International Journal of Zoology

Behavioral Ecology

Behavioral Ecology

International Journal of Zoology

Behavioral Ecology

Copyright 2011 Hindawi Publishing Corporation. All rights reserved. This is a focus issue published in volume 2011 of International Journal of Zoology. All articles are open access articles distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Editorial Board
Alan Afton, USA Nigel Bennett, South Africa W. D. Bowen, Canada Hynek Burda, Germany Terry Burke, UK Catherine Carr, USA Leo Chalupa, USA Roger P. Croll, Canada Burk A. Dehority, USA Greg Demas, USA Marcel Eens, Belgium Peter Frappell, Australia Zoltan Fuzessery, USA Zhiyuan Gong, Singapore Michael G. Hadeld, USA Craig W. Hawryshyn, Canada Marie Herberstein, Australia Alan Hodgson, South Africa Herbert Hoi, Australia Pung-Pung Hwang, Taiwan Thomas Ilie, USA David Jacobs, South Africa J. Komdeur, Netherlands Antilles Michel Laurin, France John Lewis, UK Martin Lockley, USA George A. Lozano, Estonia Royal Mapes, USA Iain J. McGaw, Canada Eugene S. Morton, USA Randy J. Nelson, USA Mark A. Norell, USA Barbara F. Nowak, Australia Beth Okamura, UK Stephen Reid, Canada Lesley Rogers, Australia Alexandre Roulin, Switzerland Ronald Schusterman, USA Stephen Secor, USA Stephen J. Simpson, Australia Ajai Kumar Srivastav, India Raul Suarez, USA Hans Sues, USA Michael Thompson, Australia Stephen Tobe, Canada Tobias Wang, Denmark

Contents
Habitat Selection and Mating Success in a Mustelid, Thierry Lod e Volume 2011, Article ID 159462, 6 pages A Review and Interspecic Comparison of Nocturnal and Cathemeral Strepsirhine Primate Olfactory Behavioural Ecology, Ian C. Colquhoun Volume 2011, Article ID 362976, 11 pages Leadership of Winter Mixed-Species Flocks by Tufted Titmice (Baeolophus bicolor): Are Titmice Passive Nuclear Species?, Thomas A. Contreras and Kathryn E. Sieving Volume 2011, Article ID 670548, 11 pages Arithmetic-Like Reasoning in Wild Vervet Monkeys: A Demonstration of Cost-Benet Calculation in Foraging, Sayaka Tsutsumi, Tomokazu Ushitani, and Kazuo Fujita Volume 2011, Article ID 806589, 11 pages Figs Are More Than Fallback Foods: The Relationship between Ficus and Cebus in a Tropical Dry Forest, Nigel A. Parr, Amanda D. Melin, and Linda Marie Fedigan Volume 2011, Article ID 967274, 10 pages

Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 159462, 6 pages doi:10.1155/2011/159462

Research Article Habitat Selection and Mating Success in a Mustelid

Thierry Lod e
UMR CNRS 6552 ETHOS, Universit de Rennes 1, 35042 Rennes, France e Correspondence should be addressed to Thierry Lod , thierry.lode@univ-rennes1.fr e Received 4 December 2010; Revised 20 February 2011; Accepted 4 March 2011 Academic Editor: Hynek Burda Copyright 2011 Thierry Lod . This is an open access article distributed under the Creative Commons Attribution License, which e permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Habitat selection remains a poorly understood ecological process, but relating mating behaviour to pattern of habitat selection constitutes a fundamental issue both in evolutionary ecology and in biological conservation. From radiotelemetry protocol, habitat-induced variations in mating success were investigated in a solitary mustelid carnivore, the European polecat Mustela putorius. Selection for marshy habitat was regarded as adaptive in that mating success was found greater using marches than other habitats. Males consorted with 1.3 females, revealing a low polygyny rate. Pregnant or lactating females selectively shifted to deciduous woods. That some habitat types may favour a good reproduction forms a key factor for species conservation and environmental management. Nevertheless, such as in various vertebrates, habitat requirements seem to be based on simple broad features of habitat, suggesting that habitat avoidance rather than habitat preference can explain polecat habitat predilection.

1. Introduction
Adaptive signicance of a behaviour is recognized when a behaviour provides a selective advantage in animal ability to adapt to its environment. Landscape structures are expected to inuence especially mating behaviour and numerous species required heterogeneous habitat composition. Dierences in habitat use among animals have been often ascribed to habitat selection although habitat selection remained a poorly known behavioural ecological process [1 3]. Patterns of habitat use may reveal specic choice for habitat, which should provide numerous benets such as resource availability, shelter, avoidance of predation, and reduced interspecic competition [4, 5]. The basic conjecture in habitat selection theory is that animals select habitat features to maximize their tness [69]. Thus, habitat selection is a behaviour related to tness and diers from habitat use in which habitat preferences are mainly linked to resources. Habitat selection can lead to a strong delity to habitat features in which tness was previously high [10]. Numerous species showed partitioning in microhabitat preferences, but patent demonstration for habitat selection was rare [11, 12]. Actually, natural selection can occur when distinct habitat types dier in successful breeding, and putative dierences between unsuccessful and successful

reproductive sites can be regarded as reecting habitat selection [8, 12, 13]. It could be predicted that no selection occurs when unsuccessful and successful reproductive sites are not discernible from most of their main habitat features, but McLoughlin et al. [12] found no variations at the homerange level but dierences within the home range level underline the importance of spatial scale dependence in habitat selection [6, 14]. Selection of better reproductive sites and habitat features should be indicative of adaptive behavioural preferences but can often result in increasing competition, habitat selectivity, and declining population density [4]. Habitat selection and nest-sites choice have been widely studied in birds although dierences in tness were not often examined [8, 15, 16]. However, dierences in habitat can have noticeable eects on reproduction [9]. The relationship between male status and mating success was reported from social mammals such as mongooses and badgers [1719], but numerous species lived a solitary life, and their social organisation was mainly based on spatial pattern [20]. This is especially the case for most carnivores, and although habitat features have been recognized as major parameters for species conservation (see [21]), the role of habitat selection has still received little attention.

2 In solitary carnivores, male and female live independently over long periods and generally exhibit a mating system in which the male home range partially overlaps the range of one or several females [2225]. Because carnivores were routine and did not try to avoid poor environmental conditions, it could be predicted that habitat traits have a major inuence on their mating success. This study investigates the role of habitat selection on the mating success of a solitary mustelid carnivore, the European polecat Mustela putorius. Based on a long-term survey of radiotracked animals, this study aims at characterising habitat features and mating success to assess whether habitat features may aect mating success (habitat selection).

International Journal of Zoology data from radiotracked polecats, we calculated the centre of activity (arithmetic mean) from xes, and the minimal dispersal distance was assessed comparing minimal distance between telemetry locations. Habitat use was inferred in male and female radiotracked polecats based on percentage of xes found in a considered habitat type and was assigned to two main periods, winter (NovemberJanuary) and breeding period (FebruaryApril for males, and May-June for females, because mating sites may dier with breeding sites in which parturitions occurred). Field study for determining habitat features was performed between July and September from 1998 to 2002, considering the minimum convex polygon of each individual and, for random sites, a number of putative locations, on the basis of average number of real xes recorded, randomly assigned within the study areas. We dened 19 habitat features as deciduous wood, oak grove, chestnut grove, hybrid poplar plantation, orchard and garden, willow grove, ooded herbaceous cover, reed-bed, ditches, river bank and riparian habitat, pond, grassland, pasture, cultivation and vineyard, shrub of bramble, hedges, road and path, barn and abandoned house, and at last farm and houses. Habitat diversity was assessed by the index E = A 1/S 1, where A = 1/ Pi2 [30] and S is the total number of habitat type, considering only 6 major habitat types. An analysis of variance was used to investigate dierences in habitat features among male sites considering male sites with consortship success, unconsorted male sites, and random sites. Because all females consorted, we only discriminated between habitat use from February to April (mating period) and from April to June (period of parturition). Paired t-test (with Bonferroni adjustment procedure) or Welch alternate t-test is used according to the case.

2. Methods
Radiotracked polecats (24 males and 25 females, 1992 2002) were mainly surveyed from winter to spring in Western France (Bri` re 47 20 N, 2 10 W, lake of Grande Lieu and Tenu river 47 05 N, 1 39 W), and data from each individual was only used once. The climate of an oceanic type is mild and humid (mean temperature August 20 C, and mean temperature February 5 C, annual precipitation 650 mm, with about 2 snowy days per year). Every animal was surveyed 121223 days, but numerous individuals were recaptured several times. From a capture-recapture design, density estimates were regarded as moderately high ranging from 0.35 to 0.57 individuals per km2 in 2002. The consortship behaviour consists of a brief association between an adult male and an adult female, showing activity within the same restricted area and often resting together in the same den during oestrus [26, 27]. Consortship success was determined by trapping, incidental observations (using night vision optics NONH4U), and radiotracking locations. Throughout the reproductive season, trapping sessions were repeatedly conducted using 20 box-traps in every studied site in order to detect the presence of other individuals during the mating season. Polecats are usually intolerant towards any congeners, exhibiting a strong individual segregation in the use of space, and associations between individuals are restricted to the breeding period [24, 28, 29]. Because copulation induces ovulation, breeding success depends upon the male tenacity, and most of recaptured females exhibited scratches on the neck and on the back resulting from the copulation, when the male remained on the female with a bite often lasting more than one hour [27]. Therefore, the consortship behaviour provides a good indication of the mating activity [26] although how consortship behaviour is related to breeding success remains unknown. Most of copulations occurred before Apri, and parturitions, as revealed by recaptures of lactating females, occurred from May to June. A consortship was regarded as successful when it has occurred about 42 days (gestation duration) before the estimated date of parturitions. On a basis of a minimum of six consecutive xes per day, the minimal consortship duration was assessed as a number of days during which male and female were diurnally associated in the den. For

3. Results
3.1. Consortship Success. Moving across several female contiguous ranges, most male polecats (80%, n = 19/24) obtained brief consortships averaging 3.11 days (sd = 1.26, range 16 days, and n = 19 males). Males consorted with 1.33 partners (sd = 0.82, n = 24 males). All females consorted with at least one male and obtained a mean of 1.12 consortships (sd = 0.33, n = 25 females; Table 1). The consortship success was related to the consortship duration (rSpearman = 0.705, P < .0001, and n = 25). While consortship patterns in males characterised a polygynous mating system with a single male consorting with one to three females, some females were regarded as polyandrous. 3.2. Habitat Selection. During breeding period, polecats mainly used marshes and wooded areas, but habitat use diered between the sexes, females occupying signicantly more woods and hedges, while males exploited mainly marshes ( 2 = 42.3, P < .0001, df = 4) (Figure 1). Actually, habitat preferences seemed to be only based on supercial features of habitat, and marshy habitat features and deciduous woods appeared as the most important descriptors of polecat habitat. Habitat use in males was

International Journal of Zoology

Table 1: Consortship duration and consortship success (number of sexual partners) for 24 radiotracked males and 25 females of European polecats Mustela putorius from Western France. Number Successful of ConMales sexual sortship partners with M1 M2 M3 M4 M5 M6 M7 M8 M9 1 1 1 2 1 2 1 1 3 F1 F2 F3 F4 F5 F6 F7 F8 F9 F10 F11 F12 F13 F14 F15 F16 F17 F18 F19 F20 F21 F22 F23 F24 F25 F17 F18 F20 Number of sexual Consortship partnersduration for (days) female 1 4 1 3 1 4 1 2 1 1 1 1 1 5 1 2 2 1 1 6 2 3 2 3 1 2 1 3 1 3 1 4 1 3 1 5 1 3 1 4 1 5 1 3 1 3 1 3 1 4 1 2 1 3 1 2 0 0 0 0 0 Mean = Mean = 2.33 1.12
Habitat use 100

75

(%)

50

25

0 Males Females

M10 Breeding males M11 M12 M13 M14 M15 M16 M17 M18 M19 M20 M21 M22 M23 M24

2 2 1 2 2 2 1 1 1 1 0 0 0 0 0 Mean = 1.33

Hedges, shrubs Meadows Riparian habitats

Marshes, ponds Deciduous woods

Figure 1: Habitat use in male and female radiotracked polecats based on percentage of xes found in a considered habitat. Table 2: Dierences among habitats used by 24 male and 25 female polecats and random sites (Anova from radiotracking locations, signicant P value in bold). Mean square Males Deciduous woods 0.0019 Marshy areas 0.429 Riparian habitat 0.0033 Meadows and cultivation 0.523 Hedges and shrubs 0.021 Females Deciduous woods 0.102 Marshy areas 0.114 Riparian habitat 0.0026 Meadows and cultivation 0.715 Hedges and shrubs 0.056 Degree of Fisher freedom F 1,39 1,39 1,39 1,39 1,39 1,39 1,39 1,39 1,39 1,39 0.87 69.25 2.47 104.38 12.42 16.38 18.39 0.99 175.6 28.9 P .358 .0001 0.125 .0001 .0011 .0001 .0001 .325 .0001 .0001

chiey inuenced by willows, reedbeds, ooded herbaceous cover, and ditches, and in females, the choice of parturition sites was mainly inuenced by ashes, oaks, willows, and reedbeds. Nonetheless, evidence of habitat selection was found when dierences among habitats, respectively, used by polecats, and habitats in random sites were tested with ANOVA (Table 2). In male polecats, marshy areas were the dominant habitat type, while meadows and various cultivations were

deserted. Moreover, polecats used signicantly more shrubs and hedges than other habitats. Female polecats were very selective in their habitat preferences using signicantly more deciduous woods, hedges and shrubs, and marshy areas than randomly estimated, and they poorly utilised meadows and cultivation. Furthermore, habitat use dierences were found according to the consortship success (Figure 2), unconsorted male polecats using signicantly more deciduous woods and less marshy areas than consorted polecats (Table 3). Because all

4
Habitat selection in males 100 100

International Journal of Zoology

Habitat shift in female polecats

75

75

(%)

(%)

50

50

25

25

0 Consorted Barns, farms Hedges, shrubs Meadows Unconsorted Riparian habitats Marshes, ponds Deciduous woods

0 Spring home range Hedges, shrubs Meadows Riparian habitats June home range Marshes, ponds Deciduous woods

Figure 2: Habitat selection according to the consortship success of radiotracked male polecats. (n = 19 consorted polecats and n = 5 unconsorted polecats) as revealed by percentage of xes recorded in a considered habitat.

Figure 3: Habitat shift in surveyed female polecats from March (consortship sites) to June (parturition sites) as revealed by percentage of xes recorded in a considered habitat.

4. Discussion
Table 3: Dierences among habitat used by consorted (n = 19) and nonconsorted males (n = 5) (Anova from radiotracking locations, signicant P value in bold). Males Deciduous woods Marshy areas Riparian habitat Meadows and cultivation Hedges and shrubs Mean square 0.089 0.022 0.034 0.018 0.0008 Degree of freedom 1,23 1,23 1,23 1,23 1,23 Fisher F 4.68 5.03 2.05 0.95 0.34 P .042 .035 .166 .338 .564

surveyed female polecats consorted and bred successfully, it was impossible to run a same analysis. Nevertheless, pregnant or lactating females settled in distinct areas in MayJune switching for more woody habitats (paired t-test = 6.28, P < .0001, and df = 23, Figure 3) and riparian habitats (paired t-test = 2.31, P = .03, and df = 23) whereas the use of marshy areas decreased (paired t-test = 9.57, P < .0001, and df = 23). The use of shrubs and hedges increased (paired t-test = 3.58, P < .002, and df = 23) probably related to the search for a quiet parturition place. The index of habitat diversity signicantly diered between space used by consorted polecats (E = 0.225, sd = 0.062) and random sites (0.428, sd = 0.087) (Welch T-test = 11.2, P < .0001, df = 53).

Polecats shifted for marshy and wooded areas during their breeding period, but many habitat features did not clearly dier from random sites with regard to most of their characteristics. Studies of animal distribution in habitats often dealt with habitat preferences with no assessment of mating success or remained mainly based on indirect approach such as variations in density or abundance [3, 15, 31, 32]. Such approaches described habitat features, which could be poorly related to tness but rather with resource availability [8]. Measurement of habitat features, which were directly associated with breeding activities such as nesting, should more reect habitat selection [8, 13, 33, 34]. Habitat features associated with consortship success should at least indirectly reect features that aect tness. Mating sites diered from random sites only in some rough habitat features, and characteristics of successful mating sites have uncertain ecological meaning. Three nonexclusive causes could be evoked for such ndings. Firstly, it may be alleged that every habitat type induces few dierences in tness, and thus, further habitat selection does not occur in polecat. Secondly, habitat use can be regarded as a result of limited opportunities for animals to optimise when preferred habitats are saturated. Thirdly, searching for the preferred habitat may result in a relatively low benet. Because habitats features diered between random sites and mating sites, it should be recognised that polecats exhibited at least a slight selection for habitat. Diversity of habitat used by breeding polecat diered signicantly from random sites, revealing that certain habitat were less occupied during reproduction. Nevertheless, it could be

International Journal of Zoology suspected that low benets in mating success resulted from habitat selection. Habitat requirements of most vertebrates seem to be based on simple supercial features of habitat [21, 3438]. Thus, the stone marten exhibited a preference for stony environment and regardless of other habitat features inhabited deciduous woods as well as barns, farms, or buildings in towns [25, 39]. Following Haila et al. [35], it may be suggested that habitat avoidance rather than habitat preference can explain such predilection. Polecats were found to avoid open meadows and cultivation and seemed to prefer high vegetation cover or undisturbed areas. Polecats showed very secretive movements in shrubs and along hedges, resting in dense vegetation, in burrows or warrens. Habitats were selectively exploited, and while polecats often moved sheltered by hedges and shrubs, most open environments were deserted. The use of bramble patches is regarded as a need for protection against predators [40]. Woods, hedges, and shrubs may ensure more protected movements [41], and most mustelids were also known to avoid openelds [40, 42, 43]. Moreover, as reproductive activity resulting in a reduced vigilance, mating may be aected by the existence of refuges. At the broader scale of habitat selection, some factors, chiey marshy and wooded habitats, were found to inuence mating success. Although some carnivores could be thought as habitat generalists, habitat denition has been recognised as scale dependent [14, 44]. Thus, successfully consorted polecats signicantly used more marshes and were found less frequently in deciduous woods than unconsorted males, whereas pregnant or lactating females increased their use of wooded areas. Habitat preferences identied for polecat males were clearly adaptive in that mating success was greater using more marshy areas than other habitats, but the reason why mating success was associated with such broad habitat features remains unclear. Marshes consisted of heterogeneous vegetation cover but were seldom used by other carnivores. Marshy areas may be regarded as preferred habitat, and polecats were found to competitively exploit a specic habitat niche. The inuence of trophic availability on habitat selection patterns cannot be ruled out [45, 46], but, as most animals, when polecats searched for mates, they considerably reduced their feeding activities. Finally, the link between the genetic divergence within polecat populations and polecat partitioning for habitat [47] supports the adaptive signicance of habitat preference. Polecats were selective in habitat use and exhibited a strong sexual segregation both in the use of space and in the activity rhythms [24], with females avoiding male-occupied zones and displaying cautiousness towards their unfamiliar conspecics. Female avoidance from male ranges may be related to the need of protection for ospring [24]. Additionally, this spatial pattern may reect a segregation limiting ecological competition [46]. Such reduced overlap was also observed in other carnivores such as the skunk [48]. Similarly, in grizzly bear, females with cubs tended to avoid habitat used by males throughout the year [12, 49]. The polecat mating system was characterised by a successive polygynous strategy, but averaging only 1.6 females

5 per male, the polygyny rate appeared very low. Because polecats assiduously exploited some patchy area until resource depletion, solitary habits were basically proved to be adaptive [24, 46, 50]. Conversely, such habits result in a low polygyny rate, suggesting an evolutionary cost induced by this specic spatial pattern. Anyway, that certain habitat features favour a best mating success constitutes a key factor for polecat conservation and environmental management.

