Loud calls as a mechanism of social coordination in a fission–fusion taxon, the white-bellied spider monkey (Ateles belzebuth)

ORIGINAL PAPER

Loud calls as a mechanism of social coordinationin a fission–fusion taxon, the white-belliedspider monkey (Ateles belzebuth)

Stephanie N. Spehar & Anthony Di Fiore

Received: 13 November 2012 /Revised: 10 March 2013 /Accepted: 11 March 2013 /Published online: 7 April 2013# Springer-Verlag Berlin Heidelberg 2013

Abstract Spider monkeys (Ateles spp.) live in social groupsthat exhibit high levels of fission–fusion dynamics, in whichgroup members form subgroups of varying sizes and com-positions. Within these fluid societies, how individuals es-tablish contact with dispersed group members with whomthey might choose to associate remains unclear. Long-rangevocalizations might facilitate interactions between groupmembers and provide a means of social coordination infission–fusion societies. We evaluated this possibility forone spider monkey vocalization, the loud call, by examiningcalling behavior, the relationship between loud calls andchanges in subgroup size, and the response of individualsto distant calls and playback experiments in a single studygroup. We found that 82 % of loud calls were emitted within30 min of a call from a different location, suggesting thatindividuals frequently emit loud calls in response to the callsof distant group members. Subgroups that emitted loudcalls, especially those that responded to distant calls, weremuch more likely to experience an increase in subgroup sizewithin an hour after calling than those that did not. Animalsalso approached distant loud calls more than they avoided orignored these calls. Finally, playbacks of male calls demon-strated that females respond preferentially to the calls ofsome individuals over others. Taken together, these results

provide support for the hypothesis that spider monkey loudcalls function to facilitate and initiate interactions betweendispersed group members and suggest that vocal signals canplay an important role in influencing social interactions infission–fusion societies.

Keywords Ateles . Communication . Loud calls . Fission–fusion . Vocalizations . Social interactions

Introduction

Spider monkeys (Ateles spp.), like a handful of other mam-malian taxa (e.g., spotted hyenas, Crocuta crocuta: Kruuk1972; Smith et al. 2008; some species of dolphin, familyDelphinidae: Connor et al. 2000; Parra et al. 2011; Africanelephants, Loxodonta spp.: Wittemyer et al. 2005; Archie etal. 2006; chimpanzees, Pan troglodytes: Goodall 1986;Nishida 1968; and many species of bat, order Chiroptera:Kerth 2008), live in societies that exhibit high levels offission–fusion dynamics (Aureli et al. 2008). Such societiesare characterized by temporal and spatial fluidity in group-ing patterns, where members of a social group are not inconstant association but instead form subgroups of varyingsizes and compositions that travel, feed, and even sleepindependently from one another (Klein 1972; Cant 1977;van Roosmalen 1985; Ahumada 1989; Chapman 1990a;Aureli et al. 2008). Flexibility is the hallmark of societieswith high degrees of fission–fusion dynamics, and subgroupsize and composition change frequently, often several timesper day (Symington 1990; Boesch 1996; Suarez 2003).These complex social dynamics are generally thought tohave evolved to minimize competition over patchily distrib-uted resources, which in the case of spider monkeys are ripefruits (Symington 1987, 1988; Chapman 1988, 1990a, b;Chapman et al. 1995; Asensio et al. 2009; Di Fiore et al.2009). In general, it seems that the flexibility afforded by

Communicated by C.L. Nunn

Electronic supplementary material The online version of this article(doi:10.1007/s00265-013-1520-y) contains supplementary material,which is available to authorized users.

S. N. Spehar (*)Anthropology Program, Department of Religious Studiesand Anthropology, University of Wisconsin Oshkosh,800 Algoma Boulevard,Oshkosh, WI 54901, USAe-mail: [email protected]

A. Di FioreDepartment of Anthropology, University of Texas at Austin, SACRoom 5.150, Mail Code C3200, Austin, TX 78751, USA

Behav Ecol Sociobiol (2013) 67:947–961DOI 10.1007/s00265-013-1520-y

fission–fusion sociality allows individual animals to adjustgroup size in response to resource availability, thus avoidingthe rapid depletion of food patches and the resulting costs ofincreased daily path length and travel time (Smith et al.2008; Asensio et al. 2009).

The high variability in spatial and temporal cohesion thatcharacterizes fission–fusion societies makes it difficult to ef-fectively describe social interactions and relationships be-tween individual group members. Associations, which arequantified as the amount of time dyads of individuals arefound in the same subgroup relative to the amount of timethey are found apart (e.g., Symington 1990; Ramos-Fernández et al. 2009), are frequently used as a proxy measureto characterize social relationships or “bonds” (cf. Ramos-Fernández et al. 2009; Parra et al. 2011) in fission–fusionsocieties. Despite the flexible nature of grouping patterns,there is substantial evidence that associations between indi-viduals in fission–fusion societies are not random. Multiplestudies have demonstrated that spider monkeys exhibit highlydifferentiated social relationships, with individuals preferen-tially associating with select group members (e.g., Symington1987; Chapman 1990a; Ramos-Fernández et al. 2009; Slateret al. 2009). Similar evidence of structured patterns of associ-ation has also been found in other fission–fusion taxa (e.g.,bats: Kerth and König 1999; Rhodes 2007; dolphins:Coscarella et al. 2011; Parra et al. 2011; Wiszniewski et al.2012; African elephants: Moss and Poole 1983; Wittemyer etal. 2005; spotted hyenas: Szykman et al. 2001; Wahaj et al.2004; Smith et al. 2007; raccoons, Procyon lotor: Prange et al.2011). However, the proximate mechanisms by which indi-viduals may initiate or coordinate interactions with othergroup members in the context of fluid grouping patternsremain generally unclear. Elucidating the mechanisms thatfacilitate social interactions in fission–fusion societies is cru-cial to understanding the factors influencing social relation-ships and, ultimately, social structure (defined as the quality,content, and patterning of social relationships: Hinde 1976) inthese societies.

Long-ranging vocal signals could play an important role inthe social lives of animals living in fission–fusion societies,and several studies of fission–fusion taxa have demonstratedthe importance of vocal signals in establishing, coordinating,andmediating interactions between dispersed individuals (e.g.,chimpanzees: Mitani and Nishida 1993; bats: Wilkinson andBoughman 1998; Chaverri et al. 2010; Furmankiewicz et al.2011; African elephants: Langbauer et al.1991; McComb et al.2003; Leighty et al. 2008; dolphins: Lammers et al. 2006). Forexample, Leighty et al. (2008) demonstrated that Africanelephant rumbles, which can carry over 2 km, promote spatialcohesion among separated group members, particularly closeassociates and social partners. Similar analyses have not yetbeen performed for spider monkeys or for many other fission–fusion taxa, and attempts to understand the social role of long-

distance vocal communication in fission–fusion taxa havebeen limited.

