do predators and thermoregulation influence choice of ......predation and thermoregulatory...

Do Predators and Thermoregulation InfluenceChoice of Sleeping Sites and Sleeping Behaviorin Azara’s Owl Monkeys (Aotus azarae azarae)in Northern Argentina?

Amanda Savagian1&

Eduardo Fernandez-Duque2,3,4

Received: 24 June 2016 /Accepted: 12 November 2016# Springer Science+Business Media New York 2016

Abstract The spatiotemporal aspects of sleeping behavior are indicative of the eco-logical pressures that primate species face. We investigated the potential influence ofpredation and thermoregulatory constraints on sleeping site choice and sleep-relatedbehaviors in a population of cathemeral owl monkeys (Aotus azarae azarae) inFormosa, Argentina. During 10 mo, we recorded data on 153 diurnal sleeping bouts(N = 5 groups), sleeping tree physical characteristics (diameter at breast height [DBH],height, foliage), sleeping sites within the tree, and grouping and positional behaviorwhile sleeping. We also conducted a vegetation survey of potential sleeping trees. Ourstudy groups used only 17 of 58 available tree species, slept in the top fifth of trees, andslept at sites midway between the trunk and crown exterior. Tree DBH, height, andsleeping site height varied among groups according to the forest subtypes within theirhome ranges. Group members slept in a huddle when temperatures were between 5°and 35°C, and slept separately only with temperatures >20°C. During the wet, hotsummer, they slept more frequently under dense foliage; in the dry, cold winter, theypreferred sites with light foliage and direct sun exposure, potentially to facilitatesunbathing, which occurred almost exclusively during the winter. While severalsleeping site characteristics were consistent with minimizing predation risk, our results

Int J PrimatolDOI 10.1007/s10764-016-9946-5

Handling Editor: Joanna M. Setchell

* Amanda [email protected]

1 Department of Ecology and Evolutionary Biology, Princeton University, Princeton,NJ 08544, USA

2 Department of Anthropology, Yale University, New Haven, CT 06511, USA3 Proyecto Mirikiná/Fundación ECO, Formosa 3600, Argentina4 Facultad de Recursos Naturales, Universidad de Formosa, Formosa 3600, Argentina

http://orcid.org/0000-0003-4060-1495

http://crossmark.crossref.org/dialog/?doi=10.1007/s10764-016-9946-5&domain=pdf

also suggest a tradeoff between predator exposure and warmer conditions at sleepingsites, especially during winter. Our results support the predation avoidance and ther-moregulatory constraint hypotheses, furthering the possibility that these pressures werealso contributing factors in the evolution of their cathemeral activity pattern.

Keywords Cathemerality . Huddling . Predation . Sleep

Introduction

Sleep can be best understood as a flexible behavioral state that has evolved to cope withspecific, and highly variable, physiological and environmental challenges (Allison andCicchetti 1976; Mignot 2008; Schmidt 2014; Siegel 2008). Sleep is universal amongprimates, but species differ in how, when, and where they sleep (Anderson 1984, 2000).Most rest at night (Martin 1990), while some, including the lorises (Loris spp.), tarsiers(Tarsius spp.), and galagos (Galago spp.), sleep during the day (Bearder 1987). Stillothers, most notably several Lemuriformes, sleep both during the day and the nightwith a cathemeral lifestyle (Tattersall 2008). Beyond the diversity in temporal sleepingpatterns, even greater diversity is found in where primates choose to sleep, from clifffaces (Papio spp.: Hamilton 1982), to tree cavities (Leontopithecus rosalia: Franklinet al. 2007), to elaborately constructed nests (Pan troglodytes: Samson 2012). Thesedifferences in the spatiotemporal aspects of sleep are indicative of the unique suites ofenvironmental pressures shaping and constraining each species’ behavior (Lima et al.2005; Siegel 2009).

The factors influencing primates’ ranging, foraging, and social behaviors duringwaking hours do not cease when they rest (Anderson 1984; Lima et al. 2005). In fact,certain pressures may intensify while animals sleep, as predators may become moreactive, weather conditions change, and metabolic rates fall. Thus, it seems reasonablethat the selection of suitable sleeping sites and related sleeping behaviors should allowprimates to cope with these environmental challenges and to mitigate their effects. Thechoice of sleeping site can even impact the quantity and quality of sleep that an animalobtains, and may thus have further implications for how it manages ecological andsocial challenges when awake (Siegel 2005).

Numerous hypotheses identify and explain the ecological factors influencing pri-mates’ sleeping site selection and their pre- and post-sleep behavioral patterns(Anderson 1984, 1998). Safety from predators (Hamilton 1982), energy conservationand thermoregulation (Ramanankirahina et al. 2012), access to nutritional resources(Basabose and Yamagiwa 2002), comfort and stability (Cheyne et al. 2012), parasiteavoidance (Hausfater and Meade 1982), and intergroup competition (von Hippel 1998)have all been invoked to explain where and how primates sleep. In empirical studies,the predation avoidance and the thermoregulatory hypotheses have garnered the mostsupport (Anderson 1998, 2000).

The predation avoidance hypothesis posits that the choice of a sleeping site is relatedto minimizing the risk and rate of predation, and may be the most important function ofa sleeping site (Anderson 2000; Colquhoun 2007; Teichroeb et al. 2012). Primates haveevolved strategies to mitigate the risk and rate of predation at every stage of sleep(Anderson 1984, 1998). To prevent predators from reliably anticipating where primates

A. Savagian, E. Fernandez-Duque

will sleep next, several species reuse sleeping sites infrequently and rarely on consec-utive nights (Holmes et al. 2011; Smith et al. 2007; von Hippel 1998). Alternatively,reusing several familiar trees could better facilitate a quick escape from predators(Albert et al. 2011; Di Bitetti et al. 2000; Struhsaker 1967). Many species also selectsleeping sites that are inaccessible to predators or that offer better concealment(Matsuda et al. 2010; Wang et al. 2011). Arboreal primates prefer sleeping sitespositioned high above the ground, making it more difficult for terrestrial predators toaccess them (Fei et al. 2012; Teichroeb et al. 2012; Wahungu 2001). Many species alsoprefer sites with concealing dense foliage cover or that are enclosed within vineentanglements (Fan and Jiang 2008; Puertas et al. 1995).