Acknowledgments
The author thanks all his assistants for help in collecting the eld data and especially Y. Benoit, Y. Biraud, H. Brault, F. Cupertino, R. Dagault, F. Dussault, A. Pihuit, M. Pondaven, and J. Y. Robert. Thanks are also due to D. Le Jacques.

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[48]

[30] [31]

[49]

[32]

[50]

[33]

[34]

[35]

Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 362976, 11 pages doi:10.1155/2011/362976

Review Article A Review and Interspecic Comparison of Nocturnal and Cathemeral Strepsirhine Primate Olfactory Behavioural Ecology
Ian C. Colquhoun
Department of Anthropology and The Centre for Environment and Sustainability, The University of Western Ontario, London, ON, Canada N6A 5C2 Correspondence should be addressed to Ian C. Colquhoun, colquhou@uwo.ca Received 13 November 2010; Revised 2 February 2011; Accepted 17 March 2011 Academic Editor: Lesley Rogers Copyright 2011 Ian C. Colquhoun. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. This paper provides a comparative review of the known patterns of olfactory behavioural ecology among the nocturnal strepsirhine primates and the cathemeral lemurid genus Eulemur. Endemic to Madagascar, all Eulemur species exhibit both diurnality and nocturnality (i.e., cathemerality), and are gregarious, making them an interesting group of taxa to compare with the nocturnal strepsirhines. This paper represents the rst comparative review of patterns of olfactory communication among the nocturnal strepsirhines and the cathemeral Eulemur species. Inductive assessment of these comparative data indicates that olfactory communication serves multiple functions in both groups, including individual recognition, sex recognition, indication of social dominance, and coordination of mating behaviour. However, the urine-washing behaviour characteristic of many nocturnal strepsirhines has no clear homologue among Eulemur species (although the latter may use urine droplets in scent marking). Despite sparse and scattered comparative data, it appears that Eulemur species exhibit dierent olfactory communication patterns that are associated with diering social organizations in this genus.

1. Introduction
In their 2004 paper reviewing comparative data on latrine behaviour among lemur species, Irwin and coauthors [1] contended that, . . . the use of chemical signals in primate communication is well documented. On this point, they cited two fundamental sources: rst, Alain Schillings 1979 review paper, Olfactory Communication in Prosimians [2], and second, Gisela Epples 1986 review of primate olfactory behaviour, Communication by Chemical Signals [3]. There are two important things to note concerning this pair of key publications on primate olfactory behaviour. The rst is that, although it has been 32 and 25 years, respectively, since these works were published, both continue to be required reading in the eld of primate olfactory communication. The second is that both these publications predate the 1987 denition of primate species with both diurnal and nocturnal activity patterns as being cathemeral, or active through the day (i.e., through the 24-hour daily cycle) [4]. This denition ushered in the extensive attention the

lemuriform primate genus Eulemur has received concerning this distinctive activity pattern, (e.g., [57], and references therein). Genus Eulemur and all the other lemuriform primates native to Madagascar, together with the lorisiform primates of Africa and Asia, represent a major adaptive radiation within the Order Primatesthe Suborder Strepsirhini. These primates retain the ancestral mammalian characteristic of the rhinarium (or wet nose). Strepsirhine primates include all the lemur species of Madagascar and the Comoro Islands, the lorises of south and southeastern Asia, and the pottos and galagos (or, bushbabies) of sub-Saharan Africa. In the closing section section of his 1979 paper, Schilling [2] remarked on the apparent distinction between the predominantly deferred olfactory signals of nocturnal strepsirhines and the combined direct olfactory and visual signalling of diurnal strepsirhines, stating, It would be interesting to study this aspect of olfactory communication in species that are intermediate between the two types (emphasis added), that is, which are greagrious to the extent that they live in family groups, and which are more or less nocturnal, like Hapalemur griseus,

2 Avahi laniger, and Lemur mongoz. Thus, the present paper represents the rst comparative review of olfactory communication exhibited by nocturnal strepsirhine primates and the cathemeral Eulemur species. The major aim of this paper is to provide an initial assessment of the types and contexts of olfactory communication of the nocturnal strepsirhines relative to those of the cathemeral genus Eulemur (as well as the cathemeral lemurid species Hapalemur griseus).

International Journal of Zoology the functional role of the VNC has not been fully examined across these former taxa [21, 30]. The accessory olfactory bulb (AOB) of the accessory olfactory system (AOS) is described as large to very large relative to body size in those strepsirhine species that have been examined [15]. There is considerable variation in AOB size relative to body size in those strepsirhine and platyrrhine species for which there are data [15]. The AOB is described as relatively well developed in platyrrhine species, but the available comparative data also indicate that AOBs in New World monkeys are generally reduced in absolute size compared to those of strepsirhine species [15]. In those Old World monkey species (Cercopithecoidea) studied thus far, the AOS is absent in adults [10, 21, 30]. In the ape species (Hominoidea) that have been studied, including humans, the AOB is absent in adults [10, 15]. If the VNO is present in hominoid species (again, including humans), it appears vestigial in structure and is thought to likely be nonfunctional [10, 1316, 19, 20, 2224, 30]. Among the strepsirhines studied to date, nocturnal strepsirhines are reported to both have larger AOBs [15], and larger olfactory bulbs (OBs) [10] than diurnal strepsirhines. Barton and colleagues [12] reported that among nocturnal strepsirhines, there is a positive correlation between the proportion of fruit in the overall diet and the relative size of the OB, (see also [25]). Haplorhine primates, by contrast, have relatively small OBs in comparison to most other mammals [19, 26]. There have been several reports noting that olfaction in primates is relatively under-studied and remains poorly understood (e.g., [10, 20, 21, 26]). Recently, the view has also been expressed that interpreting primate olfactory reception and processing as being functionally divided between the main olfactory system (MOS) and the AOS is too simplistic [8, 10, 19, 20, 27, 28]. Specically, the complexity of primate olfaction is not reected in a functional interpretation that sees the MOS primarily detecting airborne volatile odours from a variety of stimuli in the environment, such as food or predators [19, 27], and the AOS being primarily sensitive to heavy, nonvolatile, uid-borne chemical stimuli, such as urine and scent-marks, as well as pheromones, that communicate sociosexual information [10, 19, 27]. Rather, the emerging view is that there must be a degree of overlap, or integration, in the functioning of the MOS and AOS [8, 10, 19, 20, 27, 28]. This more nuanced interpretation of primate olfaction has been pushed ahead by innovative studies that have made novel applications of research techniques. For example, advances in genomic analyses have made possible the comparison of olfactory receptor (OR) gene families coding for olfactory receptor proteins (ORPs) in dierent primate species and other mammals, (e.g., [9, 11, 18, 19, 23, 24, 28]). Advances have also been realized in several recent studies of primate olfaction through the use of gas chromatography-mass spectrometry (GC-MS) to identify both the volatile components of the glandular secretions used in scent marking, (e.g., [3134]), and the chemical composition of urine [35]. Notably, genetic studies have provided new insights into primate olfactory function. Although testing across the

2. Strepsirhine Olfactory Biology in Comparative Perspective

Before comparing patterns of olfactory communication amongst nocturnal and cathemeral strepsirhine primates, it is useful to rst consider strepsirhine olfactory biology in broader primate and mammalian comparative contexts. Relative to many other mammalian orders (e.g., rodents, artiodactyls, perissodactyls, carnivores), primates have historically been regarded as microsmatic [810]. But the olfactory systems of strepsirhine and haplorhine primates also exhibit considerable dierences in the relative proportions and complexities of their anatomical structures [1019]. Early work in this area produced the proposal that those primate species possessing functional vomeronasal organs (VNOs) might be regarded as relatively macrosmatic while those primate species without functional VNOs could be considered microsmatic, (e.g., [8]). Further, these comparative anatomical data have also been interpreted as indicating, in general, relatively sensitive olfaction among strepsirhines, tarsiers, and platyrrhines, and less keen olfactory abilities among catarrhine primates (i.e., Old World cercopithecoid monkeys and hominoids); these latter taxa are considered more visually adapted, exhibiting specializations such as trichromatic vision [812, 14, 1926]. More recently, however, this interpretation and classication schema has been discarded due to mounting evidence that there is not a direct correspondence between the presence or relative sizes of olfactory structures and olfactory function, (e.g., [10, 19, 27, 28]). In terms of comparative anatomy, the extant strepsirhine primates (together with the extinct adapoid primates of the Eocene epoch) are considered to have retained the primitive eutherian mammal nasal ground plan [10]. All strepsirhine primates possess the rhinarium, the naked, moist tissue surrounding the nostrils, which is also found in many other mammalian taxa but has been lost in all haplorhine primates (i.e., New World monkeys, Old World monkeys, and hominoids [10, 29]). The available comparative anatomical data for members of the Order Primates indicate that both the VNO and the entire vomeronasal complex (VNC) are most fully developed in strepsirhines [13, 14, 30], and likely play critical roles in discrimination among chemical classes of odourants [19] and in pheromonal communication [20]. The available anatomical data on species in the haplorhine infraorders Tarsiiformes (tarsiers) and Platyrrhini (New World, or platyrrhine, monkeys) indicate that these taxa also possess VNCs that are structurally comparable [30] to those found in strepsirhines [10, 14, 17, 18, 30]; however,

International Journal of Zoology Order Primates has not been exhaustive to this point, the V1R and V2R olfactory receptor (OR) gene families and the TRP2 gene (which is crucial for pheromone signal transduction in the VNO) have been examined across several primate genera. These preliminary assessments of the genetics of olfaction have shown that catarrhine primates, with their trichromatic vision, exhibit a signicantly higher proportion of nonfunctional OR pseudogenes than do either platyrrhine monkeys or strepsirhines [9, 11, 18, 19, 23, 24]. An exception to this taxonomic pattern is the platyrrhine genus Alouatta, the howler monkeys, which have evolved trichromatic vision via convergent evolution and exhibit a level of OR pseudogenization similar to that among catarrhine taxa [11]. Yet, this does not mean that cercopithecoids and hominoids (or Alouatta, for that matter) do not use, or respond to, olfactory communication [19, 29, 36]. Despite lacking the AOS as adults, some cercopithecoid monkeys do exhibit scentmarking behaviour (e.g., [37, 38]). Although scent-marking behaviour has not been recorded among hominoid taxa [10, 39, 40], available comparative data show that specialized cutaneous scent glands, such as the axillary apocrine glands, are known in all hominoid genera [10, 39, 40]; this provides a likely channel for interindividual olfactory communication and individual recognition in hominoids, including humans [27, 3942]. Similarly, recent GC-MS analyses of the volatile components in mandrill (Mandrillus sphinx) scent marks indicated that, despite the mandrill apparently lacking a functional AOS, individual odour proles convey information about the signaller, including age, sex, dominance rank of adult males, and perhaps identity of the signaller [43]. Additionally, odour similarity between signaller and receiver is related to major histocompatibility (MHC) concordance, and represents a potential mechanism for mate selection by females in favour of MHC-diverse males [44]. These new insights into olfactory communication in a catarrhine primate seem to provide an example of the suggestion that, even without functional AOSs or VNOs, catarrhines can still detect and respond to sociosexual odour cues and pheromonal stimuli through ORPs that are expressed in the main olfactory epithelium [10, 19, 20, 22, 27, 28]. So, while we have an emerging picture of humans and other catarrhine primates being capable of responding to an array of odour cues, including chemosensory responses to volatile components of some odours [10, 19, 20, 27, 28, 43, 44], the available comparative data on strepsirhine primates (where we nd species that exhibit retention of the rhinarium, well-developed AOSs, relatively large AOBs, functional VNOs, intact OR gene families coding for functional ORPs, plus functional integration of the AOSs and the MOSs), indicate that strepsirhine primate taxa experience considerable complexity in their olfactory communication [10, 19, 20, 28, 35]. The important role of scent marking and olfactory communication in strepsirhine behavioural ecology, particularly in regard to reproductive behaviour, has been recognized for decades, (e.g., [45]). Yet, despite this, and despite important comparative works like those by Schilling [2] and Epple [3], it is surprising how little-studied strepsirhine olfactory communication remains and how little we know with certainty about strepsirhine

3 olfactory behavioural ecology. This relates to the general point raised repeatedly in the literature that research into primate olfaction lags far behind that on primate visual and vocal systems, for example, [10, 20, 21, 26]. For example, the comments of Rowell [46] over 30 years ago remain surprisingly current: Prosimians are smelly animals. . . olfactory communication occurs both at a distance and in body contact, but monitoring the conversation presents diculties for our olfactorily unsophisticated species and proceeds slowly. Over the last decade, for every peerreviewed paper dealing with primate olfaction, 115 dealing with primate vision have been published (e.g., see the PrimateLit database: http://primatelit.library.wisc.edu; see also [26]). From this, we can appreciate why Heymann [26] concluded that, Thus, it is appropriate to consider olfaction as a sense that is still neglected in the study of nonhuman primates. All this is by way of pointing out that the present, and any other, comparative review of olfactory behavioural ecology across strepsirhine primate species must rely on a body of information that is fragmentary and scattered. Thus, this review must be regarded as entirely preliminary. Recent taxonomies recognize at least 26 lorisiform strepsirhine species (i.e., the lorises, pottos, and galagos, or bushbabies; see [47]) while the number of recognized lemuriform strepsirhine species endemic to Madagascar approaches 100 and is still climbing [4850]. For most of these lorisiform and lemuriform taxa, however, there is no information available on the behavioural ecology of their olfactory communication.

3. Nocturnal and Cathemeral Strepsirhines: Comparative Data

In order to review the literature relating to strepsirhine primate olfactory behavioural ecology as completely as possible, and given the scant literature that deals explicitly with primate olfaction (see above), it was also necessary to consult reports, on strepsirhine primate species, that have dealt primarily with other topics (such as social organization, social behaviour, ranging ecology, etc.), and glean whatever material could be found concerning olfactory communication. This entailed having to pull information from a sentence here or an anecdote there, in a literature that is very scattered (relevant material was found in publications that focused on primatology, anthropology, behaviour, chemical ecology, mammalogy, and zoology). This simply underscores the fact that the behavioural ecology of strepsirhine primate olfaction and olfactory behaviour remains both a poorly researched and poorly understood dimension of the overall behavioural ecology of these taxa. It also points to this area being an extremely fertile and promising area for future research on the behavioural ecology of strepsirhine primates (moreover, the same applies to the study of primate olfactory behavioural ecology in general, as several recent publications reect, e.g., [20, 2628, 42, 43, 51]).