Spider monkeys produce two calls that are potential candi-dates for facilitating social contact between dispersed groupmembers: the whinny and the loud call. Several previousstudies have established the role of the spider monkey whinny(Klein 1972) in maintaining or establishing contact betweenindividuals (Chapman and Lefebvre 1990; Chapman andWeary 1990; Teixidor and Byrne 1997, 1999; Ramos-Fernández 2005, 2008). However, the maximum audiblerange of the spider monkey whinny is ∼300 m (Ramos-Fernández 2005; Spehar, personal observation). Dependingon the shape and size of a group’s home range—reportedspider monkey community home range sizes range from 60to over 900 ha (Spehar et al. 2010; Di Fiore et al. 2011)—individuals in different subgroups can regularly be separatedby distances of more than 2 km, and it is possible for in-dividuals to go days without encountering others. Whinniesmay allow individuals to maintain or establish contact withsubgroups or particular individuals that are nearby, but thesecalls cannot establish contact over long distances. The spidermonkey loud call, or “scream” (cf. Ramos-Fernández et al.2011), may be a better candidate for a vocalization that canestablish contact between dispersed subgroups or individuals.Loud calls are species-specific acoustic signals that carry overlong distances and are produced by many primate species(Gautier and Gautier 1977; Hohmann and Fruth 1995; Wichand Nunn 2002; Delgado 2006). The spider monkey loud callconsists of 2 to 14 repeated tonal or atonal call units, and evenin heavily forested environments, they can carry a distance ofup to 1 km or more (Eisenberg 1976; van Roosmalen 1985;Spehar 2006; Ramos-Fernández 2008; Gibson 2010; Ramos-Fernández et al. 2011; Online Resource 1). Unlike most otherprimate species in which loud calls are only produced by adultmales (Delgado 2006), the spider monkey loud call is pro-duced by both adult males and females (Spehar 2006). Thespider monkey loud call does not seem to be tied to a partic-ular behavioral context (Spehar 2006), and most species ofspider monkey seem to produce loud calls, although it may beproduced more frequently in some species and/or populationsthan others (Shimooka and Ramos-Fernández, personalcommunication).

As loud calls provide receivers with an indication of thesignaler’s location, studies of multiple primate species havehypothesized that these calls might allow conspecifics tominimize resource competition through avoidance orintergroup or intragroup spacing (Waser 1975, 1977;Robinson 1979, 1981; Sekulic 1982; Mitani 1985a;Raemaekers and Raemaekers 1985a, b; van Roosmalen1985; Clark and Wrangham 1993; Boinski 2000). The pos-sibility that loud calls might have been sexually selected andact as a means of mate attraction, selection, or defense hasalso been examined and seems especially likely for species

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in which only one sex (usually males) produces loud calls(Mitani 1985b, c, 1990; Steenbeek et al. 1999; Wich andNunn 2002; Wich et al. 2003; Snowdon 2004; Delgado2006) or when pair-bonded males and females engage in“duets,” possibly as an advertisement of their pair bond (e.g.,gibbons: Chivers and MacKinnon 1977; Mitani 1984).Finally, and particularly relevant for fission–fusion societies,loud calls may allow individuals to maintain or establishcontact with widely dispersed conspecifics (Mitani andNishida 1993; Clark and Wrangham 1994; Notman andRendall 2005; Delgado 2006). For example, Mitani andNishida (1993) examined the social and behavioral correlatesof the male chimpanzee loud call, the pant–hoot, and foundevidence that these calls served to “maintain contact with andrecruit allies and associates” (p. 735). Similarly, the spidermonkey loud call could effectively function as a coordinatingsignal or “beacon” (cf. Delgado 2006), indicating the locationof subgroups or individuals relative to one another and facil-itating interactions between group members. Researchershave suggested that the spider monkey loud call may promoteassembly and serve as an identifier (Eisenberg 1976; Ramos-Fernández 2008) and/or may allow individuals in separatesubgroups to monitor the relative locations of other groupmembers (Ramos-Fernández et al. 2011). However, to date,the function of the spider monkey loud call has not beensystematically investigated.

In this paper, we investigate the hypothesis that the spidermonkey loud call may be a way that these animals initiate orcoordinate interactions with others (the social coordinationhypothesis). We also consider how well our data matchalternative hypotheses for the functions of these calls, asdifferent hypotheses that have been proposed for loud callfunction are not necessarily mutually exclusive. Predictionsfor our primary hypothesis and the overlap between ourprimary hypothesis and possible alternative and/or related

functions of loud calls are outlined in Table 1, where eachprediction is related to a particular combination of dataabout calling behavior and responses to calls.

First, we examine the temporal pattern of loud call emis-sion by spider monkeys. If loud calls allow individuals toidentify the locations of others and to possibly initiate in-teractions with other animals by adjusting their movementpatterns, then we expect individuals to effectively exchangeinformation about their respective locations by regularlyresponding to the calls of others. Thus, calls should have aclumped distribution in time, rather than being randomlydistributed over time. Second, we examine the influence ofloud calls on changes in subgroup size. If loud calls allowindividuals to maintain or establish contact with each other,then we expect these calls to be correlated temporally withchanges in subgroup composition. In particular, loud callsemitted within a group may attract other individuals,resulting in a subgroup fusion event (Chapman andLefebvre 1990; Ramos-Fernández 2005, 2008). Third, weexamine the nonvocal behavioral response of spider mon-keys to loud calls, specifically the influence of loud calls onsubsequent movement patterns. If loud calls allow individ-uals to initiate or coordinate interactions with others, thenwe expect receivers to respond behaviorally to extra-subgroup loud calls by changing their location or the orien-tation of their movement after hearing a call, specifically bymoving toward distant calls. Finally, we examine experi-mental data: the responses of group members to playbacksof the loud calls of known individuals. If loud calls serve asa means of initiating social interactions with specific others,it is crucial that spider monkeys be able to distinguishbetween the calls of different individuals and respond ac-cordingly. Evidence for such individual discrimination be-tween callers has been demonstrated for the spider monkeywhinny (Teixidor and Byrne 1999), for the calls of other

Table 1 Leading hypotheses for the function of primate loud calls

Predictions Social coordination: callsfacilitate interactionsbetween individuals

Spacing: calls allow individualsto maintain spacing and avoidcompetition

Sexual selection: callsfunction as means of mateattraction or selection

Calls by different individuals areclumped in time

X X

Calls have an attractive function(receivers generally approach caller)

X X

Calls have a repellent function(receivers generally avoid caller)

X

Calls increase likelihood of joiningor being joined by other individuals(i.e., subgroup size increases)

X

Receivers can discriminate betweenthe calls of different individuals

X X

Calls or calling behavior is sexuallydimorphic

X

An “X” indicates that a positive response is expected for that prediction

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primate species (e.g., Cheney and Seyfarth 1980, 1982,1988, 1990; Steenbeek and Assink 1998; Wich et al. 2003;Wich and de Vries 2006), and for calls of other fission–fusion taxa (dolphins: Sayigh et al. 1999; spotted hyenas:Benson-Amram et al. 2011). Playback experiments utilizingcalls of known individuals allow us to examine the effect ofthe caller’s identity on individual responses to loud calls.

