Documentcl

American Journal of Primatology 73:11891198 (2011)

REVIEW ARTICLE

Influence of Climatic Variables, Forest Type, and Condition on Activity Patternsof Geoffroyis Spider Monkeys Throughout Mesoamerica

ARTURO GONZALEZ-ZAMORA1, VICTOR ARROYO-RODRIGUEZ2, OSCAR M. CHAVES2, SONIA SANCHEZ-LOPEZ3,FILIPPO AURELI4,5, AND KATHRYN E. STONER21Division de Posgrado, Instituto de Ecologa, Xalapa, Veracruz, Mexico2Centro de Investigaciones en Ecosistemas, Universidad Nacional Autonoma de Mexico (UNAM), Morelia, Michoacan, Mexico3Centre Especial de Recerca en Primats, Universitat de Barcelona, Barcelona, Spain4Research Center in Evolutionary Anthropology and Palaeoecology, School of Natural Sciences and Psychology, Liverpool JohnMoores University, James Parsons Building, Byrom Street, Liverpool, United Kingdom5Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mexico

Understanding how species cope with variations in climatic conditions, forest types and habitat amountis a fundamental challenge for ecologists and conservation biologists. We used data from 18communities of Mesoamerican spider monkeys (Ateles geoffroyi) throughout their range to determinewhether their activity patterns are affected by climatic variables (temperature and rainfall), foresttypes (seasonal and nonseasonal forests), and forest condition (continuous and fragmented). Data werederived from 15 published and unpublished studies carried out in four countries (Mexico, El Salvador,Costa Rica, and Panama), cumulatively representing more than 18 years (221 months, 43,645 hr) ofbehavioral observations. Overall, A. geoffroyi spent most of their time feeding (38.4714.0%, mean7SD)and resting (36.6712.8%) and less time traveling (19.8711.3%). Resting and feeding were mainlyaffected by rainfall: resting time increased with decreasing rainfall, whereas feeding time increasedwith rainfall. Traveling time was negatively related to both rainfall and maximum temperature.In addition, both resting and traveling time were higher in seasonal forests (tropical dry forest andtropical moist forest) than in nonseasonal forests (tropical wet forest), but feeding time followed theopposite pattern. Furthermore, spider monkeys spent more time feeding and less time resting (i.e.,higher feeding effort) in forest fragments than in continuous forest. These findings suggest that globalclimate changes and habitat deforestation and fragmentation in Mesoamerica will threaten the survivalof spider monkeys and reduce the distributional range of the species in the coming decades. Am. J.Primatol. 73:11891198, 2011. r 2011 Wiley Periodicals, Inc.

Key words: activity patterns; Ateles geoffroyi; climate change; fragmentation; rainfall; seasonality;temperature

INTRODUCTION

Activity patterns (time spent feeding, traveling,resting, and socializing) provide information on howanimals interact with the environment and invest timeand energy for survival and reproduction [Dunbar,1988]. Studying activity patterns is crucial for betterunderstanding why a given taxon can survive in somehabitats but not in others [Dunbar et al., 2009], and forindentifying the areas that are suitable for a specieswithin their geographical range [Korstjens et al., 2006].As a consequence of accelerating global climate changeas well as unprecedented deforestation rates in tropicalregions during the last decades [Anderson et al., 2008;FAO, 2011], it is fundamental to understand the abilityof species to develop behavioral modifications in theiractivity patterns to cope with both climatic change andhabitat deforestation [Dunbar et al., 2009].

In many primate groups, activity patterns maybe affected by climatic variables [Dunbar, 1998;

Dunbar et al., 2009; Korstjens et al., 2006;Wiederholt & Post, 2010], seasonality [Doran, 1997;Korstjens et al., 2006], habitat characteristics [Isbellet al., 1998], or some combination of these factors.Ambient temperature and rainfall, and the season-ality of these characteristics, are the main climaticvariables driving activity patterns in many primates[e.g., Ateles: Korstjens et al., 2006; Gorilla and

Published online 6 September 2011 in Wiley Online Library (wileyonlinelibrary.com).