4 3.1. Nocturnal Lemuriforms 3.1.1. Genus Microcebus: The Mouse Lemurs. Microcebus murinus, the gray mouse lemur, is the lemuriform species for which the accessory olfactory system (AOS), including the vomeronasal organ, has most fully been investigated [52]. In M. murinus, male-male, male-female, and female-female socio-sexual interactions are mediated and coordinated by urinary chemosensory cues [5355]. Studies of M. murinus in captivity have shown that male urinary marking behaviour decreases with age [56, 57]. The suite of scent-marking behaviours known for the gray mouse lemur includes punctuated urine marking (sometimes with perineal wiping), head rubbing and muzzle or lip wiping, branch chewing with salivary deposition, and, especially, urine washing (where individuals purposefully urinate on their hands and feet), which accounts for over 80% of all scent-marking behaviours performed [2, 3, 5861]. In a recent eld study of the golden brown mouse lemur (M. ravelobensis), Braune and colleagues [62] recognized two forms of scent marking: urine washing, and mouth wiping (sometimes with face and/or head rubbing). 3.1.2. Genus Mirza: The Giant Mouse Lemurs. Olfactory communication among Mirza during reproductive behaviour includes nasonasal, nasobody and nasogenital contact [63]. Both punctuated urine marking and urine trail marking occur, and experimental work indicates males can discriminate among the urine marks of conspecics [3, 58]. Both males and females anogenital scent mark, and, like Microcebus, Mirza also engages in salivary marking [59]. Notably, Mirza would also appear to exhibit ehmen (see photo Figure 8 in [59]the caption reads, The typical posture for smelling a mark of a conspecic; note the open mouth, and retracted tongue, emphasis added; cf. [64]). 3.1.3. Genus Cheirogaleus: The Dwarf Lemurs. Data on olfactory communication are available for the greater dwarf lemur (Cheirogaleus major) and the fat-tailed dwarf lemur (C. medius). Both species exhibit punctuated urine marking and urine trail marking, as well as anogenital scent marking [2, 58], but the dwarf lemurs are notable for their specialized fecal marking of branches [2, 65], which Irwin and colleagues [1] identify as arboreal latrine behaviour. Dwarf lemur fecal marking may be related to territorial advertisement. 3.1.4. Genus Phaner: The fork-Marked Lemurs. Phaner stands out amongst the nocturnal lemuriforms because of the apparent absence of any form of urine marking in this genus [2, 66]. Males may rarely scent mark branches with their throat gland [67]; more often, males use their throat gland to scent mark females during allogrooming bouts [66]. 3.1.5. Genus Lepilemur: The Sportive Lemurs. Like most other nocturnal strepsirhines studied to date, sportive lemurs exhibit urine marking [2, 3, 58]. Only males are reported to anogenital scent mark [13]. Although Lepilemur species

International Journal of Zoology are totally arboreal, patterns of defecation produce terrestrial latrines that seem to be linked to resource defence [13, 68]. 3.1.6. Genus Daubentonia: The Aye-Aye. Both sexes exhibit anogenital scent marking [2, 69], and female anogenital scent marking increases during estrus [70]. Aye-ayes also engage in urine trail marking [2, 71, 72]. 3.1.7. Genus Avahi: The Woolly Lemurs. The woolly lemurs are not at all well-studied; there is a dearth of research on their behavioural ecology. I could not nd any published information on the olfactory behavioural ecology of Avahi. 3.2. The Lorisiformes. All taxa that have been studied in this nocturnal primate infraorder (that is, the lorises, pottos, and galagos, or bushbabies) scent mark extensively with urine [58], and urine marking is much more frequent than glandular scent marking. Together with the lorisine genus Loris, all galagine primates studied to date (except the galago genus Euoticus) exhibit both urine washing and punctuated urine marking (or rhythmic micturition) [73 76]. Urine washing can occur in a variety of contexts, including mobbing behaviour, moving into an unfamiliar area, during agonistic and aggressive encounters, and, in social interactions, especially when a female is in estrus [76 78]. Greater galagos (Otolemur crassicaudatus) have been shown experimentally to dierentiate scent marks by sex and by individual [78, 79]. Allens galago (Sciurocheirus alleni) shows high frequencies of urine marking in territorial boundary zones [80]. Scent marking seems also to function as a stress-reducing mechanism in the small-eared bushbaby (Otolemur garnettii) [81]. Urine washing in Loris, the slender loris, has been reported to often occur in the context of consuming noxious insect prey, both before catching the prey and after consuming the prey; urine washing would also occur if a loris was stung by an insect [82]. Loris females have also been observed to urine wash before they groom their infantsthis has been proposed to possibly have an antipredator function when females park their infants while they forage (i.e., the possible anti-predator function of a female urine washing and then grooming her infant could be either that it provides an olfactory screen or barrier against potential predators, or that it acts as a form of predator mimicry while the infant is parked) [82]. All lorisine primates studied thus far exhibit urine trail marking in addition to punctuated urine marking [2, 58, 76, 83]. In Loris, inter-sexual social interactions often see males either sning the muzzle or anogenital region of females [82, 84]. During allogrooming bouts, Loris males and females will lick and rub a specialized brachial gland on their own face and body and on the body of the grooming partner [82]. Perodicticus, the potto, exhibits genital scratch grooming during which grooming partners of both sexes scent mark each otherthis behaviour is not linked to reproduction [85]. In Perodicticus, urine marking may accompany allogrooming [86]. During allogrooming, pottos also mark each other with saliva and genital secretions [87]. Arctocebus,

International Journal of Zoology

Table 1: Comparative interspecic proles of scent marking behaviours among nocturnal strepsirhine genera (i.e., lemuriforms, galagines, and lorisines) and the cathemeral lemurid genera Eulemur and Hapalemur, as derived from the published literature on these taxa [13, 52 112]. Scent-marking behaviours: 1, urine washing; 2, punctuated urine marking; 3, urine-trail marking; 4, muzzle wipe/branch chewing (saliva deposition); 5, ehmen; 6, fecal marking; 7, latrine behaviour; 8, anogenital scent marking; 9, head marking (males). Scent-marking behaviours Strepsirhine taxon (refs) Nocturnal lemuriforms Microcebus [2, 3, 5262]] Mirza [3, 58, 59, 63, 64] Cheirogaleus [1, 2, 58, 65] Phaner [2, 6, 66, 67] 1 +

2 + + + ?

4 + + ? ?

5 ? + ? ?

9 + ? ? + (Male throat gland) ?

+ + ?

+ (Both sexes) +
(?)

Lepilemur [13, 58, 68] Daubentonia [2, 68, 69, 71, 72] Avahi (no refs.) Galagines [58, 7383] Galagoides Galago Euoticus Sciurocheirus Otolemur Lorisines [2, 58, 76, 82, 8489] Loris Nycticebus Perodicticus Arctocebus

(?)

+ ? ? + +

? ? ? ? ? ? ? ?

? ? ? ? ? ? ? ?

(?)

+
(?)

+ (Males) + +(?) ? ? ? ? +

+ ?

? ? ? ? ? ?

+ +

+ +

+ +

+ + + +

+ + + +

? ? ? ?

+ ? + ?

+ ? + + + = passing over

Cathemeral lemuriforms [13, 90113] Eulemur Hapalemur

+ +

+ +

+ ?

+ +

the golden potto, exhibits distinctive passing over scentmarking behaviour, where the male straddles the female and scent-marks her dorsum [85]. Passing over has also been observed in Loris and Perodicticus [82]. Flehmen behaviour has recently been described in these two genera [82]; in Loris, it followed the licking of a urine mark while in Perodicticus it followed a male sning a substrate in a females home range [82]. Nycticebus, the slow loris, apparently possesses a fear scent (an Angstgeruch), and this has also been suggested for Perodicticus and Arctocebus (especially in the context of mother-infant alarm communication [86]); similarly, Loris has been suggested to have an anti-predator alarm pheromone [82]. Male pygmy slow lorises (N. pygmaeus) countermark, with urine, on both male and female urine

marks. Males countermark the urine marks of other males with signicant amounts of urine. In this species, estrus females appear to prefer countermarking males [88], and males whose scent-mark odours are already familiar to them [89]. 3.3. The Cathemeral Lemurids. Comparative data on the olfactory communication of cathemeral lemurids, a good deal of it from eld research reported since 1990, reveals both broad similarities with nocturnal strepsirhines (see Table 1; [13, 52113]), as well as interesting, and unforeseen, distinctions among the cathemeral lemurids themselves (see Table 2; [13, 90113]). In addition to anogenital scentmarking, most cathemeral lemurid species also make use

International Journal of Zoology

Table 2: Comparative interspecic proles of scent marking behaviours among lemurid species of the genera Eulemur and Hapalemur, as derived from the published literature on these taxa [13, 90113]. The patterns seen in the two pair-bonded Eulemur species, E. mongoz and E. rubriventer, are very similar to each other, and contrast in signicant ways to the patterns exhibited amongst the Eulemur taxa that occur in multimale, multifemale social groups (i.e., the E. fulvus group of taxa, E. macaco, and E. coronatus). Scent-marking behaviours Anogenital scent-mark surfaces Urine mark Bite mark (saliva deposition) males Anogenital mark Conspecics HeadMarking (males) Hand/palmarmarking (males) Anogenital sni (M F) Self-marking Marking during inter-group encounters E. fulvus group + + + E. macaco + + + E. coronatus + + + E. mongoz + + Cheek rubbing MF FM + + +

E. rubriventer + ? Teeth grinding during inter-group encounters MF FM + + +

Hapalemur + + +

MF + + + Observed in captivity

MF + + + Observed in captivity

MF + + +

MF

Variable.Vocal & Vocal and visual visual displays; displays some marking + (pers. obs.)

Vocal & visual displays

+ (Incl. F (Both substrate overmarking of and self-marking) M anogen marks) ?

Antebrachial gland marking + M marks tail with antebrachial glands to stink ght other Ms +

Flehmen Latrine behaviour

? +

of punctuated urine marking (deposited concurrently with the anogenital scent markcf. [35], where lemurids, including several Eulemur taxa, are characterized as nonurine marking species). I could not nd any report, however, of punctuated urine marking in Eulemur rubriventer, the red-bellied lemur (also, Tecot, personal communication). Urine washing has never been reported in any cathemeral strepsirhine. Head marking by males occurs across the entire genus Eulemur. Notably, the mongoose lemur (E. mongoz) and the redbellied lemur (E. rubriventer), which are both pair-bonded and territorial species, share similar patterns of olfactory communication [9094]. These two Eulemur species contrast in their patterns of scent-marking behaviour vis-` -vis a their congeners that exhibit multi-male, multi-female social organization: the crowned lemur (E. coronatus) [95, 96], the black lemurs (E. macaco and E. avifrons) [97101], and the brown lemur taxa (E. fulvus, E. rufus, E. sanfordi, E. albifrons, E. rufrons, E. collaris, and E. cinereiceps) [102 109]. I could not nd any report of male bite marking (a behaviour in which a male chews a branch and deposits a salivary mark) in either mongoose or red-bellied lemurs. Although male bite marking has not been reported in these two species, male mongoose lemurs have been observed to cheek rub branches [91]; whether or not saliva is deposited

in this process is unclear. In both of these pair-bonded Eulemur species, anogenital scent marking of conspecics of the opposite sex is performed by both sexes, rather than only males anogenitally scent marking females (a pattern seen in the multi-male, multi-female group-living Eulemur species). Scent marking also gures prominently during intergroup encounters with conspecic groups in both E. mongoz and E. rubriventer, including females overmarking male anogenital marks in E. rubriventer [93, 94]. These dierential patterns of scent-marking behaviour were only uncovered as emergent patterns because of this comparative review of olfactory communication in the genus Eulemur and other strepsirhine primates. In contrast to mongoose and red-bellied lemurs (i.e., the two Eulemur species that exhibit pair bonding), there is a tendency among the crowned, black, and brown lemurs (i.e., the Eulemur taxa that exhibit multi-male, multi-female social groups), to engage in vigorous visual and vocal intergroup displays rather than intergroup displays involving concerted scent marking. In captivity, however, adjacently housed groups of brown lemurs have been observed to exhibit scent marking in addition to the aforementioned visual and vocal inter-group displays. Self-marking has been reported in captive brown lemurs (E. fulvus) [2], and the gray gentle lemur Hapalemur griseus [113]. Male Hapalemur griseus rub

International Journal of Zoology their antebrachial glands on their tail in advance of facing o against other males in tail-waving stink ghts; these are similar in nature to the stink ght displays of male ring-tailed lemurs (Lemur catta) [44]. I have observed a captive male black lemur (E. macaco) self-mark by repeatedly making palmar markings over his tail. Flehmen behaviour has been reported in the diurnal L. catta ([64]; personal observation). I have also observed a wild male black lemur (E. macaco) exhibit ehmen during the breeding season once when he exhibited the characteristic facial grimace associated with ehmen after actively sning the air, and a second time after the same male snied a tree branch while in proximity to a juvenile male from another social group [100]. The latrine behaviour reported in Hapalemur [1] is unique among the cathemeral lemurids.

7 and dierences among strepsirhine primate species in their chemosensory biology and olfactory communication can be expected from future studies that link odour, genetics, behaviour, and ecology [20, 26, 35, 50, 114].

Acknowledgments
A brief version of this paper was presented in the Symposium on Olfactory Communication in Nocturnal and Cathemeral Primates held during the XXII Congress of the International Primatological Society in Edinburgh, Scotland, August 3 8, 2008. The author thanks to Dr. Sharon Gursky for the invitation to participate in that symposium and for encouragement in the rst place to undertake this comparative look at the behavioural ecology of olfactory communication in nocturnal and cathemeral strepsirhines. Comments provided by two anonymous reviewers and Dr. Lesley Rogers, editor of the paper, were most useful and helped to improve earlier drafts of the paper. The paper was also improved by detailed comments that were kindly provided by Dr. Susan Muir. Heartfelt thanks must go to Caleigh Farrell, the authors student research assistant, for the untold hours and boundless energy she devoted to helping him track down the relevant sources in a very scattered literature. This paper is dedicated to the late Dr. Shelley Saunders.

4. Conclusions
In broad terms, cathemeral lemurids exhibit many forms of olfactory communication that are the same as, or similar to, those seen in nocturnal strepsirhine species, including punctuated urine marking, anogenital scent marking of conspecics, male overmarking of female scent marks, and, in the two pair-bonded Eulemur species, scent marking in territorial boundary zones. Within these broadly similar patterns of olfactory communication across strepsirhine primate species, there are notable distinctions in olfactory communication within the cathemeral genus Eulemur. One pattern is exhibited by the two pair-bonding and territorial Eulemur species (i.e., E. mongoz and E. rubriventer); a second pattern is seen in the Eulemur taxa that occur in larger multi-male, multi-female social groups. Although it should have been within the power of socioecological theory to generate predictions regarding dierences in the olfactory behavioural ecology of Eulemur species with diering forms of social organization, it is also notable that such dierences were uncovered by an intensive inductive review process. Indeed, although many gaps persist in our knowledge of the strepsirhine primates, further inductive collation of both published quantitative data on, and descriptive observations of, these species could well uncover other previously unrecognized emergent patterns in their behavioural ecology. While key insights on strepsirhine behavioural ecology have come from increased eld research on these taxa over the last 20 years, it is telling that much fundamental information on strepsirhine olfactory communication still derives from research conducted in the 1970s and early 1980s. This highlights the extent to which our understanding of the olfactory behavioural ecology of Eulemur species in particular, and strepsirhine primates more generally, is still only in a preliminary state. Future eldwork should strive to record as much contextual data as possible regarding where and when various forms of olfactory communication are used (for example, what forms of olfactory communication may be exclusive to breeding behaviour? Are there types of olfactory communication that may occur primarily during inter-group encounters in zones of home range overlap or at territorial boundaries?). Additional insights on similarities

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Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 670548, 11 pages doi:10.1155/2011/670548

Research Article Leadership of Winter Mixed-Species Flocks by Tufted Titmice (Baeolophus bicolor ): Are Titmice Passive Nuclear Species?
Thomas A. Contreras1 and Kathryn E. Sieving2
1 Biology 2 Department

Department, Washington and Jeerson College, 60 S. Lincoln Street, Washington, PA 15301, USA of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611-0430, USA

Correspondence should be addressed to Thomas A. Contreras, tcontreras@washje.edu Received 30 December 2010; Revised 25 March 2011; Accepted 31 May 2011 Academic Editor: Alan Afton Copyright 2011 T. A. Contreras and K. E. Sieving. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The tufted titmouse (Baeolophus bicolor, TUTI) is a nuclear species in winter foraging ocks whose antipredator calls are used to manage predation risk by diverse heterospecics. We hypothesized that satellite species in mixed ocks follow TUTI (not vice versa), thereby dening the role of TUTI as a passive nuclear species. We followed 20 winter mixed-species ocks in North-Central Florida and assessed angular-angular correlations between overall ock, TUTI, and satellite species movement directions. We observed signicant correlations between overall ock movement directions and those of TUTI, conrming our central prediction. Within ocks, however, ne-scale movement directions of satellite species were often more highly correlated with those of other satellites than with TUTI movements. We conclude that TUTI are passive nuclear species whose movements dene ock paths, but within ocks, TUTI movements may have less inuence on satellite movements than do other factors.

1. Introduction
Multispecies bird ocks, comprising individuals that move together in organized association with each other as they forage during daylight hours, are a common phenomenon in forested ecosystems of the world [1]. Flock participants occupy dierent behavioral niches, or social roles, within ocks. Flocking species are generally classied into nuclear and satellite roles [24]. Nuclear species are those ock participants whose conspicuous behaviors (distinctive alarm or other vocalizations and active movements) enhance ock cohesion and may stimulate ock formation. Nuclear species are typically intraspecically social (occurring in extended family groups for some of the year), and they occur more often in ocks than outside of them when ocks occur [5, 6]. Nuclear species are thought to fall into two general categories : passive or active nuclear species [2, 3]. Passive nuclearity is hypothesized to come about when satellite species actively seek out and follow the nuclear species, thereby dening the nuclear species as the ock leader. Conversely, active nuclear species are hypothesized to seek out and join existing mixedspecies ocks and are just as likely to follow the satellites as

to be followed by satellites, but active nuclear species are still able to maintain ock cohesion (see review in Farley et al. [4]). A variety of tness benets can accrue to satellite species as a result of ocking with nuclear species, but benets to nuclear species are less obvious [712]. Parids (family Paridae) function as nuclear species in winter and nonbreeding mixed-species forest ocks in North America and elsewhere in the Holarctic [4, 79, 13]. As a family, parids have traits that predispose them to nuclear roles in heterospecic groups; they are intraspecically social [1, 14, 15] and aggressive mobbers of potential predators, usually leading mobbing events; their behavior may signicantly reduce predation risk for satellite species [4, 11, 13, 14, 1619]. In the Eastern United States of America, the tufted titmouse (TUTI; Baeolophus bicolor) is a socially dominant parid that functions as a nuclear species in ocks even where TUTI co-occur with chickadees in ocks (chickadees may also serve as nuclear species when not participating in ocks with TUTI [14]). TUTI, like other parids, produce copious threat-related vocalizations that are thought to be signals meant for conspecics but that are used as informational cues by numerous heterospecics [1922]. Some parids give

2 food-related cues for conspecics [23], but their use by heterospecics has not been documented to our knowledge. Thus, the central known tness benets available to satellite species, or heterospecic associates of parids more generally, may be the reduction of predation risk during critical activities [9, 19]. Dolby and Grubb Jr. [7] demonstrated that when TUTI were removed from isolated woodlots, individuals of satellite species remaining in those woodlots in winter occupied reduced foraging niches, avoided exposed foraging sites, and declined in overall physical condition relative to individuals who were in woodlots where TUTI had not been removed. The presence of parids enhances access to resources and microhabitats within forest bird home ranges ([9]; aids heterospecics in nding suitable breeding habitat via heterospecic attraction; [24]) and possibly increases nest success [25]. These ndings suggest that the prodigious amount of information that parids produce concerning their immediate perceptions of predation risk aids their fellow prey species in many aspects of decision making including (a) increased foraging eciency, (b) access to critical microand macrohabitats, and (c) an elevation of the eectiveness of antipredator defense [10, 19, 22, 25, 26]. Determination of whether nuclear species interact with heterospecics passively or actively in mixed ocks has only received speculation at this point [10], yet this kind of information could enhance understanding of the evolutionary ecology of facilitation, parasitism, and mutualism in animal communities [27]. For example, if titmice are active nuclear species, soliciting close relationships with other species, it would suggest that they accrue benets from associated heterospecics [28]. In this case, it might be productive to test whether the nely tuned antipredator calls of tufted titmice may involve active signaling to heterospecics rather than being purely intraspecic (kin) signals that are gleaned by eavesdropping heterospecics [15]. If, however, titmice are passive ock leaders being followed by other species, then exploring aspects of heterospecic exploitation of the nuclear species would be most productive [10]. To date, we have conicting evidence regarding what tufted titmice may gain in the presence of heterospecics. One potential benet is food items taken from smaller satellites (kleptoparasitism; [29]). However, we have witnessed that the only species in actively foraging mixed ocks that reliably get killed during hawk attacks are titmice (T. A. Contreras and K. E. Sieving, unpublished data), suggesting that the presence of ocks may be an important tness cost to titmice. Here, we sought to determine whether TUTI are passive or active nuclear species in order to inform future research questions and critically assess the common assumption that mixed-species bird ocks are models of mutualism [30]. If satellite and nuclear species are not gaining tness through association, then it would be more productive to assume that the full range of exploitative (parasitic and commensal) and mutualistic relationships are displayed in ocks [10, 27, 31]. We undertook an analysis to distinguish active from passive ock leadership by TUTI in order to clarify future steps in understanding the ecological and evolutionary relationships acting within mixed species ocks.