One of the presumed benefits of a fission–fusion soci-ety is that it minimizes resource competition by allowingindividuals to vary when and how often they associatewith others. Individual state or context may thus influencewhether individuals choose to call and potentially attractothers. For example, the sex of the caller may influencecalling behavior; male spider monkeys, who are generallyreported to be more social or “gregarious” than females(Chapman 1990a; Symington 1990; Shimooka 2003), maycall more than females, who are presumably moreconstrained by resource competition and should be lesslikely to risk increasing feeding competition by initiatinginteractions with others (Chapman et al. 1995). In partic-ular, males could use long-ranging vocal signals to initiatecontact and coordinate movement with other males(Mitani and Nishida 1993; Watts and Mitani 2001;Aureli et al. 2006; Wallace 2008). Similarly, femaleswho have a dependent infant or who are pregnant, whichare subject to additional energetic constraints, would per-haps call less, in order to avoid attracting other animalsand thereby increasing resource competition. Social con-text may also influence calling behavior or responses tocalls; for example, individuals in larger subgroups may beless likely to respond to distant loud calls than individualsin smaller subgroups, as increasing the size of alreadylarge groups may increase resource competition to intol-erable levels (Mitani and Nishida 1993). Therefore, wealso examined the possible influence of sex, female repro-ductive status, and social context on individual callingbehavior and responses to calls.

Methods

Study site

This study was conducted in Yasuní National Park, Ecuador(∼76° W, 01° S), an approximately 900 km2 primary tropicalrainforest reserve located in the northeastern corner of thecountry (Fig. 1). Yasuní National Park has no pronounceddry season, with no month receiving <150 mm of rain andaround 3,200 mm falling annually (Di Fiore 1997; Pitman etal. 2002). This region, part of the Napo Moist Forests ofWestern Amazonia, is an area of exceptionally high biolog-ical diversity (Bass et al. 2010) and is home to 10 species ofnonhuman primate (Di Fiore 2001). The study site, theProyecto Primates Research Area (75°28′ W, 0°42′ S), liesin the northwestern portion of the park, adjacent to a roadbuilt in the early 1990s as part of petroleum development inthe region. The topography of the site consists of largeridges interspersed with ravines created by runoff streams.The site contains over 30 km of cut and mapped trails,which are marked every 25 m.

Study animals

A single habituated community of white-bellied spidermonkeys (Ateles belzebuth belzebuth) served as subjectsfor this study. At the onset of the study (2003), this groupconsisted of 5 adult males, 12 adult and subadult females,and 5 female juveniles; at the end of the study (2004), thegroup consisted of 3 adult males, 10 adult and subadultfemales, and 4 female juveniles. Disappearances and im-migrations account for the range in numbers of individualsacross the study period. Individual identification of allstudy animals was possible using facial markings, pelagecoloration, distinguishing marks on the genitalia, crookedfingers, and other individual characteristics. Subadultswere easily distinguished from adults and juveniles; they

Fig. 1 Map of the study siteand its location in Ecuador

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traveled independently from adults, but were visibly smallerand thinner than adults and had not yet acquired adult pigmen-tation on their faces (e.g., areas of skin around the eyes andmouth remained pink and unpigmented). Juvenile age wasestimated based on body size and the degree of independencefrom the mother (amount of time carried vs. independentlocomotion).

Female reproductive status

Female spider monkeys have an ovulatory cycle that isapproximately 28 days long, and breeding occurs year-round (Hernandez-Lopez et al. 1998; Campbell et al.2001; Campbell 2004, 2006). Females do not exhibit anyvisible signals indicating estrus or ovulation, and their re-productive status is, therefore, difficult to assess. For thisstudy, then, we inferred the reproductive status of femalesusing a number of cues; these included observed matings (asfemales generally mate only when they are reproductivelyactive; Campbell 2004) and births, as well as the presence ofdependent offspring and the estimated age of these off-spring. As spider monkeys generally have a 3-year interbirthinterval in the wild (Di Fiore and Campbell 2007), it wasassumed that, if females had an offspring older than 3 years,they were likely to be cycling. The reproductive status offemales who were observed to give birth during the studyperiod (n=2) were assigned post hoc; they were assumed tobe not cycling for 6 months prior to the birth (as femalespider monkeys have gestation periods of approximately6 months) and were presumed to have been cycling priorto that 6-month period. For one of these females, we had nocalling or behavioral data during the time when she waspresumed pregnant, and her infant disappeared almost im-mediately after it was first seen and she presumably begancycling soon afterwards; she was thus categorized as “re-productively active” for our entire data set. The other femalewas categorized as “reproductively active” before the pre-sumed beginning of her pregnancy and “reproductivelyinactive” during the time she was presumed pregnant andwhen she was nursing her dependent infant. Overall, ourdata set consisted of n=7 females who were categorized as“reproductively active” for all or part of the study and n=6females who were categorized as “reproductively inactive”for all or part of the study.

Behavioral and vocal data collection

Behavioral data were collected by the lead author (SNS),assisted by one to two field assistants, from June 2003 throughNovember 2004 (excluding January 2004 and June–August2004) for a total of 14 months of behavioral data collection.Data were collected through dawn-to-dusk focal animal fol-lows on all adult males (n=5) and adult and subadult females

(n=12) in the community. Group scans every 15 min recordedtotal subgroup size, composition, and location. Location re-cords were taken from the estimated center of the subgroupand were recorded as the distance and compass direction frommapped trail points and trees in which the monkeys had beenobserved feeding (∼3,000 marked trees). A subgroup wasdefined as any number of community members that wereassociating together, taking part in coordinated activities,and maintaining relatively close spatial contact (within∼100 m of other subgroup members, as this was judged tobe the distance above which individuals would have difficultymaintaining nonvocal contact and coordination; Chapman1990a). An individual was considered a member of a sub-group if their presence was recorded by the observer during15-min group scans; we considered an individual as havingfissioned from a subgroup when their presence was notrecorded by observers for two or more consecutive groupscans (Chapman et al. 1993). Dependent infants and juvenileswere not included in subgroup counts.