DOI 10.1002/ajp.20989

Received 18 November 2010; revised 19 July 2011; revisionaccepted 22 July 2011

Contract grant sponsor: Consejo Nacional de Ciencia y Tecno-loga (CONACYT), Mexico; Contract grant numbers: 2005-51043; 2006-56799.

Correspondence to: Arturo Gonzalez-Zamora, Division dePosgrado, Instituto de Ecologa A.C. km 2.5 Antigua Carreteraa Coatepec No. 351. 91070 Xalapa, Veracruz, Mexico.E-mail: [email protected]

rr 2011 Wiley Periodicals, Inc.

Colobus: Korstjens & Dunbar, 2007; Korstjens et al.,2010; Pan: Lehmann et al., 2007; Theropithecus:Dunbar, 1998]. For instance, to deal with climaticstresses, such as high temperatures and/ordrought, primates frequently reduce traveling timebecause this is an energetically costly activity,allowing them to reduce energy expenditures[Dunbar et al., 2009; Korstjens et al., 2006] andto increase their resting time to avoid overheating[e.g., Theropithecus gelada: Dunbar, 1988, 1992a;Papio hamadryas: Stelzner, 1988; Pan troglodytes:Kosheleff & Anderson, 2009].

Rainfall can also affect activity patterns ofprimates because of the positive relationshipbetween rainfall and resource availability [Bronikowski& Altmann, 1996; Deshmukh, 1984], particularly ofripe fleshy fruits [i.e., the main food source offrugivorous primates, such as spider monkeys;Di Fiore et al., 2008; Gonzalez-Zamora et al.,2009; Stevenson & Link, 2010]. Primates needto adjust their diet and activity patterns to copewith resource scarcity in habitats and/or duringperiods with lower rainfall regimes [e.g., Kaplinet al., 1998; McConkey et al., 2002; Stevenson et al.,2000].

Resource availability also can affect amongforests with different climatic seasonality becausevegetation structure and composition differ amongthem [Gentry, 1982]. In contrast to tropical wet forests(TWF) that show little seasonality, fleshy fruit avail-ability may be limited in more seasonal forests [e.g.,tropical moist forest (TMF), tropical dry forest (TDF)],particularly during the dry season [Bunker & Carson,2005; Murphy & Lugo, 1995]. Anthropogenic activ-ities, such as deforestation, forest fragmentation andlogging, also can affect vegetation structure andcomposition, modifying resource availability for pri-mates [e.g., Arroyo-Rodrguez & Mandujano, 2006;Chapman et al., 2000]. The density of larger treesis typically lower in smaller forest fragments,particularly of those species that are used as foodresources by frugivorous primates [Arroyo-Rodrguez& Mandujano, 2006; Chaves et al., 2011a; Dunn et al.,2009]. Therefore, because larger trees produce higheramounts of fruits [Chapman et al., 1992], smallerfragments contain a lower food supply for frugivorousprimates than larger fragments [Arroyo-Rodrguez &Mandujano, 2006; Chapman et al., 1992; Dunn et al.,2009]. These changes in food availability ultimatelycan affect activity patterns. For example, time spentfeeding by gelada baboons (T. gelada) in Ethiopia isinversely related to spatial and temporal food avail-ability in three different habitats [i.e., two plateaus ofopen grassland mosaics at different altitudes and withdistinct plant compositions and one African savannah;Iwamoto & Dunbar, 1983]. In summary, activitypatterns seem to be a function of vegetation andclimatic characteristics [e.g., Caraco, 1979; Dunbar,1992a,b; Dunbar et al., 2009].