International Journal of Zoology Studies in North-Central Florida [4, 9, 16, 17] and elsewhere in Eastern NA (see Greenberg [1]) identify TUTI as the primary nuclear species in most winter mixed-species bird ocks. While this classication of TUTI is based on their pervasive presence in winter foraging ocks and their dominating role in mixed-species mobbing ocks [7, 9], the question remains whether TUTI are functioning as passive or active nuclear species in winter foraging ocks. Accordingly, we used a correlative analysis of TUTI and satellite movements at two spatial scales of ocking behavior which we categorized as: (1) the correlation between the movement of TUTI or satellites with overall ock movement through a landscape (ock leadership) and (2) the correlation between the movement of TUTI or satellites with the movement of immediate ock members (within-ock movement). We followed mixed-species ocks during a single winter (2004) in North-Central Florida, mapping the overall movement directions of ocks and the movement directions of randomly selected satellite species and TUTI in each ock (providing comparisons for both analyses; ock leadership, and within-ock movements). Based on Farley et al. [4], we classied individuals in the ock as nuclear species (TUTI), satellite species (species who are regular and occasional associates in mixed-species ocks), or nonocking species. If TUTI are functioning as passive nuclear species and ock leaders, then we predicted that (1) overall ock movement direction should be more highly correlated with the movement direction of individual TUTI than with those of satellite species (Figure 1(a)) and (2) the within-ock movement directions of satellite species in ocks should be more highly correlated with the movement direction of the nearest TUTI than with the nearest satellite species (Figure 1(b)). Previous observations of forest bird mobbing activity (see Sieving et al. [9]) also suggest that satellite species may be more likely to move through areas with less vegetative cover (open cover types) when TUTI are present, especially when perceived or actual risk of predation may be high. Therefore, we also predicted stronger correlations between TUTI movement direction and ock movement direction as ocks move through more open cover types.

2. Materials and Methods

2.1. Study System. To test our predictions, we observed and followed wintering mixed-species: forest passerine ocks in North-Central Florida from January to March, 2004. Flocks were observed at 3 sites: (1) the University of Floridas Ordway-Swisher Biological Station (Putnam County; N 29 41 45.6 , W 81 58 56.2 ), (2) the San Felasco Hammock Preserve State Park (Alachua County; N 29 42 46.3 , W 82 27 23.7 ), and (3) Paynes Prairie Preserve State Park (Bolens Blu location; Alachua County; N 29 33 24.6 , W 82 19 47.5 ). All 3 sites had similar vegetation and cover types. In hardwood stands (cover type: hardwood), the canopy and subcanopy layers were dominated primarily by laurel oak (Quercus laurifolia), live oak (Q. virginiana), sand live oak (Q. geminata), water oak (Q. nigra), pignut hickory (Carla glabra), sweetgum (Liquidambar styraciua), or cabbage palm (Sabal palmetto), while the understory was

International Journal of Zoology

Satellite species

Responding bird Focal bird N

T3

S3

T2

S2 S1

T1 Species 2 Species 1

TUTI
(a) Hypothesized movement paths

T0
(b) Diagram of ock movement

Figure 1: (a) Illustration of one example of the hypothesized relationships between the overall ock movement path (using successive ock centers to chart the path; black line) and the movement paths of two individual ock participants: TUTI (nuclear species; dashed line) and a satellite species (dotted line). (b) Diagram of a 15-minute portion of a ock movement path with T 0 , T 1 , T 2 , and T 3 representing estimated ock centers at 0, 5, 10, and 15 minutes respectively. Lines S1 , S2 , and S3 represent movement segments between estimated ock centers, with the length of the line representing the movement distance of the ock and the arrow showing the overall ock movement direction (azimuth) between ock centers. Dashed lines (SPECIES 1 and SPECIES 2) represent the observed movements of 2 randomly selected birds observed while at ock center T1 (to be correlated with ock path). Dashed lines at T3 represent the movements of a FOCAL BIRD and a RESPONDING BIRD (an individual in the same general area that moves immediately after the focal individual moves) to be correlated with each other for within-ock analysis. These observations were made at all ock centers.

dominated by Ilex spp., Lyonia spp., and saw palmetto (Serenoa repens). More open habitats (cover type: open) used in the study generally had a sparse overstory of widely dispersed mature longleaf pine (Pinus palustris) with a patchily distributed subcanopy of Quercus spp. (primarily turkey oak (Quercus laevis) and sand live oak), and rosemary (Ceratiola ericoides), and understory dominated by wiregrass (Aristrida stricta), exotic grasses, saw palmetto, and various forms. Flocks occurred throughout the woodland communities of our study areas, and we sought replicate samples in 3 major cover types that were identied as (a) hardwood and (b) pine-dominated (open) forest and (c) the boundaries between these two major forest classications. Indeed, ock dynamics varied across these three habit designations, and we included them as predictors in our analyses (see below). 2.2. Flock Observations and Data Collection. Mixed-species ocks without TUTI are rarely observed in our study region [4]; therefore, we systematically searched each of the 3 study areas for the presence of TUTI using existing trails and roads, and then initiated observations of the associated ocks. To reduce the possibility of pseudoreplication of individual and ock movement data, we never surveyed any specic area more than once and each ock observed was at least 350 m from any other ocks observed, based on maximum reported TUTI winter home range sizes [17, 32]. Once located, ocks were followed for a minimum of 15 minutes, allowing birds to become acclimated to the observer (T. A. Contreras in all cases). Flocks were considered acclimated when birds stopped approaching the observer, and alarm calls were infrequent or directed at other bird species. After acclimation, we followed the ock for a maximum of 55 minutes.

2.2.1. Flock Leadership Data. We collected data for determining ock leadership at 5-minute intervals, and during each interval, we (1) estimated and marked the center of the ock (based on the area of the aggregation with the greatest estimated number of birds) by placing a wire ag in the ground, (2) identied the ocking species and estimated the number of individuals present in the ock, and (3) estimated the movement azimuth (degrees), of multiple randomly selected TUTI and satellite focal individuals at each ock center (azimuths of sampled individuals were estimated from the ock center using a compass; Figure 1(b)). If we lost track of a ock during the observation period, we then searched for a new ock to observe. 2.2.2. Within-Flock Movement Data. During each 5-minute interval, we estimated the direction and distance of movements made by randomly selected individuals in the ock and of the next movement made by another ock participant that was closest to the rst bird, assuming that the responding individual was moving in response to the movement of the focal individual. These estimates were used for determining within-ock movement correlations (Figure 1(b)). To maximize the potential that the responding bird was actually responding to, or aware of, the focal birds movement, the second bird had to be within 5 m of the focal birds initial position and had to move within 60 seconds of the focal birds movement; otherwise, we selected a new focal bird and responding individual. And if, within a ock, we lost track of individuals under observation, we selected a new focal bird and responding individual. To randomly select individuals for observations (both ock leadership and within ock movement), at each ock center, we started at a randomly selected azimuth and

4 then scanned the ock in a clockwise direction for the rst focal individual that moved more than 5 m horizontally. We then estimated the movement distance (using a range-nder) and the movement direction (azimuth) of that individual. The azimuth for each individual was estimated from the initial point where the individual was observed. In some cases, this often meant marking the initial and subsequent horizontal positions with pin ags and then returning later to obtain measurements. Although individuals within ocks were not marked and could have been observed more than once within each ock, randomizing the selection of ock members for observations, and the relatively large number of individuals per ock may has reduced the probability of pseudoreplication of observations of individual ock participants. 2.2.3. Characterization of Flock Path and Habitat. After observations were completed for each ock, we determined the overall path of each ock. We returned to the rst ock center observed (which had been agged) and measured its position using a global positioning system (GPS, accuracy 3 m; Garmin GPSMap 76, Garmin International Inc., Olathe, Kan, USA). The distance and direction (azimuth) of each subsequent ock center relative to the previous ock center was measured using a compass and range nder and then plotted by connecting lines between successive ock centers (Figure 1(b)). Distances between ock centers ranged from 0131 m with a mean distance of 32 21 m (SD). At each of the ock centers, we recorded the cover type that the ock and individuals moved through (for each 5-min segment of movement): (1) hardwood, (2) open (generally pine sandhill or other pine stands with sparse canopy cover), and (3) boundary, for example, the ock crossed the boundary between hardwood and pine cover types during a 5-minute segment. Using the GPS to nd the approximate position of the rst ock center allowed us to plot the overall path using a GIS (ArcView v3.2, ESRI, Redlands, Calif, USA) to view ock centers overlaid on digital orthophoto quarter-quadrangles with 1-m resolution (1999; Land Boundary Information System (LABINS), Florida Dept. of Environmental Protection, Bureau of Survey and Mapping, Tallahassee, Fla, USA) and conrm cover types for each subsequent ock center. In addition, within a 0.05-ha circle surrounding each estimated ock center, we estimated (1) the proportions of overhead canopy (e.g., emergent, dominant, and codominant crown classes) and subcanopy cover using a densitometer, (2) the density of large stems >5-cm diameter at breast height (DBH) using the pointquarter method [33], and (3) the number of small stems <5-cm DBH but >1 m in height within the 0.05-ha circle. We predicted that there would be signicant dierences between hardwood and open cover types in one or more of the vegetation characteristics, and this might help inform our interpretations of movement patterns; that is, birds may move faster or slower through more open habitats, and this can inuence ock cohesion [34]. 2.3. Data Analysis. Two spatial scales of movements were analyzed to assess the prediction that satellite species primar-

International Journal of Zoology ily follow TUTI and not each other. First, we asked which species are leading/directing the path of the ock (ock leadership) by testing whether TUTI movement paths (direction of movements during 5 min intervals) are more highly correlated with the overall ock paths than with satellite species movement directions). Second, we tested whether individual satellite species were tracking the ne-scale movements of nearby titmice more so than those of nearby satellite species (within-ock movements). For all analyses we used = 0.05 to determine statistical signicance. 2.3.1. Flock Leadership. Using movement data for both ocks and individuals for each 5-minute time segment, we rst calculated correlation coecients between the azimuth for ock movement during each of the 5-minute time intervals and the azimuth for randomly selected individuals in the ock during the 5-min interval. We divided analyses between the three cover type classes where ocks were observed (hardwood, open (pine), or boundary), and for this analysis included further subdivisions of the data into two ock movement distance categories (fast, >30 m/5 minutes; slow, <30 m/5 minutes). This latter categorization was adopted, because ock movement rates varied greatly around the mean of 30 m/5 min; some ocks were sometimes stalled, whereas at other times a ock could move up to 131 m/5 min (see Section 2.2. Flock Observations and Data Collection), and we noted that movement dynamics appeared to dier between relatively slow and fast-moving ocks. Finally, analyses were further subdivided by ock role (nuclear (TUTI) vs. satellite species; Table 1). 2.3.2. Within-Flock Movements. To test the prediction that the within-ock movement direction and distance of individual ock members would be more highly correlated with those of the nuclear species (TUTI), we calculated correlation coecients (raa ) and associated 95% condence intervals between the movement azimuths of randomly selected individuals within the ock (focal species) and the rst individual to move after the focal individual moved (responding species). As above, the data were subdivided by focal species type (i.e., nuclear (TUTI) versus satellite species; nonocking species were not included in this analysis) and cover type. We further subdivided the analyses by the movement distance of focal species using two distance classes: individuals moved <15 m or >15 m. These distance classes for within-ock movement are based on the mean within-ock movement of focal species (15.521 m (SD)), and were delineated to represent biologically reasonable distinctions between exploitation of a single foraging patch (within 15 m) versus changing foraging patches (moving more than 15 m in a single movement). Only movements >5 m were recorded/analyzed, since movements of less than 5 m were very frequent and probably correlated with movements of escaping prey rather than ock mates. If only conspecics are responding to focal individuals, then correlations of within-ock movement directions between focal and responding individuals would suggest that the movement of individuals within ocks was inuenced primarily by intraspecic interactions. Therefore, we used

International Journal of Zoology

Table 1: All species encountered in mixed-species ocks during the study (classied into ock roles (nuclear, satellite, or nonocking) based on Farley et al. [4]). Percentage of ocks is the percentage of the 20 ocks where the species was encountered at a minimum of one observation point. Max. number of individuals is the estimated maximum number of individuals in a ock observed at one time. Common name Nuclear Tufted titmouse Satellite Black-and-white warbler Blue-gray gnatcatcher Blue-headed vireo Carolina chickadee Downy woodpecker Scientic name % of ocks/max. # of individuals 100/6 50/2 70/6 30/2 20/3 40/3 15/15 35/2 30/3 95/15 15/1 10/1

5 dierent. If CIs for correlation coecients (in general), and for other directional measures similar to raa s, do not overlap, and if the CIs are similar in magnitude, then meaningful dierences can safely be assumed (see Nakagawa and Cuthill [37] for discussion).

3. Results
3.1. Flock Observations. In total, 20 ocks were observed at our study sites (13 ocks at the Ordway-Swisher Preserve, 5 ocks at the San Felasco Hammock Preserve State Park, and 2 ocks at the Paynes Prairie Preserve State Park) with an average of 8 ock centers mapped per ock path recorded (range = 412 ock centers). There was a signicant difference in ock movement rates (per segment) in dierent cover types (F2,131 = 7.56, P = 0.0007, r 2 = 0.10). Flock movement rates were signicantly greater as ocks crossed boundaries (12.5 4.0 m/minute (SD)) when compared to movement rates of ocks in hardwood (6.1 4.5 m/minute (SD)) or open (6.1 3.5 m/minute (SD)) cover types. A total of 16 species were detected, and besides TUTI, only two others were present in the majority of ocks observed: Ruby-crowned Kinglets and Blue-gray Gnatcatchers which were present in 95% and 70% of the ocks, respectively (Table 1). Mean species richness for the 20 ocks was 5.6 1.7 species per ock (SD) with a mean maximum number of individuals in each ock of 23.8 23.2 individuals (SD). Five common species observed in or near ock centers, that are not ock participants (nonocking species, Farley et al. [4]; Table 1), were excluded from all analyses except for the G-test above. Along ock paths, the proportion of overhead canopy cover was greater in hardwood than in open (pine) cover types (Figure 2(a)), whereas proportions of overhead subcanopy, small stem density, and large stem density were similar between hardwood and open cover types (using 95% condence intervals; Figures 2(a) and 2(b)). This suggests that while canopy cover was dierent between the two general habitat types, subcanopy and shrub cover is similar. 3.2. Flock Leadership. We observed a total of 346 individuals (113 TUTI and 233 satellites) whose movement directions were correlated with ock movement at 117 ock centers. For all cover types (slow and fast-moving ocks pooled) and for both slow and fast-moving ocks (cover types pooled), ock movement direction was more highly correlated with the movement direction of TUTI than with the movement direction of satellites (Figures 3(a), 3(b), and 3(c)). When ocks were moving slowly across boundaries, satellite movement direction and ock movement direction were more highly correlated, whereas in open (pine) cover there was a negative correlation between ock and TUTI movement directions (Figure 3(b)). We note relatively small sample sizes for the latter two ndings (Figure 3(b)). For fast-moving ocks (>30 m/5 minutes; Figure 3(c)), the movement direction of TUTI was more highly correlated with ock movement direction than with the movement direction of satellite species in all cover types. The greatest dierence between correlation coecients calculated for TUTI and satellite species with

Baeolophus bicolor

Mniotilta varia Polioptila caerulea Vireo solitarius Poecile carolinensis Picoides pubescens Dendroica (Yellow) palm warbler palmarum Pine warbler Dendroica pinus Melanerpes Red-bellied woodpecker carolinus Ruby-crowned kinglet Regulus calendula White-eyed vireo Vireo griseus Dendroica Yellow-throated warbler dominica Nonocking Blue jay Cyanocitta cristata Eastern bluebird Sialia sialis Yellow-rumped warbler Dendroica coronata Northern parula Parula americana Zonotrchia White-throated sparrow albicollis

5/3 5/2 15/50+ 10/2 5/20

a G-test of independence to determine if there was a lack of independence between the movement of the focal species observed and whether or not the responding individual was a conspecic or heterospecic. For the G-test we used a 3 2 contingency table with the columns being the ock role of the focal species (nuclear vs. satellite vs. nonocking species) and the rows being whether or not the responding species was a conspecic or heterospecic. Cells within the table contained the frequency of responding individuals. Since correlation coecients for circular data (e.g., azimuths) should not be calculated using statistical tests for linear measurements [35], we used Igor Pro statistical software (v.6.2.1, Wavemetrics, Inc., Lake Oswego, Ore, USA) to calculate Angular-Angular correlation coecients (raa ), which are analogous to a Pearsons r (see methods described in Zar [35] and Fisher [36]) and the 95% condence intervals associated with each raa . If 0 did not fall within the condence interval calculated for an raa , then the correlation coecient was statistically signicant at P < 0.05 [35]. Given the lack of signicance testing options for angular correlations (we found none), we relied on the 95% condence intervals (CI) for each raa to make inferences about whether or not raa s from comparable categories were biologically

6
1 0.9 Proportion overhead cover 0.8 Stems/0.05 ha 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 Canopy Vegetation layer Hardwood Open
(a) Proportion overhead cover

International Journal of Zoology

200 180 160 140 120 100 80 60 40 20 0 Subcanopy Small stems (<5-cm DBH) Large stems (>5-cm DBH) Stem size Hardwood Open
(b) Steam density

Figure 2: Mean overhead canopy cover (a) and mean stem density (b) for hardwood (gray bars) and open (white bars) cover types. Error bars represent 95% condence intervals.

ock directions was when ocks moved quickly across boundaries (Figure 3(c)). 3.3. Within-Flock Movements. We were able to observe and record the movement response of birds to the initial movement of 113 focal individuals (focal species; including 3 observations of nonocking species) across the 20 ocks observed. The ocking type of the focal species observed (nuclear, satellite, or nonocking) was independent of whether or not the responding individual was conspecic or heterospecic (G = 1.4, df = 2, P = 0.5). This suggests that responding individuals did not only respond to conspecic focal individuals. Overall, a responding individuals directionality of movement within the ock was more highly correlated with satellite focal individuals than it was with TUTI focal individuals (Table 2). For movement through dierent cover types, angular-angular correlations (raa ) between the movement direction of focal individuals and responding individuals showed that in hardwoods and more open habitats, a responding species was more likely to move in the same direction as a TUTI than a satellite species; however, at boundaries, a responding individuals movement direction was very highly correlated with the movement direction of satellite focal individuals (Table 2). When considering within-ock movements for the two dierent movement distance classes (<15 m versus >15 m), when focal individuals moved less than fteen meters, a responding individuals movement direction was more correlated with the movement direction of satellite focal individuals and this was also the case for movement through open cover types (Table 2). In open habitat, there was a signicant negative correlation between the within-ock movement direction of TUTI and responding individuals. In contrast, the correlation between the movement directions of TUTI and responding individuals was signicantly greater in hardwood cover (Table 2).