The time and identity of the caller (if possible to deter-mine) were recorded continuously for all within-group loudcalls (defined as calls given by individuals within a focalanimal’s subgroup). The time and compass bearing from thecenter of a focal animal’s subgroup for all distant loud calls(defined as calls that were given by individuals who werenot members of a focal animal’s subgroup) were alsorecorded. We assumed that, if the observer could detect adistant loud call, then the focal animal and other subgroupmembers were also able to detect the call. Loud calls wererecorded as separate calling events if they were (1) producedby different individuals (determined through our identifica-tion of callers for within-group loud calls or, for distant loudcalls, if calls came from clearly distinct locations based oncompass bearings) or (2) produced by the same individualbut more than 1 min had passed between calls by thatindividual. If <1 min passed between successive loud callsby the same individual, these calls were considered part ofthe same calling “bout” and were regarded as single calls forall subsequent analyses.

Calculating individual call rate

Individual call rate was calculated by dividing the number ofseparate calls per individual by the number of hours spentobserving that individual. This included the number of hoursthat individual animal was the subject of focal follows as wellas the amount of time that the individual was present as anidentified member of another focal animal’s subgroup. Thiswas done because roughly 40–50 % of the calls that we wereable to assign to a specific individual were emitted when thatindividual was not a focal animal but was instead a member ofanother focal animal’s subgroup, and this allowed us to incor-porate these calls into our analysis. All individuals for whom

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we had fewer than 100 h of observation time (including focalhours and hours that the individual was a member of anotherfocal animal’s subgroup) were omitted from this analysis (n=2males and n=4 females of 17 nonjuvenile group members). Wedetermined 100 h was a cutoff because, upon examination ofthe distribution of observation hours across individuals, 100 hseemed to constitute a natural “break” between individuals whohad been followed infrequently vs. extensively (mean numberof observation hours per individual, 157.07±25.22), and settinga standard of 100 h of observation ensured that an individualhad been followed sufficiently to allow for confidence in ourassessment of how frequently they produce loud calls.

Temporal distribution of loud calls

We examined the frequency distribution for the amount oftime between successive calls emitted from different loca-tions in order to determine if calls made by individuals inseparate locations were emitted within a relatively short timeinterval of each other (thus, potentially indicating an ex-change of information about relative locations). To do this,we calculated the amount of time between successive loudcalls emitted by individuals in separate subgroups. Callswere judged to be from separate subgroups if the callerwas not a member of the subgroup the observer was follow-ing or, for distant calls, if calls came from clearly distinctlocations based on compass bearings. We placed each timemeasurement into one of eight possible categories (0000–0015 hours between successive calls from separate loca-tions): 0015–0030, 0030–0045, 0045–0100, 0100–0200,0200–0300, 0300–0400, and >0400 hours. Calls on dayswhen observers entered the study site after 0600 hours (ascalls are emitted from when the monkeys first become activein the morning), the first call heard on each day, and suc-cessive calls from the same subgroup with no interveningcalls by subgroups in a different location were omitted fromthis analysis, resulting in a data set of n=646 calls. It ispossible that distant callers who produced successive callsfrom the same location with no intervening calls detectedand whose calls were thus omitted from this analysis were infact responding to distant calls that observers could notdetect. However, this omission would result in anoverestimate of time between successive calls from separatelocations, rather than an underestimate, which runs counterto our predictions and would result in a more conservativeanalysis overall. Thus, we felt comfortable including timeinterval data related to these distant calls in our analyses.

The effect of loud calls on subgroup fissions and fusions

We examined the influence of both within-group and distantloud calls on changes in subgroup composition. To correctfor the fact that both distant and within-group loud calls

were often emitted within very short periods of each otherand thus may not be independent in their attractive func-tions, we only used within-group loud calls that were spacedapart in time by at least 1 h (n=104) and distant loud callsthat were emitted from clearly distinct spatial locations orwith >1 h between calls (n=129) for this analysis.

To examine the effect of loud calls on subgroup fissionsand fusions, we compared changes in subgroup size in thehour following the emission of these loud calls to changes insubgroup size in the hour following randomly selected con-trol points in time (n=500 scan records) when loud calls hadnot been produced by the subgroup being followed or beenheard at all by observers (and thus could not have influencedsubgroup changes). The interval of 1 h following either theemission of a loud call or a randomly selected control pointwas chosen because this interval is shorter than the averageinterval between changes in subgroup composition deter-mined from our overall data set (i.e., one change every 1.62 h, or 0.62 changes/h, based on an analysis of our data setof over 773.5 h of behavioral data from 193 focal follows inwhich we recorded 478 fission or fusion events).

Because there may be an underlying temporal pattern toboth calling behavior and changes in subgroup size,irrespective of the effect of the former on the latter, it isnecessary to select random control points in such a way as totake this effect into account. When we examined the tem-poral distribution of the calls to be used in this analysis (n=104 within-group calls and n=129 distant calls), we foundthat the majority (64 % for all these calls combined) wereemitted in the morning, before 1100 hours. Subgroup fis-sions and fusions also occurred more frequently in themorning—particularly the early morning—than at othertimes. Thus, to control for the effects of the similar temporalpatterning in calling behavior and subgroup changes on ouranalysis, we chose 64 % (matching the proportion of callsused in this analysis that occurred from 0600 to 1100 h) ofour randomly selected control points from data collectedbefore 1100 hours on days on which no loud calls had yetbeen emitted by the focal subgroup or heard (n=320 scanpoints), and the remaining 36 % of control points wereselected at random from data collected after 1100 hours onthese days (n=180 scan points).

Quantifying responses to loud calls

For the purposes of measuring behavioral responses to dis-tant loud calls, we utilized the direction of a focal animal’stravel during the hour following the emission of a distantloud call. A focal animal’s response to a distant call was thusclassified post hoc as either “approach,” “avoid,” or “neu-tral,” based on the focal animal’s bearing from the vectorbetween the distant caller’s estimated location and the focalanimal’s original location and whether the focal animal

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moved towards or away from the distant caller (OnlineResource 2). The focal animal’s response was considered“approach” if (1) the animal decreased rather than increasedthe distance between itself and the estimated location of thedistant caller and (2) if the bearing of the vector from thefocal animal’s original to subsequent location remainedwithin 45° of the bearing of the vector between the focalanimal’s original location and the distant caller’s estimatedlocation (see Online Resource 2). This was considered an“approach” because the focal animal was thus observed tobe moving in the general direction of the caller; this move-ment pattern could result in an actual encounter with thecaller. We classified a focal animal’s response to a distantloud call as “avoid” if (1) the animal increased rather thandecreased the distance between itself and the estimatedlocation of the distant caller and (2) if the bearing of thevector from the focal animal’s original to subsequent loca-tion was >135° of the bearing of the vector between thefocal animal’s original location and the distant caller’s esti-mated location (see Online Resource 2). We considered thismovement pattern an “avoid” because the focal animalwould then be moving away from the distant caller andessentially in a direction opposite that of the caller; thisdirection of movement made an encounter with the distantcaller very unlikely. Finally, we classified a focal animal’sresponse as “neutral” if the bearing of the vector from itsoriginal to subsequent location was between 45° and 135° ofthe bearing of the vector between the its initial location and thedistant caller’s estimated location (see Online Resource 2),regardless of whether the focal animal’s distance to the loca-tion of the distant caller increased or decreased. This responsewas considered “neutral” because, even though the focalanimal could potentially have decreased the distance betweenitself and the distant caller and remained within the “neutral”zone, the direction of movement made it less likely that thefocal animal would actually encounter the distant caller.