Activity patterns also depend on the socialsystem in which the species live [Dunbar et al.,2009; Korstjens et al., 2006; Wrangham et al., 1993].For instance, the ecological constraints model pre-dicts that larger groups deplete food patches fasterthan smaller groups, and hence individuals in largergroups have to visit more patches each day, increaseday ranges, spend more time traveling, and in somecases, expand their home ranges [Chapman, 1990;Janson & Goldsmith, 1995; Milton, 1984; Wranghamet al., 1993]. Primates that live in social systems witha high degree of fissionfusion dynamics, such asspider monkeys (Ateles spp.), adjust their subgroupsize to local food availability [Aureli et al., 2008;Kummer, 1971] and annual rainfall (an indirectmeasure of habitat quality) [Korstjens et al., 2006].In these systems, individuals that belong to the samecommunity are rarely together, but they fission andfuse in smaller subgroups of variable composition.These fissionfusion dynamics are effective in flex-ibly managing activity patterns as larger subgroupsdo not experience greater ranging costs than smallersubgroups [Asensio et al., 2009]. Although Korstjenset al. [2006] suggest that community size is astronger determinant of time budgets than subgroupsize, they actually find that the percentages of timespent feeding and moving do not correlate withcommunity size or subgroup size using a large dataset on Ateles spp. Thus, unlike group size inrelatively cohesive groups, community size andsubgroup size are unlikely to play a major role inthe activity patterns in species characterized by ahigh degree of fissionfusion dynamics.

Korstjens et al. [2006] investigated factorsaffecting activity patterns of the entire genus Ateles;however, research focusing on single species isnecessary to have a more detailed understanding oftheir ecology in changing habitats. Although somepublished studies document activity patterns ofAteles geoffroyi in continuous forests of Mesoamerica[e.g., Chapman, 1987a,b; Richard, 1970], no studiesto date have assessed the impact that climaticvariables, forest types, and forest condition mayhave on activity patterns through the distributionalrange. This information has critical evolutionary andconservation implications. From an evolutionaryperspective, throughout its distributional range,spider monkeys have adapted to certain areas orcomfort zones [sensu Anderson et al., 2008]characterized by climatic niches to which the speciesis tolerant [Korstjens et al., 2006]. These niches arecharacterized by relatively little variation in regionalclimatic conditions which allowed spider monkeys toadapt to their activity patterns, diet, and socialbehavior to the specific resource availability andenvironmental characteristics found in differentforest types [Anderson et al., 2008; Dunbar et al.,2009]. Unfortunately, predictive models about thepotential impact of climate change in Mesoamerica

Am. J. Primatol.

1190 / Gonzalez-Zamora et al.

indicate that temperature will increase and precipi-tation will decrease in the next 2050 years[Anderson et al., 2008]. These climatic alterationscould promote drastic changes in vegetation compo-sition and structure as well as changes in phenolo-gical cycles, with important implications for animalbehavior, population sizes, and distribution [Hannahet al., 2001; Parmesan, 2006]. Understanding howspecies cope with variations in climatic conditions,forest types, and conditions across their distribu-tional range is, therefore, critical for assessing theirability to cope with upcoming climatic alterationsand unprecedented anthropogenic disturbances.

In this study, we gathered data from a numberof studies and analyzed them to determine how theactivity patterns of A. geoffroyi are influenced byambient temperature, rainfall, forest type (i.e.,seasonal and nonseasonal forests), and forest condi-tion (i.e., continuous and fragmented). According tosocioecological models, we hypothesized that spidermonkeys can adjust their activity patterns in order todeal with variation in climatic variables, forest types,and forest conditions [e.g., Dunbar et al., 2009;Korstjens et al., 2006; Wiederholt & Post, 2010].Because resting is an energy-saving activity, wepredicted resting would be positively related toambient temperature and negatively related torainfall because of the inferred direct relationshipbetween rainfall and food availability [e.g.,Bronikowski & Altmann, 1996; Deshmukh, 1984].Similarly, owing to differential food availability, weexpected spider monkeys to spend more time restingin seasonal forests than in nonseasonal forests andin forest fragments than in continuous forests.Traveling was expected to follow the oppositepattern of resting to reduce travel-related energyexpenditures. Finally, as spider monkeys oftenincrease the time devoted to consumption of fibrousand hard-to-digest plant items (e.g., leaves) whenavailability and/or diversity of fleshy ripe fruits isscarce [e.g., in forest fragments and during the dryseason: Chaves et al., 2011a,b; Gonzalez-Zamoraet al., 2009], we predicted time spent feeding wouldbe negatively related to rainfall and higher inseasonal and fragmented forests to compensate forfood scarcity under these situations.