For within-ock movements where focal individuals moved >15 m, a responding individuals movement direction was more correlated with satellite movements for all habitats combined (Table 2). At boundaries, correlations were greater when focal individuals were satellite species (there was no signicant correlation for focal TUTI), but for open cover types, the correlation was greater when focal individuals were TUTI. In hardwood cover, there was no signicant correlation for the focal TUTI, but there was a signicant negative correlation with focal satellite species movement directions (Table 2).

4. Discussion
4.1. Flock Leadership by Titmice Suggests a Passive Nuclear Role. As we predicted, the movement directions of TUTI were clearly more highly correlated with overall ock paths than with the movement directions of satellite species participating in the same ock (Figure 3(a)), supporting our hypothesis that TUTI are followed by satellites in mixedspecies ocks (e.g., TUTI act as a passive nuclear species). This was particularly obvious when ocks were moving fast and moving across boundaries between hardwood and open cover types (Figures 3(a) and 3(c)). When ocks were moving slowly, however, correlations were less consistent in open and boundary cover but were consistent with our predictions in hardwood habitat (Figure 3(b)). Since mean ock movement rates were greater across boundaries than mean ock movement rates in open or forest cover types, perhaps the most parsimonious explanation for the loss of TUTI leadership in slow-moving ocks in open habitat is that vegetative substrate for perching in that cover type was sparser than in the subcanopy of hardwood forests, providing fewer options for an individual to use as a destination perch during ock-following (Figure 2). Even when ocks are stalled in hardwood habitat that is dominated by large, multibranching oaks, each ock participant will be surrounded

International Journal of Zoology

N = 12

0.45 0.3 0.25 0.2 raa 0.15 0.1 0.05 0 All cover Boundary Hardwood Cover types Open N = 233 N = 36 N = 13 N = 113 N = 24 N = 60 N = 29 N = 67 raa 0.35 0.25 0.15 0.05
0.05 0.15

N =7 N = 49 N = 110 N = 29 N = 69 N = 29

All cover

Boundary

Hardwood

N = 13 Open

Cover types
(b) Slow ock movement rate (<30 m/5 minutes)

(a) All ock movement rates

0.4 0.35 0.3 0.25 raa 0.2 0.15 0.1 0.05 0 All cover Nuclear Satellite Boundary Hardwood N = 24 N = 123 N = 17 N = 64 N = 31 N = 61

N = 16 N = 38

Open

Cover types

(c) Fast ock movement rate (>30 m/5 minutes)

Figure 3: Angular-angular correlation coecients (raa ) for correlations between the movement direction of nuclear (TUTI; gray bars) or satellite (white) ock participants and ock movement direction in all cover types combined (All Cover), boundary (boundary between hardwood and open cover), hardwood, and open cover types. The sample size for each coecient is above each bar. (a) Correlation coecients in dierent cover types for all ock movement rates; (b) Correlation coecients in dierent cover types for slow ock movement rates (<30 m/5 minutes); (c) Correlation coecients in dierent cover types for fast ock movement rates (>30 m/5 minutes). Error bars represent 95% condence intervals for each raa . Missing error bars represent 95% condence intervals that were too small to be visible (CI < 0.001).

by high densities of potential perching substrates. Thus, individuals seeking to stay close to TUTI can always move in the direction of a TUTI individual in hardwood forest and have a suitable perch in a preferred location. In an open pine habitat, however, perching and foraging substrate and cover availability will all be much sparser overall. Therefore, if the TUTI are not moving then movements of individuals seeking to stay in the area with TUTI will be inuenced more by feeding or other activities which, if perches are limited, may take them away from TUTI or closer to other satellite species (Figure 3(b)). Indeed, given (a) the dominant assumption that more open habitats convey higher predation risk for small birds in general [9, 34, 38], and (b) that TUTI may be especially targeted by predators attacking ocks (T. A. Contreras and K. E. Sieving, unpublished data, see above),

avoidance of stalled TUTI by ock mates in open habitats may be prudent (Figure 3(b)). However, these variations on our central prediction do not detract from the overall conclusion that when foraging ocks are moving, TUTI movements dene the ock path in all wooded habitats that we studied. The only way that this pattern could reect other than purely passive leadership on the part of the nuclear species is if TUTI were somehow compelling other species to follow or rally around them. Given that titmouse (and other parid) mobbing calls do indeed attract a high variety of species [20, 39], rallying calls directed at heterospecics are quite possible. However, such calls are as yet undocumented despite extensive examination of parid vocal repertoires [40]; their detection was beyond our capabilities in this study.

International Journal of Zoology

Table 2: Angular-Angular correlation coecients (raa ) for correlations between a focal individuals movement direction and the movement direction of responding individuals (within-ock movement) in dierent cover types and for dierent movement distances of focal individuals. N = number of individuals observed. Condence intervals (95% CI) for each raa are reported (L1 , L2 ; see Zar [35]). Condence intervals that do not include 0 indicate a signicant raa (in bold print) at P < 0.05. Overall (All cover types) Flock role raa All focal individuals Nuclear 0.101 Satellite 0.182 Focal individual <15 m Nuclear 0.034 Satellite 0.121 Focal individual >15 m Nuclear 0.207 Satellite 0.339 N 65 45 34 25 31 20 95% CI (L1 , L2 ) 0.097, 0.101 0.181, 0.187 0.024, 0.033 0.116, 0.129 0.201, 0.211 0.339, 0.354 raa
0.072

Boundary N 95% CI (L1 , L2 ) raa

Cover type Hardwood N 29 28 18 19 95% CI (L1 , L2 ) 0.163, 0.174 0.046, 0.062 0.151, 0.179 0.056, 0.074 raa 0.267 0.197
0.243

Open N 20 12 7 5 13 7 95% CI (L1 , L2 ) 0.257, 0.279 0.169, 0.234

0.315, 0.140

0.918
0.094

16 0.101, 0.078 0.170 5 0.880, 0.953 0.049 9 1 7 4

0.070, 0.004

N/A 0.037 0.986

N/A
0.041, 0.087

0.173 0.063
0.025 0.168

0.328

0.140, 0.650 0.369, 0.406 0.070, 0.303

0.983, 0.996

11 0.063, 0.024 0.393 9 0.182, 0.109 0.160

4.2. Within-Flock Movement Patterns May Reect Social Complexity within Flocks. We detected a great variety of patterns with respect to ne-scale movements of satellite and nuclear species (Table 2), and almost no corroboration of our central prediction of high correlations between TUTI movements and subsequent satellite movements. As mentioned above, this could be due to the rapidly shifting and complex social environment within mixed-species ocks that likely dominates participants attention simultaneously with avoiding predators and searching for food. Increasing evidence suggests that while mixed-species foraging ocks may have evolved under selection to avoid predators while enhancing foraging eciency (reviewed in Sridhar et al. [10]), once formed, ocks will host a wide variety of other behaviors that are equally critical to survival and reproduction. Within the permanent bird ocks that are characteristic of tropical forests (canopy, understory, and ant following), the life cycles of ock participants play out within an intensely social environment [4143]. While engaged in facultative winter ocks, temperate forest resident and migrant birds experience a similarly complex social milieu including (in addition to antipredator vigilance and foraging) everything from information gathering [44, 45], mate assessment and status signaling [46], territorial defense [47], courtship [48], to a complex variety of conspecic and heterospecic dominance interactions and competitive conicts over food and feeding sites [4951]. Thus, the nding that ne-scale movements of birds in mixed ocks are not predictable based on a single factor (spatial cohesion with the nuclear species). For example, 3 of the satellite species most frequently observed in ocks (Carolina Chickadee, Ruby-crowned Kinglet, Pine Warbler; Table 1) have foraging behaviors similar to those of TUTI (e.g., lower canopy/shrub foragers or gleaners; De Graaf et al. [52]) and are subordinate to TUTI. Given TUTIs propensity to steal food, it is not surprising that satellite species often move away from TUTI when approached within 5 meters (Table 2). While their aggression, vigilance, and gregariousness make TUTI excellent community informants [19, 53], mob

leaders [9, 20], and nuclear species in foraging ocks [1, 4], these same traits likely reduce their attractiveness at close distances. In our experience with keeping TUTI in aviaries [54], we nd TUTI can be exceptionally aggressive toward unfamiliar individuals in conned spaces. Our data also suggest that satellite species are more willing to tolerate each other at close range than are TUTI (Table 2). The only high correlation between satellite and TUTI movement directions in our analysis occurred when movement distances were greater than 15 m in open cover types. At these distances, we are seeing movements that are more closely related to overall ock movement; the kinds of movements that satellites should be tracking in order to keep up with ocks. Both of our analyses suggest that the nuclear-satellite species relationships and social roles are indeed context dependent [12], inuenced by habitat type (and associated perception of predation risk), habitat structure, ock speed, movement distances made by individuals, and spatial scales over which movements occur (e.g., within vs. between foraging patch and across habitat boundaries). Therefore, our results suggest that within slow-moving ocks, individuals may be responding to the movement of other individuals in the ock and less attention may be paid to nuclear species. Conversely, as ocks move greater distances, and relatively faster through landscapes, TUTI act as ock leaders and passive nuclear species, particularly in cover types that may be perceived as more hostile by forest passerines, for example, open cover types and while crossing forest-open cover type boundaries; see Sieving et al. [9]. Srinivasan et al. [12] suggested that for mixedspecies aggregations, acting as a nuclear species may not be a xed species property, that is, species characteristics that determine species suitability as a nuclear species, or even as ock leaders, may be context dependent. Heterospecic interactions and the roles of mixed-species ock members may change as ocks move through landscapes and dierent cover types. Traits that would make TUTI suitable as ock leaders and nuclear species (e.g., socially dominant/aggressive, generalized habitat use, and high vocal

International Journal of Zoology complexity; [4, 19, 20]) when ocks are moving quickly or moving long distances through potentially dangerous cover types may not make them the preferred attractant (e.g., passive nuclear species) for other ocking species as ocks engage in other activities while ocking.

9 near parids [65]. Thus, attraction of heterospecics to parids occurs across scales, from foraging microhabitat to choice of breeding patch, and it enhances tness-related measures at the level of individuals and alters species distributions within communities. Thus, our work with ocks leads us to concur with current thinking that facilitation is as important (or more so) as competition and predation in shaping selective regimes and species patterns within animal communities [66]. One clear benet that heterospecics gain by being close enough to parids to hear them is the exceptionally highquality information parids produce that precisely and accurately conveys their perception of predation risks and threats [19, 21, 22, 67]. Changes in the types of titmouse calls as they move through the landscape may reect changes in their perception of predation risk [19]. Therefore, it would be benecial for any species that share predators with titmice to be able to interpret and respond appropriately to titmouse calls. Moreover, the number and diversity of species across the Holarctic that utilize parid information to inform their predator-avoidance decisions are apparently very large [20, 53, 68]. Thus, we argue that the facilitative role of parids may best be described as community informants. The use of socially derived information from parids to eectively avoid predators enables heterospecics to achieve greater eciency in other critical activities and provides a largely sucient explanation for heterospecic attraction to parids, both within winter ocks or breeding bird communities [46, 69]. Therefore, we view the most important implication of our work as this: in attempts to conserve declining species that may be receiving important benets from association with parids, consideration should be given to maintaining or strengthening those benets in conservation strategies.

5. Conservation Implications
Our ndings contribute to an expanding base of information suggesting that parids serve as community-level facilitators of (potentially) a great number of heterospecics in diverse taxa. Because parids tend to be very common where they occur, designating them as keystone facilitators is not technically correct (their eect on ock dynamics and community structure is not disproportionate to their abundance; [55]). Moreover, we can eliminate mutualism from our descriptions, because the observed passive leadership of ocks by TUTI further underscores the probable lack of tness benets for TUTI in mixed species ocks. Nonetheless, the facilitative eects of titmice and parids are likely to be pervasive in Holarctic woodland bird communities. Tufted titmice and other parids are habitat generalists, that are able to exploit wood and shrub lands with varied species composition and habitat structures, but species that associate with them are often more specialized in habitat use [56]. Given that spatial behavior can limit the functional connectivity of fragmented and degraded forest landscapes for vertebrates (see Crooks and Sanjayan [57]), nuclear species with broad niches and less sensitivity to changes in physical connectivity may greatly enhance ock movement and increase access to spatially constrained resources for satellites willing to follow them. For example, tufted titmice clearly expand the foraging niches of their winter satellites [7], and they increase the permeability of high contrast habitat boundaries to satellite movement [8, 9, 58]. Thus, following titmice may largely counteract the strong eects of lethal and nonlethal predation threats that constrain movement and access to resources [18, 59] for ock associates. Paridae include a high proportion of nuclear species and/or ock leaders [14] and traits that support the role of nuclear species in mixed ocks are well developed and conserved across the family, including high vocal complexity [19], bold personality [60], and high vigilance [61, 62]. Therefore, across the Holarctic, it is likely that parid-led mixed-species ocks gain similar foraging and habitat exploitation advantages on their winter home ranges. Parid facilitation of other species is not limited to mixed ocks. Heterospecic attraction has been dened as the deliberate selection of breeding territories by migrants that are already populated by resident heterospecics [26, 27]. Heterospecic attraction is strong between parids (as the resident attractor) and migrant forest passerines that breed sympatrically with them (experimental documentation comes from Scandinavian and North American parid species; [24, 60]). The positive benets of using resident parids as cues for settlement are especially pronounced in high latitudes, where short nesting seasons make rapid identication of productive breeding habitat critical for longdistance migrants [63, 64]. Additionally, enhanced reproductive success may accrue to heterospecics from nesting

Acknowledgments
The authors would like to thank Marcela Machicote, Stacia Hetrick, and other members of the K. E. Sieving lab for their comments on the initial design of this study. Two anonymous reviewers provided valuable comments and suggestions on previous drafts of this paper. They thank the Department of Wildlife Ecology and Conservation at the University of Florida for allowing us to work at the Ordway-Swisher Biological Station and also to the Florida Department of Environmental Protection for granting permission to conduct parts of the study at the San Felasco Hammock Preserve and the Paynes Prairie Preserve State Parks. Their study was funded by an NSF Postdoctoral Fellowship to T. A. Contreras (DBI no. 0309753).

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Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 806589, 11 pages doi:10.1155/2011/806589

Research Article Arithmetic-Like Reasoning in Wild Vervet Monkeys: A Demonstration of Cost-Benet Calculation in Foraging
Sayaka Tsutsumi,1, 2 Tomokazu Ushitani,3 and Kazuo Fujita1
1 Department 2 Japan

of Psychology, Graduate School of Letters, Kyoto University, Sakyo, Kyoto 606-8501, Japan Society for the Promotion of Science, Sumitomo-Ichibancho FS Building, 8 Ichibancho, Chiyoda-ku, Tokyo 102-8472, Japan 3 Department of Cognitive and Information Sciences, Faculty of Letters, Chiba University, 1-33 Yayoi-cho, Inage, Chiba 263-8522, Japan Correspondence should be addressed to Sayaka Tsutsumi, sayaka.tsutsumi@gmail.com Received 2 December 2010; Revised 19 April 2011; Accepted 6 May 2011 Academic Editor: Lesley Rogers Copyright 2011 Sayaka Tsutsumi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Arithmetic-like reasoning has been demonstrated in various animals in captive and seminatural environments, but it is unclear whether such competence is practiced in the wild. Using a hypothetical foraging paradigm, we demonstrate that wild vervet monkeys spontaneously adjust their foraging behavior deploying arithmetic-like reasoning. Presented with arithmetic-like problems in articially controlled feeding conditions, all the monkeys tested attempted to retrieve articial prey according to the quantity of the remainder when the task involved one subtraction only (i.e., 21), while one monkey out of four did so when it was sequentially subtracted twice (i.e., 211). This monkey also adjusted his foraging behavior according to the quantity of the reminder for a task requiring stepwise mental manipulation (i.e., (21)1), though the results became less evident. This suggests that vervet monkeys are capable of spontaneously deploying mental manipulations of numerosity for costbenet calculation of foraging but that the extent of such capacity varies among individuals. Dierent foraging strategies might be deployed according to dierent levels of mental manipulation capacity in each individual in a given population. In addition to providing empirical data, the current study provides an easily adaptable eld technique that would allow comparison across taxa and habitat using a uniform method.