When focal animals were tracked for up to an hour follow-ing distant loud calls, the observer (and presumably the animalitself) sometimes heard multiple independent distant loud calls(range, 2–4) from different locations at roughly the same time.In these instances, we analyzed only one response, favoring“approach” over “avoid” or “neutral” if there was a discrep-ancy between responses to different roughly synchronouscalls. That is, we scored “approach” whenever an individual’smovement pattern could be categorized as “approach” to atleast one distant loud call, even if its movement could bescored as “avoid” and/or “neutral” for other calls heard aroundthe same time. This process left us with a total of 69 indepen-dent cases where we could analyze a focal animal’s movementsubsequent to hearing a distant loud call (n=53 cases in whichonly one loud call was heard in the hour preceding the followand n=16 cases for which we went through the processdescribed previously in order to analyze only one response).

Playback stimuli and experiments

Playback stimuli were selected from loud calls recorded adlibitum from three adult males in the community (Br, Ak, andEy) during focal follows from June 2003 to April 2004 using aSennheiser ME60 shotgun microphone and a Sony MZ-N1portable minidisc recorder, set to record at the highest-qualitylevel (stereo mode). Only high-quality recordings that wererecorded at distance of 20–30 m from the caller and containedminimal interfering background noise (i.e., bird calls) wereconsidered for playback experiments (four to five calls foreach male). Calls were digitized (16 bit, 44.1 kHz) onto aMacintosh computer and each recording was edited using adigital sound analysis program, Canary 1.2.1, and a digitalediting program, Digital Performer 4.0. For each call, weomitted sound immediately before and after the call; in somecases, call elements, or “units,” within a single call wereremoved and/or duplicated in order to create cleaner callexemplars and increase our sample size, following Delgado(2003). Call elements were selected for omission or duplica-tion based on the signal-to-noise ratio for that portion of thecall or, if this was not an issue, randomly. The first and last unitof each call was always preserved, and any edits ensured thatcalls remained within the range of variation for call durationand number of call elements per call for each male as thesefeatures might be salient for individual recognition. We en-sured that each male exemplar was subject to some form ofediting to control for this possible source of variation in femaleresponse. This process left us with a set of 4–5 exemplars foreach male (n=14 exemplars total). Playback stimuli were thenchosen from this set of exemplars for experiments in the fieldbased on the individuals present in the subject subgroup andwhen and how frequently members of that subgroup had beensubject to prior playbacks of different calls by each male. Toavoid habituation, we minimized the number of times eachindividual was presented with each playback stimuli; individ-uals were never played the same call exemplar more thanonce. Male calls were chosen as exemplars for these experi-ments because we had the largest set of recorded calls frommales and because conducting only playbacks of the calls ofone class of individuals (males) to another class of individuals(females) allowed us to control for the possible influence of atleast one variable (sex) on responses to calls.

Playback experiments were conducted from October toDecember 2004 by two observers in constant contact by two-way radio; one observer (always SNS) was responsible forobserving the monkeys, and the other positioned and operatedthe playback speaker. All adult and subadult females present inthe spider monkey community at that time (n=9) were potentialsubjects for playback trials. Subgroups were followed for atleast a half hour before a playback was conducted, and play-backs were conducted only when the subgroup was stationary.Focal subjects were chosen randomly from visible individuals.

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At least 5 min of baseline data were collected on the focalsubject before a playback trial, and playbacks were notconducted when a potentially disturbing event (e.g., within-group conflict) had occurred within the last half hour.Playbacks were initiated when the focal subject was not en-gaged in any active social behavior (e.g., grooming or playing).Playbacks were only conducted in subgroups in which allindividuals could be identified, ensuring that the male whosecall was used as playback stimulus was not present.

Playback calls were amplified with a Crate TX30 portablespeaker connected to a Sony CD player. Playback volume wasadjusted to the natural loudness of calling males (approxi-mately 100 dB at 1 m, measured using a digital sound meter).All playbacks were conducted at a distance of 100–150 mfrom the subject, and the playback speaker was elevated up to8 m in a tree when this was necessary to ensure the speakerwas at a higher elevation than the subject. No more than threeplaybacks were conducted in a day, and playbacks on thesame day were separated by at least 1 h. Playback experimentsusing the calls of each male were distributed roughly evenlyacross hours of the day, and playbacks were never conductedbefore 0700 hours (to allow time for preexperiment observa-tion) or after 1600 hours (to avoid travel to sleeping sitesinterfering with responses to playbacks).

Two types of reactions to a playback experiment weregauged for this study: (1) immediate response to the playbackand (2) delayed response to the playback. Immediate re-sponses to playbacks were gauged in the first 60 s followingplayback and were placed in one of four mutually exclusivecategories of behavior: ignore (the subject showed no visibleresponse to playback and no change in immediate behavior),look/orient (the subject turned its head or oriented its body inthe direction of the playback speaker), move towards (thesubject immediately began moving in a direction that de-creased the linear distance between herself and the stimulusby at least 25 m), and move away (subject immediately beganmoving in a direction that increased the linear distance be-tween herself and the stimulus by at least 25 m). Delayedresponse to playback trials was determined by assessing thedirection and distance of the subject’s next travel bout, usinglocation points recorded every 15 min during focal data col-lection. A focal animal’s delayed response to a distant call wasclassified using the same criteria outlined previously to quan-tify the behavioral response to distant loud calls.

Results

Distribution of loud calls over time

Of the 773 separate loud calls recorded by observers (bothwithin-group and distant) during this study, 32 % (n=246)was emitted within 1 min after hearing a loud call by a

different individual. An additional 32 % of calls (n=248),while not emitted within 1 min of a previous call, wasfollowed within 1 min by a call by a different individual(either another individual within the same subgroup or anindividual in a separate location from the caller). Overall,64 % (n=494) of all loud calls heard during this studyoccurred within 1 min of a call by a different individual.

An analysis of the distribution of successive loud callsgiven from separate locations relative to one another (Fig. 2)demonstrates that 82 % of loud calls were emitted within30 min of a call given by a different individual in a separatelocation (n=646 calls; mean time between successive calls bydifferent individuals, 0019±0101 hours; range, 0000–0856 hours). In order to test the significance of this distribu-tion, we compared the observed temporal distribution of callsto a Poisson distribution. Successive calls from animals indifferent subgroups were separated much less in time thanexpected by chance, indicating that calls were temporallyclumped (p=0.01 or less for all categories but 0045–0100 hours; goodness-of-fit to Poisson distribution: χ2=9,133.74, df=35, p<0.0001). A Kolmogorov–Smirnov anal-ysis also indicates that the distribution of calls is significantlydifferent from the expected distribution of calls, based on thePoisson distribution (D=0.80, critical value=0.06, p<0.01).