METHODS

Literature Review

We reviewed available studies (published arti-cles, book chapters, and unpublished theses) onactivity patterns of A. geoffroyi up to April 2011.Initially, we used internet databases (SCOPUS, ISIWeb of Science, PrimateLit, Google scholar) to locaterelevant published work. We then identified addi-tional studies cited within this primary literaturethat had not been published. We attempted to obtainas much of these unpublished data in the form of

theses or gray literature through university librariesand by directly contacting the authors. Our data baseincluded 15 studies from 18 communities ofA. geoffroyi in four countriesMexico, El Salvador,Costa Rica, and Panamarepresenting more than18 years (221 months, 43,645 hr) of behavioralobservations (Table I). From all studies included inthe data base, we obtained the percent of time (orscans) primates spent on feeding, resting, andtraveling (see the sampling method of each study inTable I). We also calculated the percent of timedevoted to other activities (including social activities)(Table I). However, we did not include data from thiscategory in our analyses because different authorsused different definitions for this category. Whenavailable, we also obtained the size of the studycommunities (Table I), but this factor was notincluded in our analyses because, as expected, itwas not related to time resting (R25 0.02, P5 0.66),feeding (R25 0.00, P5 0.95), or traveling (R25 0.00,P5 0.90). All data were obtained with noninvasivemethods, complying with the American Society ofPrimatologists principles for the ethical study andtreatment of nonhuman primates.

Climatic Variables, Forest Type, and ForestConditions

Following Gentry [1982], we grouped foresttypes into seasonal (TMF: 2,0002,800 mm rain/yearand TDF: o2,000 mm rain/year) and nonseasonalforest (TWF: 42,800 mm rain/year). Based on thesize of the forest, we identified two forest conditions:continuous and fragmented. All forest fragmentswere very small (o31 ha), whereas continuousforests were greater than 1,500 ha [Gonzalez-Zamoraet al., 2009; Table I]. Additionally, we considered thefollowing three climatic variables that were availablefor the time period of each study, using data from themeteorological station located closest to each studysite: average monthly rainfall (PMEAN), maximumtemperature (TMAX), and minimum temperature(TMIN). We selected these climatic variables becauseboth rainfall and temperature are important compo-nents of primate activity patterns models [e.g.,Dunbar, 1992a; Dunbar et al., 2009; Korstjens &Dunbar, 2007; Korstjens et al., 2006; Lehmann et al.,2007]. We could not consider the effect of variation inrainfall and temperature across the year because wedid not find relevant data to calculate an appropriatemeasure for all the studies.

Data Analyses

Percent data were transformed to proportionsand proportion data were arcsine transformed. Then,we tested if they were normally distributed (ShapiroWilk test: P40.11 for all data). To test the effectof local climatic variables on activity patterns,we performed three separate multiple regression

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Activity Patterns of Spider Monkeys / 1191

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analyses. In each analysis the dependent variable wasthe activity (resting, feeding, or traveling) and theindependent variables were PMEAN, TMAX, and TMIN.Variance inflation factor (VIF) values above fourindicate possible multicollinearity between indepen-dent variables [Chatterjee et al., 2000]. In our models,VIF never reached this value. In addition to thecomplete models (i.e., including all three climaticvariables), we used backward stepwise regressionanalyses and the Akaikes Information Criterion toselect the best model for each dependent variable[Motulsky & Christopoulos, 2003].