If predators succeed in locating and gaining access to sleeping prey, primates willhave the best chance of survival if they can detect predators quickly and have access toeffective escape routes. For some prey species, orienting in a direction different fromthat of other group members can maximize the group’s collective field of vision,increasing the probability of predator detection (Kaby and Lind 2003; van Schaiket al. 1996). Primates preyed upon by predators gaining access by both arboreal andterrestrial routes should also select sleeping sites positioned evenly between the treetrunk and crown, thus giving them sufficient time to detect, respond to, and escapeequally well from predators approaching from within the tree or from the ground(Barnett et al. 2012; Rayadin and Saitoh 2009; Stewart and Pruetz 2013).

The thermoregulatory hypothesis states that the choice of a sleeping site is related tomaintaining a relatively constant body temperature regardless of climatic factors(Anderson 1998). Primates should select specific sleeping sites within a tree to shelterthem from adverse weather conditions and should modulate interindividual distancesaccordingly. Moving to cooler or warmer micro- or macrohabitats is one way in whichprimates can cope with less than optimal meteorological conditions (Matsuda et al.2011; Ramanankirahina et al. 2012; van Schaik et al. 1996). Sleeping in the shade(Duncan and Pillay 2013; Kosheleff and Anderson 2009) or the sun (Cui et al. 2006;Huang et al. 2003) are passive mechanisms by which primates can regulate bodytemperature as needed. Energetically conservative positioning, such as huddling withother group members, is another common behavioral mechanism used to cope with lowambient temperature (Anderson 2000; Gilbert et al. 2010). The benefits of sleeping in ahuddle include lower oxygen intake (Kotze et al. 2008), reduced energy expenditure(Perret 1998; Scantlebury et al. 2006), and reduced caloric intake (Kauffman et al.2003). Huddling behavior was associated with an increase in skin temperature in wildJapanese macaques (Macaca fuscata: Hanya et al. 2007), and occurred more frequentlyas ambient temperatures cooled in several other wild primates (Bicca-Marques andCalegaro-Marques 1998; Donati et al. 2011; Donati and Borgognini-Tarli 2006; Ostner2002). Conversely, when ambient temperatures reach their uppermost extremes, pri-mates may dissipate heat more effectively by sleeping separately from one another (LeMaho et al. 1981; Nowack et al. 2013).

Azara’s owl monkeys (Aotus azarae azarae) live in energetically challengingenvironments, with extreme seasonal temperature and precipitation fluctuations, andare subject to predation from several terrestrial and arboreal predators. Owl monkeys,which range from Panama to Argentina, are the only primates to display nocturnalactivity in the New World (Fernandez-Duque 2011). The Azara’s owl monkeys ofnorthern Argentina are further unique within their genus, as they are the only

Owl Monkey Sleeping Site Selection

subspecies with a cathemeral activity pattern, being active both during the day andnight (Erkert et al. 2012; Fernandez-Duque et al. 2010; Fernandez-Duque and Erkert2006). In the population that we study, Azara’s owl monkeys are genetically monog-amous (Huck et al. 2014), living in social groups composed of two breeding adults andone to four nonreproducing immatures (Fernandez-Duque 2016; Fernandez-Duqueet al. 2001). Groups occupy home ranges that include a core area seldom used byneighboring groups, while solitary monkeys range throughout the forest (Fernandez-Duque and Huck 2013; Wartmann et al. 2014). Owl monkeys are almost exclusivelyarboreal (Wright 1994).

Most owl monkey species regularly sleep in tree holes, which have been suggestedto provide protection against diurnal predators and rainfall (Aquino and Encarnacion1986; Fernandez-Duque et al. 2008; Wright 1989). At our study site, however, we havenever observed owl monkeys sleeping in tree holes, whether diurnally or nocturnally.To our knowledge, this is the only subspecies of owl monkeys not to sleep in cavities atleast occasionally. In conjunction with the unique cathemeral lifestyle, their atypicalsleeping habits make our population an especially intriguing one in which to study theecological pressures that may affect sleeping behaviors.

Here, we evaluate the predation avoidance and thermoregulatory hypotheses tounderstand diurnal sleeping patterns and sleeping site use in Azara’s owl monkeys.Our study population in the Argentinean Gran Chaco is sympatric with several possiblepredators: tayra (Eira barbara), ocelot (Leopardus pardalis), Geoffroy’s cat(L. geoffroyi), and jaguarundi (Puma yagouaroundi; Huck et al. in press a; Hucket al. in press b). All of these predators display diurnal activity (Asensio and Gómez-Marín 2002; Bezerra et al. 2009; Di Bitetti et al. 2010; Manfredi et al. 2011; Pérez-Irineo and Santos-Moreno 2014). At our field site, several observers have witnessedwhat appeared to be near-predation events by tayras during daylight hours, to whichowl monkey groups responded with aggressive mobbing behavior and vocalizations(M. Huck pers. comm.). Although pumas (P. concolor) have been documented at thissite, they generally prefer prey >1.2 kg owl monkeys (Moreno et al. 2006). Arborealsnakes and aerial predators that are known to prey on monkeys are not present atEstancia Guaycolec (Di Giacomo and White 2005).

