, individual-based field studies. In P. M. Kappeler & D. P. Watts (Eds.), Long-term field studies of primates (pp. 437–449). Springer Berlin Heidelberg.

Digweed, S. M., Fedigan, L. M., & Rendall, D. (2005). Variable specificity in the anti-predator vocalizations and behaviour of the white-faced capuchin, Cebus capucinus. Behaviour, 142(8), 997–1021. doi:10.1163/156853905774405344 Elton, S. (2008). The environmental context of human evolutionary history in eurasia and africa. Journal of Anatomy, 212(4), 377–393. doi:10.1111/j.1469-7580.2008.00872.x Emlen, J. M. (1966). The role of time and energy in food preference. The American Naturalist, 100(916), 611–617. doi:10.1086/282455 Fichtel, C., Perry, S., & Gros-Louis, J. (2005). Alarm calls of white-faced capuchin monkeys: an acoustic analysis. Animal Behaviour, 70(1), 165–176. doi:10.1016/j.anbehav.2004.09.020 Fragaszy, D. M., Fedigan, L. M., & Visalberghi, E. (2004). The complete capuchin: the biology of the genus Cebus. New York: Cambridge Univ Press.

Kingston, J. D. (2007). Shifting adaptive landscapes: progress and challenges in reconstructing early hominid environments. Yearbook of Physical Anthropology, 50, 20–58. doi:10.1002/ajpa.20733 Potts, R. (1998). Environmental hypotheses of hominin evolution. Yearbook of Physical Anthropology, 41, 93–136.

Potts, R. (1996). Evolution and climate variability. Science, 273(5277), 922–923. doi:10.1126/science.273.

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Pyke, G. H., Pulliam, H. R., & Charnov, E. L. (1977). Optimal foraging: selective review of theory and tests. Quarterly Review of Biology, 52(2), 137–154.

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