We used students t-tests to assess possibleeffects of forest type and forest condition on eachactivity. Considering continuous forests, we testeddifferences among seasonal (N5 7 data points) andnonseasonal forests (N5 12). To test the effect offorest condition, we compared continuous forest(N5 6) and fragments (N5 6) of TWF, the onlyforest type for which we had data for forestfragments (Table I). We considered three samplesfrom the same group in the same fragment of LosTuxtlas (studies 1, 2, and 3 in Table I) as indepen-dent, because they were separated in time between3 and 12 years, and both community sizes andclimatic conditions were notably different across thethree samples (see Table I). Although we used thesame independent variables for multiple tests, we didnot apply Bonferroni corrections to our resultsbecause we only made three different tests (one peractivity), so we did not increase so much theprobability of the statistical error type I (rejects atrue Ho) by chance. Also, by applying Bonferronicorrections, we could increase the probability of thestatistical error type II (do not reject Ho when isfalse) [see Nakagawa, 2004].

Only data covering the entire year (i.e., annualsamples) were used in the statistical analyses. Whendata were available only for the dry or wet season(N5 3; see Table I), the study was only used forproviding some general descriptive statistics. Alltests were performed with JMP (version 7.0, SASInstitute Inc.) and STATISTICA (version 5.5, Stat-Soft) software.

RESULTS

Across sites and groups, spider monkeys spentmost of their time feeding (38.4714.0%, mean7SD)and resting (36.6712.8%) and less time traveling(19.8711.3%) and in other activities (7.6710.0%)(N5 22 data points from different groups or from thesame group but during different sampling periods;Table I). However, there was large variation in timespent in each activity among groups and sites(Table I). Particularly, feeding time ranged from11% in a continuous TMF (BCI, Panama) to 67% in aTWF fragment (Los Tuxtlas, Mexico); resting rangedfrom 16% (Los Tuxtlas, Mexico) to 61% (BCI,

Panama); and traveling ranged from 4.5 to 41.1%in two TWF fragments in Mexico (Table I).

The best regression model indicated that restingwas mainly affected by PMEAN; when rainfalldecreased across studies monkeys spent more timeresting (Table II). Feeding time followed the oppositepattern: the best model indicated that feeding waspositively associated with PMEAN (Table II). Finally,traveling time was negatively related to both PMEANand TMAX (Table II). Importantly, the amount ofvariance explained by these climatic factors (R2)differed greatly among the models: it was only 20%for resting and 26% for feeding, but 86% for traveling(Table II).

The percentage of time spent resting differedbetween forest types, being significantly higher inseasonal forests than in nonseasonal forests(t52.30, df5 17, P5 0.03; Fig. 1A). Similarly,traveling time was significantly higher in seasonalforests than in nonseasonal forests (t53.10,df5 17, P5 0.006; Fig. 1A). Feeding time followedthe opposite pattern, being significantly higher innonseasonal forests than in seasonal forests (t5 2.57,df5 17, P5 0.02; Fig. 1A).

Activity patterns differed between continuousforest and forest fragments (Fig. 1B). Although thepercent of traveling time did not differ significantlybetween forest conditions (t5 1.15, df5 10,P5 0.28), monkeys spent more time feeding(t5 3.00, df5 10, P5 0.01) and less time resting(t54.19, df5 10, P5 0.002) in forest fragmentsthan in continuous forest (Fig. 1B).

DISCUSSION

Overall, our results demonstrate that there is alarge variation in time spent in each main activityacross communities of spider monkeys (A. geoffroyi)throughout Mesoamerica, and that a large propor-tion of this variation can be explained by annualrainfall, ambient temperature, forest types (seasonaland nonseasonal), and conditions (continuous andfragmented). These results are consistent withrecent socioecological studies on primates, andsupport the idea that temperature, rainfall, anddegree of seasonality are important climatic vari-ables driving the activity patterns of Neotropicalprimates [Chaves et al., 2011b; Dunbar et al., 2009;Korstjens et al., 2006; Wiederholt & Post, 2010]and Paleotropical primates [Bronikowski &Altmann, 1996; Dunbar, 1992b; Dunbar et al., 2009].Furthermore, consistent with Chaves et al. [2011b],our findings also indicate that spider monkeys canchange their activity patterns in forest fragments.