Azara’s owl monkeys experience highly seasonal precipitation and temperatureextremes in the Gran Chaco region they inhabit. A cold, relatively dry season domi-nates from June to August, during which the daily mean minimum temperature is 16°Cand temperatures can drop below 0°C at night (Erkert et al. 2012). However, during thehot and wet summer that spans from December to March, the maximum daily meantemperature is 27°C and is regularly above 33°C (Erkert et al. 2012; Fernandez-Duqueet al. 2002). Azara’s owl monkeys may have adapted to such seasonality by switchingto a cathemeral activity pattern, which offers greater flexibility in exploiting temporalniches as environmental conditions fluctuate (Curtis and Rasmussen 2006; Fernandez-Duque and Erkert 2006; Fernandez-Duque et al. 2010). Temperature has been associ-ated with changes in owl monkey activity level at this study site, with an optimal rangebetween 15° and 25°C and a cessation of activity below 5°C (Fernandez-Duque et al.2010). If thermoregulation is an important factor influencing the choice of sleepingsites and sleep-related behaviors for owl monkeys, we predict that sleeping patterns willchange with season and temperature. In addition, if predators influence owl monkeydiurnal sleeping habits, then according to the predation avoidance hypothesis, we


should expect to observe them using certain sleeping trees and adopting positions andusage patterns that minimize predation risk while asleep (Table I).

Methods

Study Site and Subjects

The field site is located in the cattle ranch Estancia Guaycolec, in the northern provinceof Formosa, Argentina (58°11′W, 25°58′S). The study area, situated within the Argen-tinean Gran Chaco region, comprises a mosaic habitat of grassland, isolated dry forestpatches, and a gallery forest that flanks the Pilagá River. In 2006, the ranch adminis-tration set aside an area of ca. 1100 ha, where there had been selective logging in thepast, as the Reserva Mirikiná. The reserve is protected against all future logging,hunting, and grazing. A georeferenced transect system with trails at every 100 m spansthe width and breadth of the forest and covers ca. 200 ha.

Owl monkeys in the ranch are found both in the isolated dry forest patches and thegallery forest. In the gallery forest, owl monkeys range throughout four types of forest.The low flooded forest directly abuts the river and is dominated by only a few small-stature tree species. The Austro-Brazilian transitional forest, which grades into thesurrounding grassland, and the high and low albardón (a Spanish word used to refer toriverine forests situated on lateral, sandy-silt deposits from the riverbeds) forests arecharacterized by taller trees and a botanical gradient that dictates the forest structure andcomposition within those habitats (van der Heide et al. 2012). The transitional andalbardón forests, on higher ground, are more floristically diverse than the low-groundflooded forest.

The present study focuses on the first five groups identified when the Owl MonkeyProject began (Fernandez-Duque and Bravo 1997): C0, CC, D100, D500, and E500.From August 1998 to September 1999, we contacted them weekly as part of a larger

Table I Hypotheses explaining sleeping tree and sleeping site selection by Azara’s owl monkeys (Aotusazarae azarae) in Formosa, Argentina from 1998 to 1999 and associated predictions to be tested

Hypothesis Prediction

Predation avoidance P1. Monkeys reuse trees infrequently, rarely on consecutive nights.P2. Sleeping trees are relatively tall.P3. Sleeping sites are high within sleeping trees.P4. Sleeping sites have dense foliage cover year-round.P5. Foliage cover of sleeping trees is composed of leaves and vines to provide greater

concealment.P6. Sleeping sites have very dense vine entanglements.P7. Monkeys sleep oriented in different directions to increase predator detection.P8. Sites are midway between trunk and crown exterior.

Thermoregulatoryconstraints

P9. Monkeys sleep at sites that do not receive direct sunlight in summer and that doreceive it during winter.

P10. Sleeping sites have light foliage cover in summer and dense foliage cover inwinter.

P11. Huddle frequency decreases with ambient temperature.P12. Huddle participation decreases with ambient temperature.


study on activity patterns (see Fernandez-Duque 2003 for detailed information onsampling methods). Sleeping site data collection occurred from November 1998 toAugust 1999. We report here only sleeping bouts that occurred during daylight hours.At the outset of this study, groups C0 and CC had five individuals, D500 and E500 hadfour, and D100 had three. Group composition changed over the course of the studybecause of one dispersal event (C0) and one death/dispersal (D500).

Data Collection

Ecological Data We obtained information on forest structure by surveying 16 ha ofgallery forest, subdivided into 25 × 25 m subplots, between 2005 and 2008. Through-out all 16 ha, we recorded diameter at breast height (DBH) and species for allvegetation with a DBH ≥10 cm (N = 7127 trees and palms; van der Heide et al.2012). We did not record height. The surveyed area encompassed most of the rangesof four of the five groups considered in this study (CC, D500, E350/D100, E500).Results from this survey matched results from a smaller 1998 survey that relied on 3050 × 10 m plots placed randomly within the home ranges all five groups (C0, CC,D100, D500, E500) across all forest subtypes (Fernandez-Duque et al. 2002). Temper-ature data loggers located at the gallery forest entrance have recorded ambient temper-ature hourly since 1998 (Erkert et al. 2012).

Sleeping Trees, Sleeping Sites, and Sleep-Related Behaviors We defined a sleepingtree as the individual tree in which owl monkeys slept and a sleeping site as a specificsection within a sleeping tree, e.g., a branch, a vine entanglement, where we observedthe individuals sleeping. Owl monkeys usually sleep synchronously; it is rare for oneindividual to sleep while others in the group are active (Fernandez-Duque 2003). Wedefined a sleeping bout to begin the moment the group entered a sleeping tree and tofinish the moment it left, including the time for any pre- or post-sleeping behaviors suchas foraging and socializing in the sleeping tree.