Changes in subgroup size

We found that subgroups that emitted loud calls were sig-nificantly more likely to experience a change in subgroupsize—specifically an increase in subgroup size—within thefollowing hour than were subgroups that had not yet emittedor heard a loud call on a given day (χ2=35.78, p<0.001;Table 2). Subgroups that had heard a distant loud call werealso more likely to experience an increase in subgroup sizewithin an hour than were subgroups that had not yet emitted

Fig. 2 Distribution of successive spider monkey loud calls over time

954 Behav Ecol Sociobiol (2013) 67:947–961

or heard a loud call on a given day (χ2=30.45, p<0.001;Table 2).

Distant loud calls were frequently followed by a loud callfrom a focal animal’s subgroup; out of the 129 distant loudcalls heard while following a subgroup, 51 % was followedby a within-group loud call within 30 min and 60 % wasfollowed by a within-group loud call within an hour. Wefound that subgroups that responded vocally to distant callswithin 1 h were joined significantly more often thanexpected by chance within the following hour (χ2=37.18,p<0.001; Table 3), while subgroups in which no loud callswere emitted within an hour of hearing a distant call werenot joined more often than expected (χ2=4.19, p=0.12;Table 3). We also found that subgroups that emitted callswithin an hour of hearing distant caller were, on average,slightly larger than those subgroups that did not (subgroupsthat emitted calls: n=78, mean size of 4.10±0.33 individ-uals; subgroups that did not emit calls: n=51, mean size of3.33±0.24 individuals; Mann–Whitney U=1,494, p=0.02).

Nonvocal behavioral responses to loud calls

Males and females both approached distant loud calls sig-nificantly more often than expected (Table 4). Sex did notappear to have a significant effect on this behavioralresponse of individuals to distant calls (χ2=0.99, df=2, p=0.61) nor did female reproductive status (χ2=0.46, df=2,

p=0.79). There was also no significant difference in the sizeof the subgroup of individuals who approached, avoided, orremained neutral in their movement patterns relative todistant loud calls (approach, n=38, mean subgroup size of4.66±0.40 individuals; neutral, n=15, mean subgroup sizeof 3.6±0.62 individuals; avoid, n=13; mean subgroup sizeof 3.38±0.51 individuals; Kruskal–Wallis H=3.69, df=2,p=0.16).

We also analyzed these data to determine if individualswho approached distant calls were more likely to experiencean increase in subgroup size than those who avoided orremained neutral relative to distant calls. Of the cases inwhich focal animals approached distant loud calls (n=39cases), 49 % experienced an increase in subgroup size overthe next hour, while of those cases in which the focal animalavoided or remained neutral relative to a distant caller (n=30 cases), 37 % experienced an increase in subgroup size;however, this difference did not reach significance (χ2=1.14, df=3, p=0.57). As subgroups may increase in size intwo ways after a loud call—i.e., by approaching a distantcaller or by having a distant caller approach them—we alsoexamined whether subgroups that did not approach a distantcaller (avoided or remained neutral) but did emit a loud callwithin the next hour (n=16) were more likely to experiencean increase in subgroup size than those subgroups that didnot approach and also did not emit a loud call (n=14). Wefound that, of subgroups that did not approach distant callersbut did emit a loud call, 44 % experienced an increase insubgroup size, compared to 29 % of those that did not emit acall; however, this difference was also not significant (χ2=0.74, df=2, p=0.39).

Playback experiments

We conducted 53 playbacks of male calls to female subjects(Br calls, n=21; Ey calls, n=17; Ak calls, n=15). Welumped responses across females because of our small sam-ple size of experiments conducted to each individual (n=9females, with a mean of 5.89±0.58 calls to each). We feltcomfortable doing this because each female was played acall by each male at least once, and the proportion of thetotal calls played to each female represented by the calls of

Table 3 Changes in size for subgroups in which loud calls were emitted within an hour of hearing a distant call and for subgroups in which no loudcalls were emitted within an hour of hearing a distant call

Time before next within-group loud call Increase within hour Decrease within hour No change within hour Significance

≤1 h 41 7 30 χ2=34.74, p<0.00118.86 8.11 51.01

>1 h 17 4 30 χ2=2.42, p=0.3012.34 5.31 33.35

Expected values are in italics and were calculated using random points in time (n=500) selected from data collected when no loud calls had yet beenemitted or heard and controlling for temporal patterning in calling behavior and subgroup fissions and fusions

Table 2 Changes in subgroup size in the hour following distant andwithin-subgroup loud calls

Call type Increase Decrease No change Significance

Distant loud calls(n=129)

58 11 60 χ2=30.45,p<0.00131 14 84

Within-group loudcalls (n=104)

51 10 43 χ2=35.78,p<0.00125 11 68

All loud calls(n=233)

109 21 103 χ2=9.26,p=0.0157 24 152

Expected values are in italics and were calculated using random pointsin time (n=500) selected from data collected when no loud calls hadyet been emitted or heard and controlling for temporal patterning incalling behavior and subgroup fissions and fusions

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individual males did not differ significantly between fe-males (mean proportion of exemplars played to each femalerepresented by individual males: Oso, 0.35±0.06; Sako,0.30±0.05; Deye, 0.35±0.05; Kruskal–Wallis H=0.60,df=2, p=0.74). Playbacks commonly elicited some sort ofimmediate response by playback subjects; females looked inthe direction of the playback speaker 74 % (SE=3 %) of thetime and ignored playbacks only 9 % (SE=3 %) of the time.Females rarely moved immediately toward or away fromplaybacks (15±5 and 2±2 % of the time, respectively).Females did not show stronger immediate response to onemale over another (female responses lumped into two cate-gories, “ignore” and “respond,” for each male to addresssmall observed and expected values; χ2=0.91, df=2, p=0.63). When we examined the delayed response of females,however, we found that females approached the speakernearly twice as often after playbacks of Br’s loud calls thanplaybacks of calls by Ak and Ey (χ2=11.25, df=4, p=0.004). Playbacks of Br’s calls were approached more andavoided less often than expected by chance, while the callsof Ey and Ak resulted in movement patterns that did notdiffer from expected (Table 5).

Effect of sex and reproductive status on calling rate

Analysis of individual call rate indicates that males pro-duced loud calls at a significantly higher rate than didfemales (males: mean=0.18±0.10 calls/h, n=3 males forwhom we had more than 100 h of behavioral observation;females: mean=0.04±0.01 calls/h, n=8 females for whomwe had more than 100 h of behavioral observation; Mann–

Whitney U=22, p=0.05; Fig. 3a). Female call rates rangedfrom 0.003 to 0.21 calls/h, while male call rates ranged from0.05 to 0.37 calls/h. We found no significant difference incall rates between females categorized as reproductivelyactive or cycling (n=6 females for whom we had more than100 h of behavioral observation) and females categorized asreproductively inactive or not cycling (n=3 females forwhom we had more than 100 h of behavioral observation)(reproductively active: mean=0.06±0.03 calls/h; reproduc-tively inactive: mean=0.04±0.02 calls/h; Mann–WhitneyU=14, p=0.26; Fig. 3b).