In agreement with our predictions, we foundthat, in habitats with lower rainfall, spider monkeysspend more time resting and that resting time washigher in seasonal forests. Similarly, as predicted,traveling time was strongly and negatively related to

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ambient temperature. Food availability for primates(including spider monkeys) increases with rainfall[Di Fiore et al., 2008; Kaplin et al., 1998; Stevenson,2001; Stevenson et al., 2000], and those living inseasonal forests are exposed to more stressfulconditions [e.g., temporal food scarcity, drought,high ambient temperature; Murphy & Lugo, 1995;Stoner & Timm, 2004]. Therefore, it is reasonable toexpect that, just like we found, monkeys devote moretime resting in seasonal forest and where rainfall islower. This could be an energy-saving strategy tocope with resource limitations during the driestperiods and/or in the driest forests [Chaves et al.,2011b]. In addition, as traveling and feeding repre-sent energetically costly activities [Dunbar, 1988,1992a; Dunn et al., 2009; Korstjens et al., 2006],reducing travel time when ambient temperature ishigher could allow primates to minimize energy costsand feeding effort owing to overheating [e.g., Dunbaret al., 2009].

Interestingly, feeding time was positively relatedto rainfall but not significantly to temperature,suggesting that this activity could be more con-strained by differences in food availability. Similarly,feeding time was significantly higher in nonseasonalforests (TWF). Spider monkeys have been reportedto spend more time feeding during the rainy season[Chaves et al., 2011b; Felton et al., 2009], possiblybecause feeding is an energetically costly activitythat needs to be minimized during the dry season

TABLE II. Influence of Climatic Factors on Activity Patterns of Spider Monkeys (Ateles geoffroyi) Found inMesoamerica (We Indicate Both the Complete Models and the Most Parsimonious (i.e. Best Modelsa)).

Activity R2adj AIC Factorsb Parameterc Fratio P

Complete modelsResting 0.20 69.6 Intercept 0.328 0.38 0.713

PMEAN 0.0004 1.24 0.239TMAX 0.025 1.28 0.224TMIN 0.010 0.84 0.416

Feeding 0.15 67.6 Intercept 0.691 0.75 0.469PMEAN 0.001 1.99 0.070TMAX 0.004 0.17 0.871TMIN 0.005 0.37 0.717

Traveling 0.85 91.2 Intercept 2.114 4.77 0.001PMEAN 0.001 5.01 o0.001TMAX 0.046 4.59 o0.001TMIN 0.002 0.31 0.763

Best modelsResting 0.20 71.1 Intercept 0.720 10.3 o0.001

PMEAN 0.001 4.70 0.048Feeding 0.26 71.3 Intercept 0.490 7.05 0.010

PMEAN 0.001 6.13 0.027Traveling 0.86 93.1 Intercept 1.988 12.2 o0.001

PMEAN 0.001 30.0 o0.001TMAX 0.043 89.3 o0.001

aThe best models were selected through backward stepwise regression analyses. We indicated the adjusted R2 and Akaikes Information Criterion for eachregression model.bClimatic factors: PMEAN, average monthly rainfall; TMAX, maximum temperature; TMIN, minimum temperature.cThe sign of each parameter indicates the relationship (positive or negative) between each continuous factor and the response variable.

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[Dunbar et al., 2009; Korstjens et al., 2010]. Feltonet al. [2009] and Chaves et al. [2011b] also interpretgreater feeding time in the rainy season as a strategyfor spider monkeys to take advantage of peakseasonal foods allowing them to ingest surplusenergy and store it as fat in preparation for theimpending period of food scarcity. Other primatespecies accumulate fat during peaks of fruit abun-dance [Pongo pygmaeus: Knott, 1998; Lemur cattaand Eulemur sp.: Simmen et al., 2010; Lagothrixlagotricha cana: Peres, 1994; Ateles paniscus: Milton,1998; A. chamek: Wallace, 2005], which is a logicalstrategy for animals experiencing fluctuating foodsupply [Felton et al., 2009]. Further information onnutritional ecology and energetic strategies ofA. geoffroyi is needed to test the fat accumulationhypothesis.