While following the groups during the day, we recorded information on thecharacteristics of the sleeping trees and sleeping sites they used. We also obtaineddata for each sleeping bout that occurred while we were following a group. Variablesrecorded were duration of sleeping bout; length of time spent active in the tree beforeand after sleeping; sleeping tree species, height, DBH, and density of its vineentanglements (moderate or very dense); sleeping site height; amount of surroundingfoliage cover (light, moderate, or full) and its composition (mixed leaves and vines oronly leaves); the site’s position with respect to the trunk axis (at the trunk, exterioredge of crown, or midway between trunk and crown exterior); and the grouping,orientation, and number of individuals at the sleeping site. We visually estimatedsleeping tree height, from the ground to the top of the tree crown, and the height ofthe sleeping site. Before the study, E. Fernandez-Duque trained all observers in heightestimation by repeatedly estimating the height of known points in trees and by thencomparing estimates between observers. During data collection, two observers alwaysindependently estimated height.

We classified grouping behavior at a sleeping site as huddling or sleeping separately.We defined huddling as two or more individuals resting in contact. If at least oneindividual was facing a direction that differed (≥90°) from other group members, we


scored the group as oriented in different directions. We scored a group as oriented in thesame direction if there were no individuals forming an angle of ≥90° with the rest of thegroup. For recording data on sun exposure, we recorded the group as sleeping in thesun if at least one group member was exposed to direct sunlight; we recorded the groupas not sleeping in direct sunlight if the group was in the shade or if there was no directsunlight on any individual’s fur.

Data Analysis

For sleeping bouts during which not all group members displayed the same behaviorsat the same time (e.g., slept at different heights), we took the mean across individuals togenerate a composite score for the group. If entrance and exit times differed amonggroup members during a single sleeping bout, we used the earliest entrance time and theearliest exit time in our analyses. If individuals slept at different positions along abranch, e.g., two at the trunk and one at the exterior, during a single sleeping bout, weused the position at which the majority of individuals slept for analysis.

We calculated huddle participation as the number of group members huddlingdivided by the total number of individuals present in the group. A score of 0 indicatesno huddling and all individuals sleeping separately, while a score of 1 indicates allgroup members huddling.

For the ambient temperature when groups began sleeping, we used the temperaturerecorded on the hour closest to the first record of them sleeping. For example, if a groupbegan sleeping at 10:15 h, then we used the 10:00 h recorded temperature. If the timewas 10:45 h, we used the 11:00 h recorded temperature.

Statistical Analysis

We used a χ2 goodness of fit test to estimate the probability that differences foundbetween tree species availability and actual species use were different from chance, and

we estimated Cramer’s V, the effect size, asffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi

χ2= Nð Þðp

c−1ð ÞÞ, where N is the totalsample size (number of individual trees sampled in the 16 ha plus the number ofsleeping trees used by each group) and c is the number of categories considered (totalnumber of species available). We compared differences in mean DBH, tree height, andrelative site height among groups using a one-way ANOVA. We log transformed treeheight data and arcsine transformed relative site height data (proportions); DBH datawere normal without transformation. Data met assumptions for homoscedasticity atα = 0.01: DBH Fmax = 2.09, df = 16; tree height Fmax = 1.58, df = 20; relative site heightFmax = 4.41, df = 20. We used a χ2 goodness of fit test to evaluate the probability thatdifferences in preferences for vine density within groups were different from chanceand a χ2 test for association to evaluate the likelihood that differences among groups forsleeping site position and huddling behavior were also different from chance. Withingroups, we used Fisher’s exact test to estimate the probability that our data on foliagedensity and composition between seasons were statistically different, and to comparethe immediacy with which monkeys began sleeping at a site or left the site afterwaking. All statistical tests were conducted in R (R Core Team 2016).


Ethical note

All research complied with Argentine national and provincial laws and regulations at thetime the study was conducted. The OwlMonkey Project has had continued approval for allresearch presented here by the Formosa Province Council of Veterinarian Doctors, theDirectorate of Wildlife, the Subsecretary of Ecology and Natural Resources, and theMinistry of Production. At the national level, the procedures were approved by theNationalWildlife Directorate in Argentina and by the IACUC committees of the Zoological Societyof San Diego (2000–2005) and of the University of Pennsylvania (2006–2010).

Results

Vegetation Survey

We identified 7127 trees and palms with DBH ≥10 cm representing 58 species with amean DBH ± SD of 25 ± 17 cm within the 16 ha surveyed. The three most abundantspecies were Gymnanthes discolor (19%), Chrysophyllum gonocarpum (9%), andTrichilia catigua (6%), in that order. Thirty-four species had very low abundance, witheach of them representing <1% of all trees sampled.

Characteristics of Sleeping Trees

We recorded information during 153 sleeping bouts (C0 = 30, CC = 21, D100 = 53,D500 = 27, E500 = 22) that took place in 116 unique sleeping trees (Table II). We wereunable to measure every variable for each sleeping bout; thus the N used in analysisdiffers slightly for each group and each variable. The majority (82%, 95/116) of treeswas used only once, 14 were used twice, 6 were used 3 times, and 1 was used on 4occasions. All groups reused sleeping trees on different days (range: 2–9 reused treesper group), whereas only D500 reused trees on the same day (two trees).

The five groups slept in 17 different tree species. We never observed owl monkeyssleeping in the most frequent species in the forest, Gymnanthes discolor (19% estimat-ed frequency), a relatively small tree (mean DBH ± SD: 13 cm ± 3, N = 1328). All fivegroups used Calycophyllum multiflorum and Patagonula americana, and four groupsused C. multiflorummost frequently, even though it accounted for only 5% of availabletrees in the 16-ha vegetation survey. Owl monkeys used certain species more thanexpected given their estimated availability in the forest, and these differences in usereached statistical significance for all groups except CC (Table III).