Discussion

Taken together, the results presented here provide supportfor the social coordination hypothesis (Table 1), i.e., that theloud call functions in facilitating and initiating interactionsbetween group members within the fission–fusion societiesof spider monkeys. Our results suggest that individualscommonly emit loud calls in response to the calls of distantgroup members, allowing calls to constitute an exchange ofinformation about current location between distant signalersand providing a potential means of coordinating individualor group movement (e.g., Byrne 1981a, b; Boinski 1991,1996; Hohmann and Fruth 1994). Such temporal“clumping” is also in keeping with the predictions of anoth-er possible explanation of loud call function, the spacinghypothesis (Table 1), as this kind of exchange could alsoallow individuals to avoid each other to maintain spacingand minimize resource competition. However, the role of

Table 4 Behavioral response of males (n=4 individuals) and females (n=9 individuals) to distant loud calls

Approach Neutral Avoid Significance

Males (n=21) 13 (62 %) 5 (24 %) 3 (14 %) χ2=15.29, p<0.0015.25 (25 %) 10.5 (50 %) 5.25 (25 %)

Females (n=48) 26 (54 %) 10 (21 %) 12 (25 %) χ2=24.50, p<0.00112 (25 %) 24 (50 %) 12 (25 %)

Expected values for each cell are in italics and are based on the chance that the subject would move into each of the movement categories (approach,avoid, and neutral), assuming an equal chance of moving in any direction following a distant call

Table 5 Behavioral responses of females (n=9) to playbacks of male loud calls

Approach Neutral Avoid Significance

Br (n=21) 12 (57 %) 7 (33 %) 2 (10 %) χ2=11.85, p=0.0035.25 (25 %) 10.5 (50 %) 5.25 (25 %)

Ey (n=17) 5 (29 %) 7 (41 %) 5 (29 %) χ2=0.53, p=0.774.25 (25 %) 8.5 (50 %) 4.25 (25 %)

Ak (n=15) 1 (7 %) 10 (67 %) 4 (26 %) χ2=2.87, p=0.243.75 (25 %) 7.5 (50 %) 3.75 (25 %)

Expected values for each cell are in italics and are based on the chance that the subject would move into each of the movement categories (approach,avoid, neutral), assuming an equal chance of moving in any direction following a playback

956 Behav Ecol Sociobiol (2013) 67:947–961

loud calls in facilitating social interactions within spidermonkey groups is further supported by our results demon-strating the relationship between loud calls and subgroupfusions and by the behavioral responses of individuals todistant loud calls. Subgroups that emitted loud calls weremore likely to be joined within an hour than those that didnot. We also found that subgroups that heard a distant loudcall were more likely to be joined than those that did nothear distant calls (Table 2). This is likely because the ma-jority of subgroups that heard distant loud calls (60 %)responded vocally within an hour, and those subgroups thatresponded had a significantly higher chance of experiencingan increase in subgroup size within the hour than those thatdid not (Table 3). Therefore, it appears that emitting loudcalls (and especially responding to the distant calls ofothers) substantially increases the likelihood that an individ-ual or subgroup will be joined within the following hour.

Indeed, we found that individuals approached the loud callsof distant individuals more often than they avoided or ef-fectively ignored these calls, and at a frequency greater thanexpected by chance (Table 4).

We should note here that personnel limitations did notallow us to conduct simultaneous follows of different sub-groups, thus we were not able to confirm the accuracy of ourestimates of the locations of distant callers. It is possible thatan error in the estimate of the direction of a distant callercould result in a miscategorization of the receiver’s subse-quent movement bout. We have no way of determining if, orhow often, this was the case for our analysis. However, wealso see no reason for our direction estimates to be biased insuch a way as to inflate the proportion of “approach” re-sponses. The fact that the majority of receivers approacheddistant callers despite this movement pattern being muchless likely than that of remaining neutral relative to thedistant caller’s location—along with results of our playbackexperiments in which the source of the distant call wasknown and which demonstrate that distant callers werefrequently approached by receivers—suggest that these re-sults are likely to be reliable.

Overall, our data documenting a relationship betweenloud calls and subgroup joining events and a general attrac-tive function of loud calls suggest that an important functionof the spider monkey loud call is to facilitate social interac-tions between group members. However, it is also clear thatcalls do not always result in joining events or in receiversresponding in ways that would facilitate interaction withothers. For example, 40 % of distant calls did not result ina vocal response from individuals within a focal animal’ssubgroup within an hour. Refraining from calling in re-sponse to others appears to be an effective way to avoidinteraction, as subgroups that did not emit a loud call inresponse to distant calls increased in size significantly lessoften over the next hour than did subgroups that did re-spond. Furthermore, although both males and femalesapproached distant callers far more often than expected,they still remained neutral or moved away from distantcallers ∼35 % of the time. We found no relationship betweensex or female reproductive status and the likelihood ofresponse to distant callers, suggesting that these factors donot substantially influence the likelihood that an individualor subgroup will respond to (or ignore) the calls of others.We also found that subgroup size did not influence whethersubgroups approached, avoided, or remained neutral relativeto a distant caller. We did, however, find a relationshipbetween subgroup size and likelihood of vocal response todistant callers: subgroups that responded within an hour todistant calls were, on average, slightly larger than subgroupsthat did not respond (4.10 vs. 3.33 individuals). This is inthe opposite direction than expected, as we assumed thatindividuals in larger subgroups would be more likely to

a

b

Fig. 3 Mean call rate (±SE) for a males and females and b reproduc-tively active and inactive females. Significance or nonsignificance ofrelationship is indicated in each figure

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refrain from calling in order to avoid increasing competitionfor resources. However, it may be that larger subgroups aremore likely to contain individuals who could benefit fromattracting others and who are thus more likely to respond todistant calls. Our data on call rate does suggest that there is agreat deal of variation between individuals, even withineach sex, in how frequently they call, and the cost–benefitratio for responding to the calls of others is expected to varybetween individuals, depending on a number of consider-ations (e.g., rank, relationships with other individuals cur-rently in the subgroup, satiation, and so on; see succeedingparagraphs). It may be that the composition of subgroupsplays an important role in determining whether individualsrespond to distant calls. Finally, although our data suggestthat the call plays a role in the active coordination of in-teractions, these calls could also be used as a more passiveform of social monitoring (Ramos-Fernández et al. 2011):individuals might use calls to advertise their location andmonitor the locations of conspecifics, but may not alwaysmake immediate efforts to initiate direct contact.