In contrast with our prediction, traveling timewas negatively related to rainfall. We expected apositive relationship between the two variables,as low rainfall is usually associated with lowfruit availability [Bronikowski & Altmann, 1996;Deshmukh, 1984]. Under these circumstances, areduction in traveling could be an energy-savingstrategy. The negative relation is likely owing to thefact that, when more fruit sources are available,the monkeys spend less time traveling because thedistance among food patches decreases. This idea issupported by Chaves et al. [2011b], as they also findthat traveling time tended to be higher during thedry season. However, Asensio et al. [2009] do not findthat traveling time changed with season, and arguedthat monkeys adjust their subgroup sizes (i.e.,smaller subgroups are found during the dry season)to avoid travel costs associated with larger subgroups.Nevertheless, because most of the studies analyzed inour study did not provide data on average subgroupsizes, we cannot determine the relative influence ofsubgroup size on activity patterns.

In TWF (i.e., the only forest type for which wehad data for forest fragments), forest conditionaffected the activity patterns of spider monkeys.Specifically, monkeys spent more time feeding andless time resting in forest fragments than incontinuous forest, and hence the feeding effort[sensu Cavigelli, 1999] of monkeys was higher infragments. Similar differences in activity patternshave been reported for Chiropotes satanas in Brazil[Boyle & Smith, 2010; Boyle et al., 2009] andAlouatta palliata in Mexico [Dunn et al., 2009].Dunn et al. [2009] relate the variations in activitypatterns (and feeding effort) to the differences in dietbetween groups: leaf consumption is higher in thegroup inhabiting the smallest fragment, and thisgroup visits more food sources resulting in moretraveling, more feeding, and less resting. They arguethat this could be explained by the lower amount ofenergy these primates probably gain per food patch,as well as the need to diversify food sources when

consuming leaves (i.e., to obtain the best complementof nutrients and avoid an overload of particulartoxins or digestibility-reducing compounds). Ourfindings are consistent with this idea, as we foundin a previous study (using a data base similar tothat in this article) that spider monkeys have amore folivorous diet in fragments [Gonzalez-Zamoraet al., 2009], which could force them to diversify theirdiet [see Chaves et al., 2011a; Felton et al., 2009;Milton, 1981, 1998] and spend more time feeding andless time resting. However, it is important to gatherdata on activity patterns in fragmented seasonalforests (TMF and TDF), to assess whether it ispossible to generalize this finding to other foresttypes.

Conclusions and Recommendations forConservation

Our findings indicate that spider monkeys inMesoamerica can adjust their activity patterns inorder to cope with changes in temperature, rainfall,forest type (seasonal and nonseasonal), and condition(continuous and fragmented). However, it is stillunclear whether these behavioral adjustments willinsure their health and survival in the long term,especially if we consider the current high rates ofdeforestation and the impact that climate change willhave on Mesoamerican ecosystems in the nextfew decades [Anderson et al., 2008; FAO, 2011;Wiederholt & Post, 2010]. Studies evaluating therelationships between changes in activity patternsassociated with climatic variables, forest type andcondition, and the demographic consequences (e.g.,birth and death rates) in spider monkeys populationsare urgent for their conservation.

Based on our results, if ambient temperaturesincrease and annual rainfall decrease approximatingthe figures predicted by the climate change modelsfor Mesoamerica [Anderson et al., 2008], spidermonkeys will probably increase the enforced restingtime [i.e., resting needed for digestive and/or ther-moregulatory purposes; Korstjens et al., 2010] limit-ing the time monkeys can devote to other criticalactivities, such as feeding, traveling, and socialbehavior. This could reduce their population sizes,limit the distributional range of the species, and eventhreaten their long-term survival in the comingdecades.