Groups regularly use trees with DBH greater than the forest mean of 25 cm(Table II). Across groups, the mean height of sleeping trees ranged between 16 and20 m (Table II). Owl monkeys never slept in trees with a DBH <13 cm or height <10 m,and used trees with DBH as large as 282 cm (group CC) and as tall as 30 m (groupE500). Despite their overall use of large trees, there were marked differences in meanDBH and height among groups. The groups inhabiting albardón forest on high ground(D500, E500) slept in trees that had mean DBH 30–60 cm wider and mean height 3–4 m taller than those used by groups ranging in low, flooded forest near the river (C0,CC) and/or in transitional forest near the bordering grassland (C0, D100; Fig. 1). These


differences among groups were statistically significant (one-way ANOVA: DBH F =4.56, df = 4, P = 0.002; height F = 8.55, df = 4, P < 0.001).

Characteristics of Sleeping Sites

All groups consistently slept in the upper half of the tree (Fig. 2), between 6 and 25 mabove the ground. Groups C0 and D100, which inhabit sections of transitional forest orlow, flooded forest with shorter tree species, did not appear to compensate for theirshorter sleeping trees by positioning themselves higher in their trees. The mean heightof their sleeping sites was still 3–4 m lower than those of D500 and E500 (Table II).Therefore, the differences in the height of the sleeping site relative to the height of thesleeping tree were not statistically significant among groups (one-way ANOVA: F =1.62, df = 4, P = 0.174). Only two groups ever slept in the lower half of the tree (C0 =3%, 1/30 sleeping bouts; CC = 5%, 1/21; Fig. 2).

Table II Sleeping tree and sleeping site characteristics and positional behavior for five groups of Azara’s owlmonkeys (Aotus azarae azarae) in Formosa, Argentina from 1998 to 1999

Group

C0 CC D100 D500 E500

Number of unique sleeping trees 27 (30) 18 (21) 38 (53) 17 (27) 16 (22)

Number of unique trees reused 2 (30) 2 (21) 9 (53) 5 (27) 3 (22)

Number of species used 8 (25) 7 (17) 14 (46) 5 (21) 9 (21)

Mean sleeping tree DBH ± SD (cm) 107 ± 49(24)

131 ± 62(17)

133 ± 52(46)

162 ± 66(22)

170 ± 46(18)

Mean sleeping tree height ± SD (m) 16 ± 3 (30) 19 ± 5 (21) 16 ± 4 (53) 20 ± 4 (27) 19 ± 4 (22)

Mean sleeping site height ± SD (m) 12 ± 3 (30) 15 ± 5 (21) 13 ± 3 (51) 16 ± 4 (26) 16 ± 4 (21)

Sleeping site position

% at trunk 14 (29) 10 (21) 16 (51) 12 (26) 18 (22)

% at midway on branch 83 76 78 88 82

% at exterior of crown 3 14 6 0 0

Density of vine tangles

% with moderately dense 79 (14) 92 (12) 79 (38) 68 (19) 58 (19)

% with very dense 21 8 21 32 42

Foliage composition

% with leaves only 21 (28) 20 (20) 10 (51) 12 (24) 9 (22)

% with leaves and vines 79 80 90 88 91

Mean time spent sleeping ± SD (min) 214 ± 126(18)

225 ± 156(13)

183 ± 120(34)

198 ± 146(18)

160 ± 138(13)

Mean time active in sleeping tree beforesleeping ± SD (min)

13 ± 11(28)

20 ± 31(20)

10 ± 8 (42) 13 ± 9 (23) 15 ± 10(19)

Mean time active in sleeping tree aftersleeping ± SD (min)

9 ± 8 (17) 6 ± 5 (11) 4 ± 6 (35) 13 ± 35(18)

4 ± 3 (12)

% with huddling 96 (28) 95 (20) 94 (50) 96 (24) 94 (17)

% with monkeys facing different directions 67 (24) 94 (17) 59 (32) 50 (14) 100 (9)

Values in parentheses represent the number of sleeping bouts (N) for which we measured the relevant variable.Percentages represent the percentage of sleeping bouts for which we observed particular characteristics


All groups most frequently used sleeping sites located midway between the centertrunk and the periphery of the tree. Groups slept 81% of the time at these midwaypositions whereas they only slept at the trunk 14% and at the exterior 5% of the time(means across all groups; Table II). We never recorded two groups (D500, E500)sleeping at the exterior of the tree. Patterns of sleeping site positioning did not showstatistically significant differences among groups (χ2 test for association: χ2 = 7.7, df =8, P = 0.464).

Table III Percentage of sleeping bouts during which five groups of Azara’s owl monkeys (Aotus azaraeazarae) in Formosa, Argentina from 1998 to 1999 slept in their three most used tree species and results of χ2

goodness of fit tests (χ2 value, P, and effect size as calculated with Cramer’s V) comparing observed use of allspecies with estimated availability throughout the forest

Group First most Second most Third most χ2 P Cramer’sV

C0N = 25

Calycophyllummultiflorum(40%)

Patagonulaamericana(16%)

Albizia inundata/Gleditsia amorphoides/Ocotea diospyrifolia/

Sideroxylonobtusifolium/

Tabebuia heptaphylla (8%)

298.9 <0.001 0.03

CCN = 17

C. multiflorum(35%)

G. amorphoides(24%)

Inga uruguensis/P. americana (12%)

72.1 0.086 0.01

D100N = 46

C. multiflorum(22%)

P. americana(15%)

Chrysophyllumgonocarpum (11%)