1. Introduction
Outstanding numerical competence characterizes human nature as much as language does. In search of the evolutionary origin of such ability, a broad range of nonhuman animals from both the laboratory and semiwild settings have been shown to possess the ability to attend to numerical attributes of the environment (see [1, 2] for review). For example, insects can attend to small number of landmarks that are passed en route (e.g., honeybees [3]), amphibians can discriminate between small number of objects (e.g., salamanders [4]), birds can count, discriminate numerosities, and attend to number (e.g., pigeons [5, 6], parrots [5, 7, 8], corvids [5, 9], and domestic chicks [912]). Mammals can count, discriminate numerosities, and attend to number

(e.g., dolphin [13], raccoon [14], lemurs [15, 16], monkeys [1721], and apes [22, 23]). Spontaneous application of such ability has also been seen in daily survival of wild animals, for example, avoiding brood parasitism in coots [24], assessing feasibility in intergroup contests in lionesses [25] and in chimpanzees [26]; thus, at least in those species there seems to be ecological validity [27] for the ability to represent numerical attributes. Reasoning about those representations, for example arithmetic, requires more complex cognitive processes because it requires two levels of information processing: representation of numerical attributes and mental manipulation of those representations. There exist reports suggesting that birds and mammals might be capable of rudimental arithmetic (i.e., corvids [28], chicks [29], dogs [30], lemurs

2 [31], monkeys [3236], and apes [3742]), though chimpanzees [41] and orangutans [42] seem to have diculties understanding subtraction (review in [1, 2]). Given those evidences from the laboratory and seminatural settings, we would expect them to exploit such abilities in their daily interaction with the environment in the wild. How could such sophisticated competence have evolved had it not been put into practical use? Presumably, to be favoured by natural selection, a cognitive ability should confer adaptive value [43], given the costs of installing requisite neural processes in the brain. However we have not yet seen evidence of arithmetic-like manipulations of such representations in the wild. There even exists an anecdotal report of failed subtraction, in which a bird reacts as if it assumes two persons minus one person = nobody there when two birdwatchers go behind a blind screen and one then departs [44]. This behavior is generally known to birdwatchers and forms the basis of a birdwatching technique. As a transitive attempt to bridge the gap between the documented competence of arithmetic-like reasoning in the captive and seminatural settings and yet-to-be-described application of such ability in the wild, the current study aimed to demonstrate a context in which practicing arithmetic-like reasoning may lead to increased tness in wild animals. In such contexts, natural selection acts directly on the survival of animals, for example, foraging. Consider an insectivore that witnesses two insects go into a hollow up in a tree. One comes out and leaves. The ability to mentally subtract, glossed as two insects minus one insect leaves one, not zero, before deciding whether to climb up the tree or not, would reduce wasteful costs of time and energy, thus leading to increased foraging eciency. This presents an interesting situation where attention to numerical attributes of an object can guide cost-benet calculation of a given behavior. We asked a particular question: do animals spontaneously engage in arithmetic-like reasoning in a situation analogous to the above hypothetical foraging paradigm in their natural habitat? To answer this question, we experimentally set up an articial foraging situation in the native habitat of a group of wild vervet monkeys (Chlorocebus aethiops) in Kenya, and opportunistically tested whether they would spontaneously change their behavior according to the quantity of the articial prey. This paradigm was developed by modifying Hauser et al.s seminatural foraging paradigm [21, 36] in order to measure the response of wild monkeys to controlled feeding conditions in the normal and native home range of their troop. The current paper deals with numerical and quantitative attributes of an object and not number per se (see [12] for discussion on strictly numerical attributes of a stimulus distinguished from the continuous physical variables of the stimulus that covary with number); thus, in this paper we refer to the term subtraction as subtraction-like reasoning rather than strict arithmetic. We aimed to reveal a more compelling picture of how the ability has evolved by coupling approaches that examine how animals benet from arithmetic-like reasoning (=ecological function) [27] with those that examine how numbers are represented by animals (=mechanism).

International Journal of Zoology

2. Methods
2.1. Field Experimental Site. The eld experiment took place in the backyard of the rst authors residence, which happened to be inside the regular home range of a troop of wild vervet monkeys (Kibaki group) inhabiting areas adjacent to Mombasa Marine National Park, Kenya. Vervet monkeys are omnivorous and forage for a variety of food, including fruits, leaves, invertebrates, reptiles, birds, and mammals [45]. As vervets are not shy of humans by nature, they are known to forage in various habitats including human residential areas [4649]; thus, in a sense those articial habitats are natural in the very recent history of evolution (i.e., after farming started and early humans settled with food storage). The rst author resided in the above location for two years prior to the commencement of the current study in March 2002, which provided an opportunity to collect general information regarding the troop, such as daily migration pattern, diet, population size, and individual identication. We set up a testing site on the veranda (4 m width 50 cm depth 90 cm height) of the rst authors residence, which was regularly visited by the monkeys to forage for human food. 2.2. Subjects and Data Sampling Periods. The subjects were adult members of the Kibaki group who spontaneously visited the eld experimental site during the data sampling periods (experiment 1: March 2002 to May 2002, experiment 2-a: July 2004 to August 2004, experiment 2-b: February 2005). All the monkeys tested were identied by clear natural markings such as a torn-o limb, a bent tail, and skin spots. All of them were experimentally nave. 2.3. Apparatus. The apparatus consisted of a face-down opaque cup (5 cm diameter on top, 7 cm diameter on bottom, 8.5 cm height) with a side opening (3.5 cm width, 4 cm height) on the lower side of the wall, and an opaque cardboard box (25 cm, 23 cm, 8 cm: width, depth, height respectively) below the cup (Figure 1(a)). Bread pieces cut in approximately 1 cm3 cubic were used as food stimuli. The cup served as an articial tree, the side opening as an articial hollow, and the bread pieces as articial prey, analogically representing the hypothetical foraging paradigm of Two insects go into a hollow in a tree. One then leaves the hollow. Anything left in the hollow? The opaque cardboard box containing a slice of the same bread served as an olfactory control device. The amount of food stimuli used for a day, typically between 1 to 3 pieces per individual, was small enough not to interfere with their daily natural foraging. 2.4. Procedure 2.4.1. Experiment 1: One-Step Subtraction. Experiment 1 was designed to depict basic requisite components for arithmetic-like reasoning using a simple one-step subtraction task where a quantity is subtracted once (i.e., 11). We placed the apparatus on the windowsill between the veranda and adjoining room and waited for the monkeys to arrive at the testing site (Figure 1(b)). We opportunistically

International Journal of Zoology

3 of the apparatus without using a piece of bread. This baseline condition was to conrm that the monkeys would not approach the cup when there was no food from the beginning. These 6 conditions were presented once each in random order within a session (6 trials in 1 session). The experimental sessions were recorded by a video camera, and another experimenter coded whether the subject monkey approached and moved the cup to collect food within 30 seconds after subtraction (=foraging attempt made) or not. It was obvious whether the monkey approached and moved the cup or not; thus, coding was very simple. A full slice of the same bread used for the session was concealed in the cardboard box to eliminate the possibility of the monkeys making decisions using olfactory cues. Given the risk involved in approaching human properties, the monkeys should approach the cup only when they decide that the benet of acquiring food is greater than the cost of a wasteful inspection of the cup. Therefore, it was predicted that if the monkeys perform arithmetic-like reasoning in this experimental situation, they will be more likely to approach the cup when the remainder is greater than zero (i.e., there is some food left in the cup) than when it is zero (i.e., the cup is empty). This was analogically equivalent to a hypothetical situation where the monkeys make a decision on whether or not to forage by weighing the cost (possibility of losing time and energy) and benet (possibility of foraging success) of a single foraging opportunity. The six conditions were carefully designed to depict each requisite component for arithmetic-like reasoning; in the 11 condition, the monkeys could rst see inside the cup through the opening (Figures 2(a)(1) and 2(a)(2)), but then they could no longer see the contents and had to mentally represent what they sawone piece of breadwhen the opening was rotated back again (Figure 2(a)(3)). Based on this representation, they were now required to mentally manipulate it to solve the subtraction task (Figure 2(a)(4)). In this case, the monkeys could arrive at the correct answer by representing and processing the piece of bread either in the form of object category (i.e., bread bread = nothing), numerosity (i.e., one piece of bread one piece of bread = nothing), or number (i.e., one one = zero). According to Lloyd Morgans canon [50], we should conclude that they are at least mentally manipulating a representation of object category if they solve the task. We refer to this as categorymonitoring subtraction. The same logic applies to the 10, 20, and 22 conditions. In the 21 condition, the monkeys would be required to represent and manipulate what they saw as numerosity (i.e., two pieces of bread one piece of bread = one piece of bread left) or number (i.e., two one = one), but not as object category, because they would fail the task if they thought bread bread = nothing (Figure 2(b), (1)(4)). Thus, we may conclude that they are capable of mentally manipulating a representation of at least numerosity (=numerositymonitoring subtraction) if they attempt to collect the food in the 21 condition more often than in the 22 condition. If their attempt rate in the 21 condition is not dierent

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Figure 1: (a) Apparatus (not to scale). (b) Testing site (not to scale).

tested them once a monkey sat down on the veranda facing the apparatus within 1 meter (for males) or 2 meters (for females) for 5 seconds. We applied dierent distance criteria to males and females because the males were more adventurous and approached closer to the apparatus than the females. The monkeys usually came to the testing site individually, but if two or more monkeys were present, the experiment was not carried out until only one monkey remained. For the test condition 11, a human experimenter stood in the adjoining room about 1m away from the apparatus and showed one piece of bread on his palm to the monkey (Figure 2(a)(1)). He then put it into the cup through an opening and rotated the cup 180 degrees so that the monkey could see and conrm what was in the cup through the opening (Figure 2(a)(2)). After making sure that the monkey looked inside the cup, the experimenter rotated the cup 180 degrees back to the original position (Figure 2(a)(3)) and removed the piece of bread from the opening (Figure 2(a)(4)). Then he walked away from the apparatus, still showing the food on his palm to the monkey, and went out of view into another room 2.5 m away from the veranda. In the control condition 10, the experimenter performed exactly the same sequence of actions except that he imitated movements of removing a piece of bread by reaching into the opening without actually removing the bread and walked away from the apparatus showing his empty palm to the monkey. Similarly, there were 22 (test), 21 (test), and 20 (control) conditions as subtraction from 2, where two pieces of food were handled at once so that the hand movements were identical across conditions. There was also a 00 condition as a baseline where the experimenter made all the same manipulations

International Journal of Zoology

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Figure 2: Subtraction sequences for the 10 (a) and 21 (b) conditions. The upper row shows the actual movement of the cup and bread pieces, and the two lower rows indicate the hypothesized view (1, 2) and representation (3, 4) of bread pieces in the monkeys mind.

from the 22 condition, we should conclude that their operation is category-monitoring subtraction. 2.4.2. Experiment 2: Two-Step Subtraction. Experiment 2 was designed to depict further components of arithmeticlike reasoning using a two-step subtraction task where a quantity is subtracted twice (i.e., (21)1). In one-step subtraction (i.e., 21 condition), the monkeys needed to mentally manipulate the representation of numerosity only once. In two-step subtraction (i.e., (21)1 condition), monkeys were required to mentally manipulate the representation of numerosity twice. For example, to solve the (21)1 task, the monkeys would have to rst represent the results of 21 mental manipulation and then carry out another mental manipulation (i.e., 1) using that representation. We examined two-step subtraction in two ways: simultaneous visibility and successive visibility. Experiment 2-a: Simultaneous Visibility. For experiment 2a, a separate data sampling period was set 2 years after the data sampling period for experiment 1. Applying the same procedure as in experiment 1, we carried out the 000, 200, 210, 201, 211, 220, and 202 conditions (1 session = 7 trials, presented in random order within a session). For example, for the 211 condition, a human experimenter stood in the adjoining room about 1m away from the apparatus and showed two pieces of bread on his palm to the monkey (Figure 3(a)(1)). He then put it into the cup through an opening and rotated the cup 180 degrees so that the monkey could see and conrm what was in the cup through the opening (Figure 3(a)(2)). After making sure that the monkey looked inside the cup, the experimenter rotated the cup 180 degrees back to the original position (Figure 3(a)(3)) and removed one piece of bread from the opening (Figure 3(a)(4)). After conrming that the monkey looked at the removed piece of bread, he removed another

piece of bread from the opening using the other hand, still keeping and showing the previously removed piece of bread on his other palm (Figure 3(a)(5)). Then he walked away from the apparatus, still showing the food on both palms to the monkey and went out of view into another room as in experiment 1. In the control condition 200, the experimenter performed exactly the same sequence of actions except that he imitated movements of removing a piece of bread by reaching into the opening without actually removing the bread and walked away from the apparatus showing his empty palms to the monkey. In these simultaneous visibility conditions, the monkeys could either solve the task by performing the 22 mental manipulation (=one-step subtraction), the 2(1+1) mental manipulation (=two-step subtraction), or the (21)1 mental manipulation (=two-step subtraction). Experiment 2-b: Successive Visibility. For experiment 2-b, another separate data sampling period was set 6 months after the data sampling period for experiment 2-a. Applying the same procedure as in experiment 2-a, we carried out the (00)0, (20)0, (21)0, (20)1, (21)1, (22)0, and (20)2 conditions (1 session = 7 trials, presented in random order within a session). For example, for the (21)1 condition, an experimenter performed exactly the same sequence of actions until the rst piece of bread was removed (Figures 3(b)(1) through 3(b)(4)). After conrming that the monkey looked at the removed piece of bread, he dropped the removed piece into a bucket which was placed in an inaccessible location from the monkeys on the oor and closed the bucket lid by using a foot pedal. He then removed another piece of bread from the opening (Figure 3(b)(5)) and walked away from the apparatus, still showing the food on his palm to the monkey and went out of view into another room as in experiment 1. In the control condition (20)0, the experimenter performed exactly the same sequence of actions except that he imitated movements of removing a piece of bread by reaching

International Journal of Zoology

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Figure 3: Subtraction sequences for the 211 (a) and (21)1 (b) conditions. The upper row shows the actual movement of the cup and bread pieces, and the lower row indicates the hypothesized view (1, 2) and representation (3, 4, 5) of bread pieces in the monkeys mind for each condition.

into the opening without actually removing the bread and also imitated movements of placing a piece of bread into the bucket then walked away from the apparatus showing his empty palm to the monkey. In these successive visibility conditions, the monkeys must solve the task by performing two-step subtraction (i.e., (21)1 mental manipulation) instead of one-step subtraction (i.e., 22 mental manipulation).

3. Results
3.1. Participation. In the current eld experimental paradigm, participation in the experiment depended on the spontaneous choice of the monkeys. During the 2-month data sampling period for experiment 1 (March 2002 to May 2002), four adult monkeys (Mkono: male, Mkia: male, Vidole: male, Mke: female) spontaneously visited the testing site and participated in the experiment. Mkono and Mkia each completed 17 sessions, and Mke completed 12 sessions during the data sampling period. Mke completed fewer sessions because she visited the testing site less frequently. Vidole participated in the experiment much less frequently, completing only 2 sessions. Thus his data were excluded from the analysis. During the 2-month data sampling period for experiment 2-a (July 2004 to August 2004), another four monkeys (Mr. Funny: male, Meno: male, Macho: female, Matiti:

female) spontaneously visited the testing site and participated in the experiment. Mr. Funny completed 20 sessions, Meno completed 17 sessions, and Macho and Matiti each completed 12 sessions during the data sampling period. The four other monkeys who participated in experiment 1 either did not visit the testing site or they did not spontaneously participate in the experiment during the data sampling period for experiment 2. During the 1-month data sampling period for experiment 2-b (February 2005), we targeted only one monkey (Mr. Funny) based on his performance in experiment 2-a. During this period, Mr. Funny completed 16 sessions. 3.2. Reaction to Articial Foraging Situation 3.2.1. Experiment 1: One-Step Subtraction. Typically, the monkeys either inspected the cup within 10 seconds or did not approach the apparatus at all after witnessing the subtraction sequences; thus, the 30-second criterion for the foraging attempt seemed reasonable. All three monkeys made a foraging attempt more often in the 10 condition than in the baseline 00 condition (Fishers exact test; Mokono: P < .0001, Mkia: P < .0001, Mke: P < .0001, Figure 4, all P values are two-tailed in the current paper), meeting the assumption that the monkeys react dierently according to whether there was some food or no food from the beginning.

6
Mkia

International Journal of Zoology

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Figure 4: Foraging attempt rates for one-step subtraction. The foraging attempt rates were expressed as the percentage of attempt made trials over the total number of trials in each condition for each subject. The number of sessions completed was 17 for Mkono and Mkia, and 12 for Mke. : P < .001, : P < .01, : P < .05. P values are two tailed. Fishers exact test was conducted only once between the 21 and 22 conditions for testing dierences among the three conditions: 20, 21, and 22 for Mkono, since the frequencies for the 20 and 21 conditions were identical. The dierence between the 20 and 22 conditions becomes marginally signicant when the threshold is set at 2.5% for multiple comparison for Mkia. The dierence between the 20 and 21 conditions becomes marginally signicant when the threshold is set at 2.5% for multiple comparison for Mke.