It is alarming that A. geoffroyi has been recentlylisted as Endangered by the IUCN, because habitatloss and fragmentation across its range has beensevere and the species has been estimated to havedeclined by as much as 50% over the past 45 years[Cuaron et al., 2008]. In addition, it has beensuggested that A. geoffroyi could be one of the firstMesoamerican primate species to become locallyextinct in human-modified landscapes [Garberet al., 2006]. The remaining populations are isolated

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in few reserves and different-sized forest fragments[Cuaron et al., 2008]. Our results demonstrate thatfeeding effort is higher in forest fragments than incontinuous forests, and studies on other primatesindicate that an increase in feeding effort maynegatively affect fitness by increasing stress levels[Papio anubis: Sapolsky, 1986; L. catta: Cavigelli,1999; A. palliata: Jake Dunn, unpublished data].Thus, our results support the idea that monkeyscould experience higher stress levels in fragments, asit has been recently demonstrated by Rangel-Negrnet al. [2009] by analyzing fecal cortisol levels ofspider monkeys living in conserved forests, fragmen-ted forests, and captive conditions in the YucatanPeninsula, Mexico.

Considering the potential negative effects thatclimate change would have for spider monkeys,particularly in fragmented landscapes in whichinterfragment movements is highly limited [Arroyo-Rodrguez & Mandujano, 2009], conservation effortsshould be focused on the increase of landscapeconnectivity. Landscape corridors are required tofacilitate species and population movements betweenhabitats in response to climate change [Ewers &Didham, 2006]. In this sense, the MesoamericanBiological Corridora system of land planningcoordinated by the governments of the countrieslocated in the Mesoamerican regionwould connectthe largest reserves of Mesoamerica and could have acrucial positive impact on the conservationof primates and other plant and animal species[Anderson & Jenkins, 2006; Miller et al., 2001].Furthermore, increasing fragment size is critical toreduce primates foraging effort and maintain larger(and viable) primate populations.

It is important to recognize that our results arelimited by variation in data collection length,methodology, and interobserver experience acrossstudies. To address this shortcoming, we recommendthat, although research designs need to be appro-priate to the research questions and characteristicsof the study population and field site, we need tostandardize methodologies as much as possible. Morecoordination among scientists working on the samespecies and/or similar topics is needed in order tobuild the data bases required to address importantissues. These data bases are fundamental in allowingscientists carrying out more accurate comparisonsamong studies in order to reach critical general-izations and build theories that can be put to use forprimate conservation.

ACKNOWLEDGMENTS

This study satisfied the legal requirements ofMexican Secretary of Environment and NaturalResources (SEMARNAT) and meets all the Mexicananimal care policies and the Principles of theAmerican Society of Primatologists for the Ethical

Treatment of Nonhuman Primates. This work wassupported by grants from the Consejo Nacional deCiencia y Tecnologa (CONACYT), Mexico (2005-51043, 2006-56799). We thank ML Chavarra and RBlanco from Santa Rosa National Park, the person-nel of the Smithsonian Tropical Research InstituteEnvironmental Science Program, Biological Stationof Los Tuxtlas, Biology Institute of the UniversidadNacional Autonoma de Mexico, Coba ClimatologicStation of the Comision Nacional del AguaMexico (CNA, Mexico), and the Lacandona ClimaticStation of the Comision Federal de Electricidad(CFE, Mexico) for providing climatic information.We thank C.J. Campbell, P.S. McDaniel,S.M. Lindshield, J.A. Weghorst, F. Garca,J. Jimenez, N.A. Argueta, and G.M. Rivera forallowing us to use some data of their unpublishedThesis. We also thank A. Di Fiore and two anon-ymous referees for useful comments. SSL thanks thetechnical support provided by the Instituto deNeuroetologa (UV) and Universitat de Barcelona.VAR thanks the financial support provided by theDireccion General de Asuntos del Personal Acade-mico (DGAPA-UNAM). VAR, KES, and OCBacknowledge the technical assistance provided byJ.M. Lobato-Garca, H. Ferreira, and A. Valencia-Garca. The Instituto de Ecologa A.C and Centrode Investigaciones en Ecosistemas (UniversidadNacional Autonoma de Mexico) provided logisticalsupport.

FA is grateful to the financial support from theNorth of England Zoological Society. The Institutode Ecologa A.C and Centro de Investigaciones enEcosistemas (Universidad Nacional Autonoma deMexico) provided logistical support.

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