456.3 <0.001 0.03

D500N = 21

C. multiflorum(52%)

Phyllostylonrhamnoides(19%)

Phytolacca dioica (14%) 144.4 <0.001 0.02

E500N = 21

Pterogyne nitens(24%)

S. obtusifolium(19%)

C. multiflorum/P. rhamnoides (14%)

1059.3 <0.001 0.05

The χ2 analysis considers all tree species, but we show only the top three species used by the groups here.N = number of sleeping bouts for which we recorded species

Fig. 1 Box plots for diameter at breast height (DBH) of sleeping trees used by five groups of Azara’s owlmonkeys (Aotus azarae azarae) in Formosa, Argentina from 1998 to 1999. The thick horizontal line within thebox marks the median. The upper and lower boundaries of the box represent the 75th and 25th quartiles,respectively. Whiskers extend beyond the box boundaries to the most extreme observation within 1.5 times theinterquartile range. Empty circles represent outliers beyond 1.5 times the interquartile range; filled circlesrepresent mean DBH. N = number of sleeping bouts for which we recorded DBH.


All five groups slept more frequently at sleeping sites covered by moderately densevine tangles than in those with very dense tangles. These differences were statisticallysignificant for groups CC and D100, but not for groups C0, D500, or E500 (χ2 goodnessof fit test: C0 χ2 = 4.6, df = 1, P = 0.033; CC χ2 = 8.3, df = 1, P = 0.004; D100 χ2 = 12.7,df = 1, P < 0.001; D500 χ2 = 2.6, df = 1, P = 0.108; E500 χ2 = 0.5, df = 1, P = 0.491).

The choice of cover changed in relation to the season, with groups sleeping at full foliagesites most frequently during the summer, and at light andmoderate foliage sites most duringthe winter (Fig. 3). Most marked was the change in the use of sleeping sites with lightfoliage from summer, when three groups (C0, D100, E500) never used lightly covered sites,to winter, when they slept under light cover between 17 and 59% of their sleeping bouts.However, this difference was statistically significant for only one group, C0 (Fisher’s exacttest: C0 P = 0.004; CC P = 0.511; D100 P = 0.372; D500 P = 0.836; E500 P = 0.208).

Groups consistently used sleeping sites with surrounding foliage composed of bothleaves and vines more frequently than sites covered only by leaves. This was statisti-cally more frequent than expected (combined for all groups, χ2 goodness of fit test:χ2 = 76.0 df = 1, P < 0.001). There was no statistically significant difference in usebetween seasons (all groups, Fisher’s exact test: P = 1).

Behavior at Sleeping Sites

Groups spent more time active in their sleeping tree before resting than after resting(Table II). Mean time spent active before sleeping (foraging, grooming, etc.) was13 min combined for all groups (range: 0–136 min). Only one group slept immediately

Fig. 2 Percentage of sleeping bouts for which five groups of Azara’s owl monkeys (Aotus azarae azarae) inFormosa, Argentina from 1998 to 1999 slept at different heights relative to the height of the sleeping tree.Relative sleeping site height was calculated by dividing site height by tree height. Number of sleeping boutsfor which we recorded height: C0 = 30, CC= 21, D100 = 51, D500 = 26, E500 = 21.


on entering the sleeping tree (D500, two occasions). After waking, owl monkeys leftthe sleeping tree after a mean of 7 min, combined for all groups (range: 0–152). Theywere more likely to leave the tree immediately (13/93 sleeping bouts, combined for allgroups) than to begin sleeping immediately (2/132 for all groups; Fisher’s exact test:P < 0.001). The mean time spent sleeping per sleeping bout was 194 min, combined forall groups (range: 9–620).

Members of four groups (C0, CC, D100, E500) slept facing different directionswhile sleeping more often than facing the same direction, and all groups slept morefrequently in a huddle than separated from one another (Table II). All group membershuddled together when temperatures were ≤20°C. With temperatures >20°C, owlmonkeys slept sometimes in group-wide huddles (38/55 sleeping bouts for all groups),but also partially (11/55) and completely separated (6/55). When ambient temperaturesreached 35°C (2/111), we never observed the owl monkeys huddling while sleeping.

Groups rarely slept at sleeping sites with direct exposure to sunlight, and when theydid, it was almost exclusively during the austral winter months. During the summermonths (November–March), only one group (D100) ever slept in the direct sun, in oneof eight sleeping bouts. During the winter months (April–August), all five groups sleptin direct sunlight (C0 = 22%, N = 18 sleeping bouts; CC = 7%, 15; D100 = 21%, 42;D500 = 19%, 16; E500 = 11%, 9).

Discussion

Can the Choice of Sleeping Site Minimize Predation Risk?

As predicted by the predation avoidance hypothesis, owl monkeys reused sleeping treesinfrequently, which may have prevented predators from cueing into their ranging patterns(Fei et al. 2012; Smith et al. 2007; Teichroeb et al. 2012; von Hippel 1998). Reused treesmay have conferred compensatory benefits, such as concealment from predators,

Fig. 3 Percentage of sleeping bouts when five groups of Azara’s owl monkeys (Aotus azarae azarae) inFormosa, Argentina used sleeping sites with light, moderate, or full foliage cover during the austral summer(November 1998–March 1999; solid gray) and austral winter (April–August 1999; solid black). Number ofsleeping bouts for which we recorded foliage density for each group are as follows (summer/winter): C0 = 10/17, CC= 6/11, D100 = 8/41, D500 = 11/14, E500 = 12/10.


thermoregulatory benefits, or increased familiarity facilitating a quicker escape (Di Bitettiet al. 2000; Struhsaker 1967). This pattern of alternating betweenmany Bdecent^ sites and afew Bbest^ reused sites has been described for golden-handed tamarins (Saguinus midasmidas: Day and Elwood 1999), pigtailed macaques (Macaca leonine: Albert et al. 2011),and tufted capuchins (Cebus apella nigritus: Di Bitetti et al. 2000). Low rates of reuse mayalso reduce parasite transmission through accumulated feces (Anderson 1984; Day andElwood 1999), although owl monkey feces do not usually collect on branches (A.Savagian, pers. obs.) and may pose little risk of infection.