In subtraction from 1, all three monkeys made a foraging attempt more often in the 10 condition than in the 11 condition (Fishers exact test; Mokono: P < .0001, Mkia: P = .039, Mke: P = .009), suggesting that they were capable of (1) mentally performing category-monitoring subtraction (i.e., bread bread = nothing) and (2) changing their behavior accordingly when the number of objects represented and manipulated was one. In subtraction from 2, again all three monkeys made a foraging attempt more often in the 20 condition than in the 22 condition (Fishers exact test; Mokono: P = .039, Mkia: P = .044, Mke: P = .005), suggesting that their category-monitoring subtraction extended to a situation where the number of objects represented and manipulated was two. Comparison of the three conditions resulting in no remainders (i.e., 00, 11 and 22 conditions) over the three monkeys as a group revealed that there was a pattern of increasing foraging attempt rates as the number of objects represented and manipulated increased (Friedman 2 = 6.000, D f = 2, P = .05). This could either imply that the monkeys motivation was greater when the number of bread pieces inserted in the cup was greater or the diculty of performing category-monitoring subtraction increased as the number of objects handled at once increased. Comparisons of the 21 condition with the 20 and 22 conditions revealed varying foraging attempt rates among the three monkeys. Mkono approached the 21 cups as often as the 20 cups (Fishers exact test; P = 1.000) but more often than the 22 cups (Fishers exact test; P = .039), indicating that he was (1) mentally

performing at least numerosity-monitoring subtraction (i.e., two pieces of bread one piece of bread = one piece of bread left) and (2) changing his behavior accordingly. Mke approached the 21 cups less often than the 20 cups (Fishers exact test; P = .037) but as often as the 22 cups (Fishers exact test; P = .684), suggesting that she applied category-monitoring subtraction instead of numerositymonitoring subtraction when both types of reasoning are possible. Although the order of attempt rates was the same as the other monkeys, Mkias reaction to the 21 condition did not reveal signicant dierences compared with the 20 and 22 conditions (Fishers exact test; 20 versus 21: P = 1.000, 21 versus 22: P = .175). We have no basis for distinguishing between the two types of reasoning that Mkia might have employed. The correct response rates for the rst session for each monkey were as follows: Mkono: 66.6%, Mkia: 83.3%, and Mke: 83.3% (Figure 5). Group analysis of the correct response rates in the rst and the last 6 sessions for the three monkeys did not reveal signicant dierences (F1,2 = 3.000, P = .225), nor was there any interaction between the order of sessions and conditions (F5,10 = 0.313, P = .894). This implies that the monkeys were less likely to have learned to approach or not in each condition over repeated tests through operant reinforcement. The results therefore appear to reect spontaneous subtraction. 3.2.2. Experiment 2: Two-Step Subtraction Experiment 2-a: Simultaneous Visibility. Comparison of the 200 condition with the 000 condition revealed

22

International Journal of Zoology

Correct response rate (%) 100 80 60 40 20 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Sessions
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7 or the (21)1 mental manipulation (=two-step subtraction) in this case. Mr. Funnys correct response rate for the rst session was 57.1% (Figure 7). The average correct response rates in the rst and the last 6 sessions was the same (71.4%), suggesting that he was less likely to have learned to approach or not in each condition over repeated tests through operant reinforcement. The results therefore appear to reect spontaneous subtraction. Experiment 2-b: Successive Visibility. Comparison of the (20)0 condition with the (00)0 condition for Mr. Funny revealed that he did not meet the baseline assumption for experiment 2-b (Fishers exact test; P = .433, Figure 8); however, comparisons among the test conditions did reveal that he approached the cup equally often when the remainder was two and when the remainder was one but less often when the remainder was zero (Figure 8; Fishers exact test; remainder = two versus remainder = one: P = .386, remainder = one versus remainder = zero: P < .004; N/B: frequencies for (21)0 and (20)1 conditions were summed to form a remainder = one condition, and frequencies for (21)1, (22)0, and (20)2 conditions were summed to form a remainder = zero condition). Mr. Funnys correct response rate for the rst session was 42.9% (Figure 9). The average correct response rate in the rst 6 sessions (57.1%) was not signicantly dierent from the one in the last 6 sessions (66.7%) (t = 1.348, df = 10, P = .207). The fact that the baseline assumption was not met does not allow us to draw any concrete conclusion, but it still stands true that Mr. Funny inspected the cup more often when there was some food left compared with when there was no food left, when the bread pieces were sequentially removed twice and the animal could only see the removed pieces successively, not simultaneously, except for the case where there was no food from the beginning. We could only speculate, but Mr. Funny might indeed have changed his behavior by performing two-step subtraction (i.e., (21)1 mental manipulation) instead of one-step subtraction (i.e., 22 mental manipulation); however, the tendency to inspect the cup might have generally increased for all conditions as the diculty and complexity of the tasks developed from simultaneous visibility task to successive visibility task. In other words, he might be capable of performing two-step subtraction, but he could have gradually changed his foraging strategy from mainly deploying mental manipulation of numerosity to a mixture of mental manipulation and inspection anyway for all conditions. We could further speculate that in a given population of vervet monkeys more individuals are capable of onestep subtraction and they deploy mental manipulation of numerosity as a foraging strategy, while fewer individuals are capable of two-step subtraction and they start to depend more on other strategies as mental manipulation of numerosity becomes less eective. Several factors could be involved in decreased eectiveness in their mental manipulation; for example, a possible failure in attentional mechanisms or in working memory capacity may have contributed

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Figure 5: Correct response rates over sessions for one-step subtraction. The correct response rates were calculated as the percentage of attempt made trials when the remainder was 2 and 1, and attempt not made trials when the remainder was 0, over the total 6 trials for each session for each subject.

that one out of four monkeys met the baseline assumption (Fishers exact test; Mr. Funny: P = .004, Meno: P = .084, Macho: P = 1.000, Matiti, P = 1.000, Figure 6). Further analysis on Mr. Funny revealed that he approached the cup equally often when the remainder was two and when the remainder was one, but less often when the remainder was zero (Figure 6; Fishers exact test; remainder = two versus remainder = one: P = 1.000, remainder = one versus remainder = zero: P < .0001; N/B: frequencies for 210 and 201 conditions were summed to form a remainder = one condition, and frequencies for 211, 220, and 202 conditions were summed to form a remainder = zero condition). This suggests that at least one monkey inspected the cup more often when there was some food left compared with when there was no food left, when the bread pieces were sequentially removed twice and the animal could see the removed pieces simultaneously. He might have either solved the task by performing the 22 mental manipulation (=one-step subtraction), the 2(1+1) mental manipulation (=two-step subtraction),

8
Mr. Funny

International Journal of Zoology

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Figure 6: Foraging attempt rates for simultaneous visibility. The foraging attempt rates were expressed as the percentage of attempt made trials over the total number of trials in each condition for each subject. The number of sessions completed was 20 for Mr. Funny, 17 for Meno, and 12 for Macho and Matiti. : P < .001, : P < .01. P values are two tailed.

to explain Mr. Funnys behavior in experiment 2-b as well as that of the other three monkeys that failed in experiment 2a. Also, from an evolutionary perspective, an inspection could be considered worthy whenever a monkey witnesses repeated (i.e., more than one or two) manipulations even though no food is ever visible (such as in the 000 condition of experiment 2-a and in the (00)0 condition of experiment 2-b). Unlike other conditions, the 000 and (00)0 conditions involve a peculiar behavior of the human experimenter repeatedly manipulating the empty cup and the monkeys might have associated such manipulation to the possible presence of food from the previous experience. In any case, more individuals should be tested in the future to further discuss such speculations, as

the current data involve only a few individuals and the result is interestingly pregnant.

4. Discussion
We asked two major questions in the current study: how animals benet from arithmetic-like reasoning (=ecological function), and how such reasoning is conducted (=mechanism). The results demonstrated that vervet monkeys spontaneously change their foraging behavior according to the quantity of the articial prey in the current experimental setup and that attention to the numerosity of objects guides this behavior in some individuals while other monkeys attend to the category of objects rather than the numerosity.

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Correct response rate (%) 100 80 60 40 20 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Sessions Mr. Funny

9 The increased foraging eciency in the current articial foraging paradigm (i.e., involving a cup, bread pieces, and human experimenter) does not necessarily mean that the monkeys would similarly adjust their foraging behavior in their actual natural foraging scenario (i.e., involving a hollow and insects), nor does it imply that they did so in their evolutionary history. This does not allow us to draw any conclusion about whether foraging is one possible factor for the evolution of arithmetic-like reasoning, but the current study sets a platform for future cross-species comparison. To answer evolutionary questions, we need a cross-comparison of the phylogenic and ecological factors in question (e.g., foraging pattern, social complexity, etc.). We can look for dierences in numerical competence between animals with dierent foraging patterns (i.e., omnivores and carnivores who chase moving objects like insects, birds, mammals, etc. versus herbivores who attend to stable objects like fruits, leaves, etc.). In addition to providing empirical data on one species (i.e., vervets) as a starting point, the current study provids a simple and easily adaptable eld technique that would allow comparison across taxa and habitat using a uniform method. Phylogenically, vervets are Old World monkeys (Family Cercopithecidae) whose foraging pattern includes mobile objects (i.e., invertebrates) [45]. Using a comparable seminatural foraging paradigm, it has been shown that the phylogenically and dietarily similar rhesus macaque is capable of rudimentary subtraction in seminatural settings [36]. The dietary similarities extend to foraging in human residential areas [51]. In addition to this wellmatched cross-species comparison, phylogenically similar but dietarily dierent species can be compared, like the leaf monkey, the most folivorous of Old World monkeys. Concerning mechanisms, the current study demonstrated that at least some vervets spontaneously engage in mental manipulation of numerosity and that numerosity can mentally be manipulated at least once and potentially twice. The fact there was no extensive training suggests that the ability already existed in the wild. Various models have been proposed for the mechanisms of numerical representation in nonverbal and preverbal mind, including the widely discussed object le model [52] and accumulator model [53], and empirical evidence exists in support of both models as discussed in [36]. In either of the two models it is possible to perform simple arithmetic (i.e., addition, subtraction, multiplication, and division) as long as it involves the rst three or four numerosities [36], so the focus of our research was how arithmetic-like reasoning is put into practice in a cost-benet decision-making situation by referring to more general mechanisms. By considering the elemental distinction between a category and particular instances of a category, we found that monkeys use both categorymonitoring and numerosity-monitoring mechanisms for responding to subtraction-like manipulations of objects and that such cognitive processes aect their cost-benet decision making. We cannot rule out a possibility that the monkeys used estimates of continuous physical variables (e.g., volume, area, perimeter, etc.) for their arithmetic-like reasoning. However the size of bread pieces was not strictly identical, and each piece had a slightly dierent area, perimeter,

Figure 7: Correct response rates over sessions for simultaneous visibility. The correct response rates were calculated as the percentage of attempt made trials when the remainder was 2 and 1, and attempt not made trials when the remainder was 0, over the total 7 trials for each session.
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Figure 8: Foraging attempt rates for successive visibility. The foraging attempt rates were expressed as the percentage of attempt made trials over the total number of trials in each condition. The number of sessions completed was 16. : P < .01. P values are two tailed.
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Correct response rate (%)

Sessions

Figure 9: Correct response rates over sessions for successive visibility. The correct response rates were calculated as the percentage of attempt made trials when the remainder was 2 and 1, and attempt not made trials when the remainder was 0, over the total 7 trials for each session.

202

10 shape, and so forth. While acknowledging that the data only represent instances of magnitude estimation (of which numerosity is just an example), it would be cognitively economical to attend to an overall numerical attribute of an object (i.e., numerosity) rather than to varying physical variables when subtraction-like manipulation is mentally performed. This seems to be in line with the case with other species; for example, lemurs [15] and rhesus monkeys [18] are known to spontaneously attend to numerical attributes when information on both numerosity and other physical variables is available, and in chicks the identication of objects as dierent and separate individuals is crucial for the computation of number rather than continuous extent [12]. This also seems to be in line with the fact that each prey has dierent physical features in the actual environment; if foraging did play a role in the evolution of subtraction-like reasoning then such cognitive ability should be applicable to, and functional in, the actual foraging situation. While we leave a distinction between magnitude estimation and strict numerosity to further controlled research, we attach importance of the current data to a demonstration of spontaneous arithmetic-like reasoning in a wild population of monkeys. It is also interesting to note that at least one monkey responded to both one-step and two-step subtractions according to the numerosity of the remainder but that his performance for two-step subtraction became undistinguishable from the baseline (00)0 condition. The overall eectiveness for his two-step subtraction seems to have decreased compared to one-step subtraction. While acknowledging that sequential steps involved in subtraction manipulations are not immediately comparable to the rst-order and second-order representation of social events (i.e., theory of mind, [54]), it is worth noting that in this domain of quantitative cognition the monkeys also showed varying responses towards dierent number of steps.

International Journal of Zoology

[2] E. M. Brannon and J. F. Cantlon, A comparative perspective on the origin of numerical thinking, in Cognitive Biology: Evolutionary and Developmental Perspectives on Mind, Brain, and Behavior, L. Tommasi, M. A. Peterson, and L. Nadel, Eds., pp. 191220, MIT Press, Cambridge, Mass, USA, 2009. [3] M. Dacke and M. V. Srinivasan, Evidence for counting in insects, Animal Cognition, vol. 11, no. 4, pp. 683689, 2008. [4] C. Uller, R. Jaeger, G. Guidry, and C. Martin, Salamanders (Plethodon cinereus) go for more: rudiments of number in an amphibian, Animal Cognition, vol. 6, no. 2, pp. 105112, 2003. [5] O. Koehler, Vom Erlernen unbenannter Anzahlen bei V geln, Die Naturwissenschaften, vol. 29, pp. 201218, 1941, o cited in: J. Emmerton, Birds judgments of number and quantity, in R. G. Cook, Ed., Avian Visual Cognition, 2001, http://www.pigeon.psy.tufts.edu/avc/emmerton/default.htm. [6] S. Hirai and M. Jitsumori, Counting absolute numbers of items, from 1 to 8, in pigeons, Learning and Behavior, vol. 37, no. 4, pp. 365379, 2009. [7] I. M. Pepperberg, Numerical competence in an African gray parrot (Psittacus erithacus), Journal of Comparative Psychology, vol. 108, no. 1, pp. 3644, 1994. [8] I. M. Pepperberg and J. D. Gordon, Number comprehension by a Grey parrot (Psittacus erithacus), including a zero-like concept, Journal of Comparative Psychology, vol. 119, no. 2, pp. 197209, 2005. [9] R. Rugani, D. M. Kelly, I. Szelest, L. Regolin, and G. Vallortigara, Is it only humans that count from left to right? Biology Letters, vol. 6, no. 3, pp. 290292, 2010. [10] R. Rugani, L. Regolin, and G. Vallortigara, Rudimental numerical competence in 5-day-old domestic chicks (Gallus gallus): identication of ordinal position, Journal of Experimental Psychology, Animal Behavior Processes, vol. 33, no. 1, pp. 2131, 2007. [11] R. Rugani, L. Regolin, and G. Vallortigara, Discrimination of small numerosities in young chicks, Journal of Experimental Psychology, Animal Behavior Processes, vol. 34, no. 3, pp. 388 399, 2008. [12] R. Rugani, L. Regolin, and G. Vallortigara, Imprinted numbers: newborn chicks sensitivity to number vs. continuous extent of objects they have been reared with, Developmental Science, vol. 13, no. 5, pp. 790797, 2010. [13] R. W. Mitchell, P. T. Sherman, and M. ORegan, Discriminative responding of a dolphin (Tursiops truncatus) to dierentially rewarded stimuli, Journal of Comparative Psychology, vol. 99, pp. 218225, 1985. [14] H. Davis, Discrimination of the number three by a raccoon (Procyon lotor), Animal Learning and Behavior, vol. 12, no. 4, pp. 409413, 1984. [15] K. P. Lewis, S. Jae, and E. M. Brannon, Analog number representations in mongoose lemurs (Eulemur mongoz): evidence from a search task, Animal Cognition, vol. 8, no. 4, pp. 247 252, 2005. [16] D. J. Merritt, E. L. Maclean, J. C. Crawford, and E. M. Brannon, Numerical rule-learning in ring-tailed lemurs (Lemur catta), Frontiers in Psychology, vol. 2, no. 23, 2011. [17] E. M. Brannon and H. S. Terrace, Ordering of the numerosities 1 to 9 by monkeys, Science, vol. 282, no. 5389, pp. 746 749, 1998. [18] J. F. Cantlon and E. M. Brannon, How much does number matter to a monkey (Macaca mulatta)? Journal of Experimental Psychology, Animal Behavior Processes, vol. 33, no. 1, pp. 32 41, 2007.

Acknowledgments
The authors thank Dr. J. R. Anderson, Dr. Kang Lee, and anonymous reviewers for providing useful comments. For assistance during data collection, we thank Kenya Wildlife Services, Institute of Primate Research, Dr. J. M. Mwenda, Dr. D. O. Obura, and Mr. B. Ogwoka. Fieldwork was conducted under Kenyan research permit no. MOEST 13/220. This study was supported by the Japan Society for the Promotion of Science (JSPS) Research Fellowship for Young Scientists to S. Tsutsumi, the JSPS Grant-in-Aid for Scientic Research Nos. 17300085 and 20220004 to K. Fujita, and by the 21st Century COE Program D-10 from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan, to Kyoto University.

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International Journal of Zoology

[19] B. R. Smith, A. K. Piel, and D. K. Candland, Numerity of a socially-housed hamadyras baboon (Papio hamadryas) and a socially housed squirrel monkey (Saimiri sciureus), Journal of Comparative Psychology, vol. 117, no. 2, pp. 217225, 2003. [20] M. D. Hauser, F. Tsao, P. Garcia, and E. S. Spelke, Evolutionary foundations of number: spontaneous representation of numerical magnitudes by cotton-top tamarins, Proceedings of the Royal Society B, vol. 270, no. 1523, pp. 14411446, 2003. [21] M. D. Hauser, S. Carey, and L. B. Hauser, Spontaneous number representation in semi-free-ranging rhesus monkeys, Proceedings of the Royal Society B, vol. 267, no. 1445, pp. 829833, 2000. [22] T. Matsuzawa, Use of numbers by a chimpanzee, Nature, vol. 315, no. 6014, pp. 5759, 1985. [23] S. T. Boysen, G. G. Berntson, M. B. Hannan, and J. T. Cacioppo, Quantity-based interference and symbolic representations in chimpanzees (Pan troglodytes), Journal of Experimental Psychology, Animal Behavior Processes, vol. 22, no. 1, pp. 7686, 1996. [24] B. E. Lyon, Egg recognition and counting reduce costs of avian conspecic brood parasitism, Nature, vol. 422, no. 6931, pp. 495499, 2003. [25] K. McComb, C. Packer, and A. Pusey, Roaring and numerical assessment in contests between groups of female lions, Panthera leo, Animal Behaviour, vol. 47, no. 2, pp. 379387, 1994. [26] M. L. Wilson, M. D. Hauser, and R. W. Wrangham, Does participation in intergroup conict depend on numerical assessment, range location, or rank for wild chimpanzees? Animal Behaviour, vol. 61, no. 6, pp. 12031216, 2001. [27] D. L. Cheney and R. M. Seyfarth, How Monkeys See the World, The University of Chicago Press, Chicago, Ill, USA, 1990. [28] A. A. Smirnova, O. F. Lazareva, and Z. A. Zorina, Prototype symbolization in hooded crows, Neuroscience and Behavioral Physiology, vol. 33, no. 4, pp. 335348, 2003. [29] R. Rugani, L. Fontanari, E. Simoni, L. Regolin, and G. Vallortigara, Arithmetic in newborn chicks, Proceedings of the Royal Society B, vol. 276, no. 1666, pp. 24512460, 2009. [30] R. E. West and R. J. Young, Do domestic dogs show any evidence of being able to count? Animal Cognition, vol. 5, no. 3, pp. 183186, 2002. [31] L. R. Santos, J. L. Barnes, and N. Mahajan, Expectations about numerical events in four lemur species (Eulemur fulvus, Eulemur mongoz, Lemur catta and Varecia rubra), Animal Cognition, vol. 8, no. 4, pp. 253262, 2005. [32] A. Olthof, C. M. Iden, and W. A. Roberts, Judgments of ordinality and summation of number symbols by squirrel monkeys (Saimiri sciureus), Journal of Experimental Psychology, Animal Behavior Processes, vol. 23, no. 3, pp. 325339, 1997. [33] J. F. Cantlon and E. M. Brannon, Basic math in monkeys and college students, PLoS Biology, vol. 5, no. 12, pp. 29122919, 2007. [34] M. D. Hauser, P. Macneilage, and M. Ware, Numerical representations in primates (concepts/arithmetical abilities/ comparative methods), Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 4, pp. 15141517, 1996. [35] M. D. Hauser and S. Carey, Spontaneous representations of small numbers of objects by rhesus macaques: examinations of content and format, Cognitive Psychology, vol. 47, no. 4, pp. 367401, 2003.