Along these same lines, the complexity of spider monkeysocial networks may help to explain why distant calls aresometimes ignored or avoided. Studies to date indicate thatindividuals in fission–fusion societies, including spidermonkeys, are linked to other members of their social groupthrough both strong and weak bonds, which can vary basedon sex, age, and as-yet-undetermined individual consider-ations (Kerth 2008; Ramos-Fernández et al. 2009; Parra etal. 2011). If loud calls act as a mechanism for facilitatingcontact between group members, an individual’s position inthis social network and their relationships with other groupmembers could play an important role in determining theirdecisions about how they respond to distant loud calls.However, such decisions—and by extension the potentialrole of loud calls in coordinating interactions between spe-cific individuals—depends on the ability of individuals todistinguish between the calls of different individuals andrespond accordingly. Our playback experiments demon-strate that females do respond differently to the calls ofdifferent males; specifically, females approached the callsof one male far more often than the calls of the two othergroup males. Although we cannot be sure why femalespreferred male Br, our long-term observations of interac-tions between males and between males and females allowus to speculate that Br appeared to be more “socially cen-tral” or socially important than the other two males (domi-nance rank could not be determined). The strong preferenceof females for one male suggests that spider monkeys areable to distinguish between the calls of different individualsand respond preferentially to the calls of some individualsover others, which in turn suggests that spider monkey loudcalls do have the necessary acoustic features (detectableindividual variability) to coordinate interactions between

specific individuals. That such variability exists in spidermonkey loud calls is also supported by previous acousticanalysis of the loud calls of individuals from this commu-nity (Spehar 2006), which demonstrated variability in theacoustic structure of calls between males. However, thelimitations of our playback experiments (a sample size ofonly three males, and the necessity of lumping female re-sponses) makes it difficult to determine exactly what fe-males are able to detect from the acoustic structure of thecall without extensive further study.

The fact that sex influences individual call rate, withmales calling at higher rates than females, may providefurther indirect support for the role that the loud call playsin facilitating social interactions. Male spider monkeys, likechimpanzees, are generally philopatric and form strong so-cial bonds with other male group members to whom they arelikely related (Symington 1990; Chapman 1990a; Chapmanet al. 1995; Shimooka 2003; Ramos-Fernández et al. 2009;Slater et al. 2009). Male spider monkeys in many commu-nities studied to date also seem to engage in cooperativecommunity defense in the form of all-male “patrols” of thecommunity’s boundaries, much like chimpanzees (Chapman1990a; Watts and Mitani 2001; Shimooka 2005; Aureli et al.2006; Wallace 2008). It may, therefore, be very importantthat males be able to locate one another or indicate theirtravel direction to other males in order to initiate contact andcoordinate their movements for the purpose of cooperativecommunity defense. However, information on the rangingand association patterns of the community of spider mon-keys on which this study was conducted indicates that thisparticular group may not adhere to the male-bonded patternsseen in spider monkeys elsewhere (Spehar et al. 2010),perhaps due to low male–male relatedness (Di Fiore et al.2009). This suggests that another explanation for highermale call rate may be needed.

Higher male than female call rate is in keeping with analternative hypothesis for the function of loud calls, thesexual selection hypothesis, which predicts sexual dimor-phism in calling behavior (Table 1). Although sexual dimor-phism in calling behavior is generally manifest in primatesas only one sex (males) producing loud calls, a difference incalling rate between the sexes could also be interpreted asconsistent with this prediction. If male spider monkey loudcalls serve a sexually selected function, such as mate defense(e.g., by indicating male presence and defense of a particulararea, and the females within that area, from outside males;Waser 1975; Mitani 1985a, b, c; Wich and Nunn 2002), or as ameans of mate attraction and selection (e.g., by transmittinginformation that would allow females or males to assess amale as a potential mate or competitor; Steenbeek et al. 1999;Kitchen et al. 2003a, b; Fischer et al. 2004; Delgado 2006), wewould indeed expect males to call more frequently than fe-males. The results of this study demonstrating the generally

958 Behav Ecol Sociobiol (2013) 67:947–961

attractive function of loud calls and the potential forindividual variability in calls also fit the predictions ofthis hypothesis, suggesting that the spider monkey loudcall may have been subject to sexual selection. However,the fact that both males and females produce loud callsand the clear relationship we found between call emissionand subgroup joining events suggests that this call likelyfunctions in a much broader social context.

In summary, our data provide overall support for the socialcoordination hypothesis and suggest that the loud call is amechanism by which spider monkeys can, and often do,initiate social contact and interactions with other group mem-bers. Our results indicating the potential for individual vari-ability in the call and the ability of receivers to distinguishbetween callers are not conclusive, but they do allow us tospeculate that the call might allow individuals to make in-formed decisions about when and where they associate withparticular others, functioning to initiate social interactionsbetween individuals in spider monkey society. Confirmationof this possibility, of course, requires further testing. Thesocial coordination function of the loud call is not incompat-ible with additional functions of mate attraction and selection,and it is possible that loud calls may also function in this way,particularly for males. The spider monkey loud call may thusbe most accurately characterized as a coordinating signal or“beacon” (cf. Delgado 2006) that provides information aboutthe location and possibly the identity of the caller and facili-tates interactions between widely dispersed group members.The evidence presented here, combined with previous studiesof the role of vocalizations in the social lives of other fission–fusion taxa, suggests that certain vocal signals may be animportant way that individuals mediate social interactionsover long distances in fission–fusion societies.

Acknowledgments We would like to thank the Ministerio deAmbiente of the government of Ecuador for their continued supportof the long-term primate research in Yasuní National Park. Logisticalsupport for this study was provided by the Estación Cientifica Yasuníof the Pontificia Universidad Católica del Ecuador. We are also gratefulto the Maxus Ecuador, Inc., Repsol-YPF, and the Waorani communi-ties in the region for providing additional logistical support and per-missions. We are indebted to Wampi Ahua, Dylan Schwindt, SethKolloen, and Paul Mathewson for providing invaluable assistance incollecting behavioral data in the field and to Wilmer Pozo, Larry Dew,Andres Link, and Scott Suarez for habituation and background behav-ioral work on the study group, which facilitated this research. YukikoShimooka and Gabriel Ramos-Fernández provided valuable and muchappreciated comments and information on spider monkey loud calls inother study populations, and the constructive suggestions of the Asso-ciate Editor and two anonymous reviewers have greatly improved thismanuscript. Financial support was provided by the National ScienceFoundation, the L.S.B. Leakey Foundation, Primate Conservation,Inc., New York University, and the New York Consortium in Evolu-tionary Primatology.

Ethical standards All appropriate institutional permissions and eth-ical approvals were obtained for this research, and all research

undertaken adhered to the relevant laws of the country in which it tookplace (Ecuador).

Conflict of interest The authors declare that they have no conflict ofinterest.

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