Overall, owl monkeys preferred sleeping trees with DBH much larger than the forestmean. Although we lack data on the height of available sleeping trees at our study site,the tight relationship between DBH and height (Mehtätalo et al. 2015; Vibrans et al.2015) suggests that owl monkeys may also be selecting sleeping trees that are tallerthan surrounding trees, which has been implicated in predation avoidance strategies (DiBitetti et al. 2000; Feilen and Marshall 2014). The effects of DBH, height, otherstructural characteristics, and species are all likely interdependent, making it difficultto disentangle for which characteristics owl monkeys may be selecting.

Owl monkeys slept relatively high within trees, concentrating their sleeping sites only inthe top fourth to fifth of the sleeping tree. The apparent avoidance of the upper canopy islikely not a response to eagle or owl predation, as these birds of prey are either not present inthis forest or hunt smaller prey (Di Giacomo and White 2005). It is more likely, however,that owl monkeys sleep lower within trees to avoid exposure to excessive wind, rain, or sunin the canopy. Western woolly lemurs (Avahi occidentalis) also balance competing terres-trial predation pressure and adverse weather conditions at high sleeping sites by preferringthe middle storey within their sleeping trees (Ramanankirahina et al. 2012). Interestingly,the sleeping site height relative to tree height was consistent among groups, suggesting thatideal sleeping structures, like thick perpendicular branches that can support multiplemonkeys or are resistant to wind damage, may be more common at this relative height(Cheyne et al. 2012; Di Bitetti et al. 2000).

Once within a sleeping tree, owl monkeys showed a strong tendency to use sitesconcealed by leaves and vines, which may offer more protection against predators thanleaves alone, since interwoven and tangled vines can bemore difficult to penetrate (Fan andJiang 2008). In support of the hypothesis that early detection of a predator is an effectiveway to reduce predation risk (Colquhoun 2007; Janson et al. 2014), we found that owlmonkeys often faced opposite directions as they rested, a pattern that may allow them tomaximize their group’s collective field of vision. They also slept at the midway point alongbranches, possibly allowing themmore time to detect predators approaching from the trunkor predators approaching from neighboring trees (Barnett et al. 2012).

Taken together, the characteristics and use of owl monkey sleeping sites give supportto the predation avoidance hypothesis. However, a more comprehensive understandingof predator diets, hunting strategies, and activity patterns at this study site is also neededto make a claim about how predator pressure influences owl monkey behavior(Zuberbühler and Jenny 2002).

Conserving Energy in a Seasonal Environment

As predicted, owl monkeys’ sleeping behaviors showed some association with changesin ambient temperature and season. The number of individuals huddling increased as


temperature decreased, suggesting that owl monkeys may employ social thermoregu-lation to minimize energy expenditure. Although primates are endotherms and can relyprincipally on physiological mechanisms to regulate their body temperature, behavioralmechanisms still play a critical role in thermoregulation (Gilbert et al. 2010; Kosheleffand Anderson 2009; Terrien et al. 2011). Azara’s owl monkeys, which experiencehighly variable temperatures, precipitation, and day length in their subtropical habitat,may particularly rely on behavioral adaptations (Erkert et al. 2012; Fernandez-Duqueet al. 2002). Precipitation and other climatic factors, such as humidity and wind, werenot quantified in this study but have been implicated in sleeping site selection in otherspecies of owl monkey (Aquino and Encarnacion 1986).

Despite the change in huddling participation associated with temperature changes,huddling of some degree was observed on all but the hottest days of data collection(35°C), suggesting it may have a function beyond thermoregulation. Sleeping sites mayserve a social purpose, reflecting and reinforcing group bonds as individuals huddle andmaintain proximity while sleeping (Anderson 2000; Lock and Anderson 2013;Takahashi 1997). As new adults join the group, and as subadults disperse, theirproximity to group members and behavior at sleeping sites can reflect theirtransforming membership status (Moos and Immelmann 1987; Pfalzer and Ehret1995). The social function of owl monkeys’ sleeping sites is further supported by thepre- and post-sleep activity observed within their sleeping trees.

While attempting to minimize thermal stress, primates are likely to encountercompeting pressures (predatory, nutritional, social) that constrain their behavior andresult in a tradeoff (Cui et al. 2006; Hill 2006; José-Domínguez et al. 2015;Matsuda et al. 2010). Owl monkeys may face a compromise between thermoregu-lation and predation at the level of the sleeping site, and our data suggest thatthermoregulation may weight more heavily in this tradeoff. Concealment is animportant antipredation strategy from which owl monkeys could benefit (Fan andJiang 2008; Nijman and Nekaris 2013; Stewart and Pruetz 2013), and yet groups inour study preferred to sleep under light and moderate foliage during the winter,eschewing full and cryptic cover.

It is possible that owl monkeys prefer to sleep under patchy foliage so that they canbetter detect approaching predators (Albert et al. 2011; Koops et al. 2012). However, ifearly detection were the primary reason to sleep at exposed sites, we would expect owlmonkey groups to use lightly covered sites year-round. This was not the case: duringthe wet, hot summer, groups actually preferred to sleep under dense foliage. Theirpreference for light foliage was only observed during the winter, when the mean dailyminimum temperatures are 10–15°C and when sunbathing at a patchily coveredsleeping site would be most adaptive (Erkert et al. 2012). It appears that our owlmonkey population may be willing to risk the heightened predation cost of sunbathingin full view (Nowack et al. 2013; Seiler et al. 2013) to reap the benefits of a warmersleeping site (Hanya et al. 2007).

Intergroup Variation and Forest Types

An unexpected difference in the types of trees chosen for sleeping emerged in associ-ation with the forest habitat type in which each of the five groups ranged (groups C0and CC in low, flooded forest; D100 in transitional forest; D500 and E500 in high


ground albardón forest). Tree species diversity and abundance change across foresttype, potentially resulting in a change in available sleeping trees. Owl monkeys’observed preference for sleeping in smaller trees and moderately dense vine tangleswhen in the flooded and transitional forests may simply be due to a lack of large treesthat are able to support bigger, denser vine tangles (Malizia and Grau 2006; Pérez-Salicrup et al. 2001). A frequently flooded forest may also explain why groups C0 andCC slept at lower sleeping sites: flooded terrain may be more difficult for terrestrialpredators to traverse (Matsuda et al. 2010). Pigtailed macaques and proboscis monkeys(Nasalis larvatus), for example, both preferred sleeping sites located along the riveredge (Albert et al. 2011; Bernard et al. 2010).

Predation risk and thermoregulation are likely not the only pressures influencing owlmonkey sleeping site selection, especially across multiple forest types. In this study, wedid not evaluate the role of the distribution and availability of nutritional resources onthe selection of sleeping trees. Primates are also expected to sleep in or near importantfood sources to maximize their foraging efficiency (Albert et al. 2011; Anderson 1984;Basabose and Yamagiwa 2002; Teichroeb et al. 2012). Meeting metabolic needs maybe especially critical in the seasonal Gran Chaco, where periodic drought limits foodavailability and plays an important role in structuring owl monkey home rangedistribution (Fernandez-Duque and van der Heide 2013; van der Heide et al. 2012).

Possible Relationship Between Sleeping Sites and Activity Patterns

During this study, we only observed Azara’s owl monkeys sleeping on branches orlianas, or enclosed within vine tangles. In the 20 years of research at Guaycolec, wehave never observed an owl monkey sleeping in a tree cavity, a common sleepinglocation for other species of Aotus (Aquino and Encarnacion 1986; Fernandez-Duqueet al. 2008; Wright 1989). Other populations of Azara’s owl monkeys also sleepexclusively at external sites (Garcia and Braza 1993; Rathbun and Gache 1980).Satisfactory cavities may be lacking in Azara’s owl monkey habitat due to forestcomposition or abiotic factors (Aquino and Encarnacion 1986). In addition, theirgreater size (1.2 kg compared to smaller 0.7–0.8 kg species; Fernandez-Duque 2011)may prohibit them from using holes suitable for other Aotus (Fernandez-Duque et al.2008). This distinction between the sleeping habits of Azara’s owl monkeys, whichinhabit the southernmost tip of the Aotus range, and those species living in moretropical habitats may also be a result of divergent predation pressures and climaticconditions. Reduced aerial predation pressure in Azara’s owl monkeys’ habitat mayhave permitted them to sleep at more accessible external sites (Wright 1989). Thesesites are also more exposed to sunlight, which can benefit owl monkeys during the coldwinters, when temperatures dip below 0°C (Erkert et al. 2012; Garcia and Braza 1993;Seiler et al. 2013). A harsher climate that demands greater behavioral flexibility mayhave pushed Azara’s owl monkeys out of their tree holes and into a greater variety ofsleeping sites.

The divergence in sleeping site preferences between the Azara’s owl monkey andits congeners may be a result of the same selective pressures that precipitated theirswitch to cathemerality, which permits primates to concentrate their activity withinthe least energetically demanding or risky portions of the 24-h cycle (Colquhoun2007; Curtis and Rasmussen 2006). This is especially critical in extreme


environments. The only other known cathemeral primates, Malagasy lemurs withinthe genera Eulemur and Hapalemur, also live in highly seasonal habitats and havefew aerial predators (Curtis and Rasmussen 2006; Hill 2006; Kappeler and Erkert2003; Tattersall 2008). By examining the factors influencing cathemeral species’daily decisions about where to sleep, we can evaluate and refine hypotheses about theselective pressures that spurred their shift from nocturnality to their uniquecathemeral lifestyle. Future research should concentrate on comparing cathemeralspecies’ diurnal and nocturnal sleeping sites to identify what selective forces varyacross the 24-h cycle and how these differences may have led certain species toexploit a cathemeral niche.

Acknowledgements This research was supported by grants to E. Fernandez-Duque from the L. S. B.Leakey Foundation, Douroucouli Foundation, Dumond Conservancy for Primates and Tropical Forests,Argentinean National Council for Scientific and Technological Research (PIP 0051/98 CONICET),Wenner-Gren Foundation, National Geographic Society, and National Science Foundation (BCS-6400621020, BCS-837921, BCS-904867, BCS-924352). A. Savagian received financial support from theUniversity of Pennsylvania’s University Scholars program. Thank you to the many students, volunteers,and assistants who were vital in collecting these data during the first years of the Owl Monkey Project. Specialthanks go to Mr. F. Middleton, Manager of Estancia Guaycolec, and Ing. A. Casaretto (Bellamar Estancias) fortheir continued support of the Owl Monkey Project. We thank Dorothy Cheney for her helpful comments on aprevious version of this manuscript and Joanna Setchell, Ikki Matsuda, and an anonymous reviewer forcomments that have greatly improved the manuscript.

Compliance with Ethical Standards

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

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do predators and thermoregulation influence choice of ......predation and thermoregulatory...

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