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[36] G. M. Sulkowski and M. D. Hauser, Can rhesus monkeys spontaneously subtract? Cognition, vol. 79, no. 3, pp. 239 262, 2001. [37] D. M. Rumbaugh, S. Savage-Rumbaugh, and M. T. Hegel, Summation in the Chimpanzee (Pan troglodytes), Journal of Experimental Psychology, Animal Behavior Processes, vol. 13, no. 2, pp. 107115, 1987. [38] S. T. Boysen and G. G. Berntson, Numerical competence in a chimpanzee (Pan troglodytes), Journal of Comparative Psychology, vol. 103, no. 1, pp. 2331, 1989. [39] M. J. Beran, Summation and numerousness judgments of sequentially presented sets of items by chimpanzees (Pan troglodytes), Journal of Comparative Psychology, vol. 115, no. 2, pp. 181191, 2001. [40] M. J. Beran and M. M. Beran, Chimpanzees remember the results of one-by-one addition of food items to sets over extended time periods, Psychological Science, vol. 15, no. 2, pp. 9499, 2004. [41] M. J. Beran, Chimpanzees (Pan troglodytes) respond to nonvisible sets after one-by-one addition and removal of items, Journal of Comparative Psychology, vol. 118, no. 1, pp. 2536, 2004. [42] J. Call, Estimating and operating on discrete quantities in orangutans (Pongo pygmaeus), Journal of Comparative Psychology, vol. 114, no. 2, pp. 136147, 2000. [43] C. Darwin, On the Origin of Species by means of Natural Selection, John Murray, London, UK, 1859. [44] M. D. Hauser, What do animals think about numbers? American Scientist, vol. 88, no. 2, pp. 144151, 2002. [45] T. M. Butynski, Vertebrate predation by primates: a review of hunting patterns and prey, Journal of Human Evolution, vol. 11, no. 5, pp. 421430, 1982. [46] J. H. Wolfheim, Ed., Primates of the World: Distribution, Abundance, and Conservation, University of Washington Press, Seattle, Wash, USA, 1983. [47] D. Eley and J. G. Else, Primate pest problems in Kenya hotels and lodges, International Journal of Primatology, vol. 5, no. 4, p. 334, 1984. [48] E. J. Brennan, J. G. Else, and J. Altmann, Ecology and behaviour of a pest primate: Vervet monkeys in a tourist-lodge habitat, African Journal of Ecology, vol. 23, no. 1, pp. 3544, 1985. [49] T. L. Saj, P. Sicotte, and J. D. Paterson, The conict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda, African Journal of Ecology, vol. 39, no. 2, pp. 195 199, 2001. [50] C. L. Morgan, An Introduction to Comparative Psychology, Arnold, London, UK, 1894. [51] A. C. Ciani, Intertroop agonistic behavior of a feral rhesus macaque troop ranging in town and forest areas in India, Aggressive Behavior, vol. 12, no. 6, pp. 433439, 1986. [52] D. Kahneman, A. Treisman, and B. J. Gibbs, The reviewing of object les: object-specic integration of information, Cognitive Psychology, vol. 24, no. 2, pp. 175219, 1992. [53] W. H. Meck and R. M. Church, A mode control model of counting and timing processes, Journal of Experimental Psychology, Animal Behavior Processes, vol. 9, no. 3, pp. 320 334, 1983. [54] D. Premack and G. Woodru, Does the chimpanzee have a theory of mind? Behavioral and Brain Sciences, vol. 1, no. 4, pp. 515526, 1978.

Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 967274, 10 pages doi:10.1155/2011/967274

Research Article Figs Are More Than Fallback Foods: The Relationship between Ficus and Cebus in a Tropical Dry Forest
Nigel A. Parr, Amanda D. Melin, and Linda Marie Fedigan
Department of Anthropology, University of Calgary, 2500 University Drive NW Calgary, AB, Canada T2N 1N4 Correspondence should be addressed to Nigel A. Parr, nparr@ucalgary.ca Received 1 January 2011; Revised 4 April 2011; Accepted 29 July 2011 Academic Editor: Michael Thompson Copyright 2011 Nigel A. Parr et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In many studies on primate feeding ecology, gs (Ficus spp.) are characterized as fallback foods, utilized only when preferred sources of food are unavailable. However, for white-faced capuchin monkeys (Cebus capucinus) living in northwestern Costa Rica, gs are a consistently important resource and may increase groupwide energy intake. We investigated whether visits to gs aect ranging and behavioural patterns of capuchins. Although daily range length and average travel speed do not dier on days when g trees are visited, capuchins spend more time in directed travel and more time stationary on g days. Capuchins also increase time spent foraging for fruit and decrease time spent foraging for invertebrates on days when gs trees are visited. Capuchins experience higher energy intake and lower energy output on g days. Thus, the patterns of foraging for gs support an energy-maximization strategy and constitute an important nutritional resource for capuchins.

1. Introduction
Fig syconia (hereafter referred to as gs or g fruits) produced by Ficus trees are important resources for a plethora of tropical mammal, bird, reptile, and invertebrate species [1, 2]. Many of these animals are in turn important to g trees, acting as seed dispersers. Three major types of g-eating frugivores have been identied: birds, bats, and arboreal mammals. The evolution of the physical characteristics of dierent g species is linked to particular types of seed dispersers [3]. Bat-dispersed gs tend to be larger, cryptically coloured (greenish), and highly odorous while birddispersed gs are small, conspicuously coloured (reddish), and less odorous [3, 4]. There is no specic g dispersal syndrome that is linked with all arboreal mammals, but there is signicant overlap in the g species consumed by monkeys and birds [2]. Many Neotropical primates, including capuchins, have trichromatic vision and, like birds, are attracted to conspicuously coloured gs [5]. Figs are often described as fallback foods for tropical primates, eaten only when preferred foods are unavailable [6], or not eaten at all [7]. Rarely are gs described as consistent or preferred food items for primates (but see [8, 9]).

However, the characterization of gs as fallback foods has been strongly inuenced by feeding studies of gibbons and orangutans [1012] and may not be ubiquitous across the order Primates. In particular, there is evidence that g fruits are both a consistent and preferred resource for many New World primates (Valenta and Melin, in review). Neotropical monkeys are frequent consumers of gs [6, 8, 9, 1316] and are likely candidates as seed dispersers thereof. Ecologists propose that nutritional needs explain food preferences and selection, including energy- and proteinmaximization and the avoidance of plant secondary metabolites (PSMs; [17]). Figs are palatable, easily digested, contain few PSMs, and exhibit protein contents that are high enough to inuence food selectivity in some Neotropical primates [1, 18]. Published nutritional data for Ficus fruits are highly variable, depending on the g species analyzed and whether or not g seeds were removed prior to analysis [1924]. Proper assessment of nutritional uptake for a given fruit requires not only data on the nutritional content of single fruits, but information on the fruit intake rate as well. Figs eaten by capuchins and howler monkeys are most often small and conspicuously coloured and are consumed at higher rates than other fruits [8, 25].

2 Energy maximization is a key concept in optimal foraging theory [26, 27], which proposes that animals will maximize their net energy uptake during foraging and feeding behaviour [17]. Thus, according to optimal foraging theory, animals should travel to the next food patch at the most energy-ecient pace when the food energy available in their current patch is below a threshold level, and they should stop moving to feed when the available energy rises above this threshold [28]. Therefore, in food patches with high energy yields primates should feed more and move less [29]. While optimal foraging and patch depletion theories describe net energy maximization in regards to food acquisition, they do not predict behaviours after animals have become satiated, which likely occurs in very large fruit patches. If food acquisition is a primary motivation for primate movement, a higher proportion of stationary behaviours, such as resting and socializing, would be expected after satiation at large fruit patches. For example, primates in a Peruvian national park rested more and traveled less when seasonal fruit availability was highest [6]. Because g trees produce extremely large fruit crops, fruit availability in g trees can be high even if habitat-wide fruit availability is low. Therefore, we should expect more rest and less travel when primates visit g trees. An increase in resting or stationary behaviours should be reected in short-term ranging measures such as day range length. An abundance of food may allow primates to relax their search eorts, leading to shorter day range lengths or an overall reduction in the amount of time dedicated to foraging movements [30, 31]. Additionally, the energy available in easily acquired, abundant foods may permit primates to expend extra energy on movement, such as increasing travel speeds between food patches. Our objective is to combine data from previous studies of capuchin nutritional ecology [19, 21] with new data on ranging behaviour, foraging rates, duration of visits to fruit trees, monkey carrying capacities of fruit trees, and activity budgets to achieve a multifactor assessment of the relationship between capuchin monkeys and Ficus trees in Sector Santa Rosa, Costa Rica. We test the hypothesis that if Ficus trees provide a uniquely rich resource, in terms of energy gain per minute for all group members, then capuchins will alter their ranging and foraging behaviours in a way that that is more energy optimal on the days that they feed from g trees (g days) than on days that g trees are not visited.

International Journal of Zoology characterized by high ambient temperatures, strong winds, little to no rainfall, and the defoliation of many nonriparian trees [33]. Most of the natural water sources in the area dry up towards the end of the dry season. The wet season occurs from the second half of May through November, with the majority of the 1500 mm of annual rainfall occurring during September and October. A short but relatively drier period (the veranito) occurs between mid-July and mid-August, dividing the early and late wet seasons [34], a pattern that is typical of tropical forests at this latitude [35]. 2.2. Subjects. Capuchin monkeys are frugivore-insectivores and live in matrilineal social groups [36]. We studied the movement and foraging behaviours of one small group (EX: 811 individuals), two medium-sized groups (LV: 20 23; CP: 2426), and one large group (GN: 3335) of free-ranging white-faced capuchins (Cebus capucinus) for 22 months (January through April 2007, September 2007 through January 2008, May through August 2008, January through August 2009). All groups were habituated to human presence, and two have been studied intensively for over 20 years (e.g., [37, 38]). Each group was followed, on average, for three consecutive days each month. 2.3. Data Collection 2.3.1. Energy Acquisition. We recorded a fruit patch visit (FPV) whenever we observed a monkey to enter a new fruit source. For each FPV, we recorded the plant species, GPS location, trunk circumference at breast height (CBH) and, whenever possible, the carrying capacity of the patch (maximum number of monkeys simultaneously feeding) and the duration of the FPV (time elapsed from entry of the rst monkey until the exit of the last monkey). We designated all days that included at least one FPV in a Ficus tree as a g day. To calculate invertebrate capture rates, we collected behavioural data using 10-minute continuous focal animal samples [39] of all adult, subadult, and large juvenile capuchins in each of the four study groups. We recorded behaviour states and foraging events whenever they occurred and attempted to identify all consumed insects. Insect capture rates were calculated by dividing the number of captures for each insect, or set of insects, by the total time spent in the visually foraging state (scanning nearby substrates; [40]). We used previously published nutritional data for insects consumed by capuchins [19] to calculate nutrient uptake from insect foraging. We conducted 1- to 5-minute continuous focal animal samples [39] of all independently foraging group members (i.e., not infants) to record feeding events when we observed them feeding in fruit trees. The durations of the focal samples were dependent on visibility. We counted a feeding event whenever the focal animal swallowed a fruit whole or took at least two bites from it. The total number of individual fruits ingested was divided by the total duration of the foraging state to calculate the feeding rate for each fruit tree species. We reviewed the literature to obtain nutritional data for Ficus species and found great variation in the results.

2. Materials and Methods

2.1. Study Site. This study took place in the Santa Rosa Sector (SSR) of the 153,000-hectare Area de Conservacion Guanacaste (ACG), in Guanacaste province, Costa Rica. SSR is approximately 108 km2 of evergreen and semideciduous tropical dry forest with a highly seasonal climate [32]. Sections of the forest were cleared for cattle pasture over the past 300 years and currently exhibit various stages of regeneration following the establishment of Santa Rosa as a national park in 1971. The area experiences an intense dry season from mid-December to mid-May, which is

International Journal of Zoology While capuchins likely chew and digest some seeds, they are predominantly gentle g eaters, squeezing the pulp and juice out of gs and rarely masticating the seeds [41]. Therefore, we decided that Jordanos [24] nutritional data for gs are most applicable to our study because Jordano did not include the nutritional value of seeds and also because his study took place in Sector Santa Rosa, as did ours. We obtained nutritional data for other fruits consumed by capuchins from the published literature as well [19, 21, 22] to compare with gs. To calculate the energy uptake rate (KJ/minute) for each fruit species, we multiplied the feeding rate (fruits/minute) by the energy content (KJ/fruit). We only calculated energy uptake rates for 31 fruit species with available nutritional data (Table 1). We have additional feeding rates, FPV durations and carrying capacities for another 45 plant species. 2.3.2. Ranging Data. We used Garmin GPSMAP 76Cx handheld GPS units to record group locations on the hour and half hour throughout the day (N = approx. 25 per day), and at the sleep sites in the morning and evening. Best eorts were made to record the location of the centre of the group. Analysis for this study only included data from full-day follows of monkey groups (N = 186), when we were with the group from their wake site in the morning to their sleep tree in the evening. We sampled evenly between the dry (N = 90) and wet (N = 96) seasons. Day range lengths were calculated using Garmin MapSource software (Garmin, USA) by summing the vector distances between consecutive location points over the course of the day. We measured stationary time daily by counting the number of half-hour intervals in which the travel distance was less than 10 metres. Travel speed was calculated by dividing the average distance traveled for each half-hour interval by the length of the interval (30 minutes). For each day, we averaged travel speed by summing the travel speeds for each interval and dividing by the number of intervals. Travel speed calculations only included intervals where the distance traveled was 10 metres. Any travel distance <10 metres was considered to be stationary. This distance was chosen as the cut-o point because it was the maximum error range (+/10 m) of the GPS unit, and it allowed to us to account for the fact that the monkeys could be spread out within the crown of especially large fruit trees that could reach 10 metres in diameter. 2.3.3. Activity Budgets. Every half hour we conducted group scan samples and assigned a behaviour class to each monkey we could locate within 10 minutes. We calculated daily activity budgets as the proportion of scans devoted to each behaviour class (Table 2). 2.4. Statistical Analyses. We used general (GLM), and generalized linear mixed models (GLMM) to test the eect of g day on the ranging parameters: day range length (GLM), travel speed (GLM) and stationary time (GLMM; negative binomial distribution). To analyze the group scan data relating to activity budgets, we classied and subclassied

3 each variable (Table 2). We rst compared foraging to nonforaging behaviours and then compared the types of behaviours to the others within each of these larger classications (i.e., fruit foraging behaviours to the remaining foraging behaviours.) To maintain adequate sampling, we removed days from the analysis if they had <10 scans in the category of interest. We included group size (small, medium, large) and season (wet, dry) as covariates in all analyses, as these variables aect ranging patterns and activity budgets of capuchins in Sector Santa Rosa. For all statistical models, signicance was set at P < 0.05. All statistical analyses for this study were performed using SAS software, Version 9.1.3 (SAS Institute Inc., Cary, NC).

3. Results
We observed the capuchins eating the fruits of 117 plant species including eight dierent g species: Ficus bullenii, F. citrifolia, F. cotinifolia, F. goldmani, F. hondurensis, F. morazaniana, F. obtusifolia, and F. ovalis. Four of these g species (F. citrifolia, F. cotinifolia, F. hondurensis, F. ovalis) are conspicuous, while the other four species have crypticallycoloured fruits characteristic of bat dispersal. Among the conspicuous Ficus species, F. citrifolia is rare in SSR; to date we have recorded only two trees in the monkeys home ranges. Thus, data on this g species should be interpreted with caution, as the sample size is low for all our measures. 88% of capuchin g foraging time was dedicated to the four conspicuous gs. One g species in particular, Ficus cotinifolia, was consumed approximately three times more often than any of the other conspicuous gs. As F. cotinifolia fruits are similar in size and colour to other conspicuous gs, and this species is the only conspicuous g in SSR for which nutritional data have been published, we use this species as a representative of all conspicuous g species in our discussion. 3.1. Energy Obtained for Foraging Visits to Figs. Fig trees in SSR fruit both asynchronously and aseasonally (Fedigan, unpub. data). Hence, we observed the consumption of gs by capuchins during every month of the year. Fig trees in SSR had the largest carrying capacities of any species (Table 1). The single highest maximum carrying capacity recorded during our study was for the entire CP group (26 monkeys) cofeeding in a single Ficus ovalis tree. Four of the ve maximum carrying capacities belonged to Ficus species, with several other Ficus species ranking closely behind. Ficus species also had among the highest average carrying capacities, nearly lling the top 10 spots. Along with large carrying capacities, Ficus trees also had the longest FPV durations recorded. One visit to a F. cotinifolia resulted in four hours of continuous foraging as group members took turns feeding. Ficus species occupied the top three spots for FPV duration, as well as the 7th spot. Of the 76 fruit tree species for which we could calculate feeding rates, the conspicuous Ficus hondurensis, F. cotinifolia, F. ovalis, and F. citrifolia ranked 5th, 7th, 10th, and 23rd, respectively. The feeding rate for F. citrifolia is likely an underestimate, not only because our sample size for this

Table 1: Fruit patch data, nutritional information, feeding rates, and nutrient intake rates for 31 fruit species consumed by Cebus capucinus at Sector Santa Rosa, ACG, Costa Rica. FPV = fruit patch visit. Carrying capacity Maximum Mean Intake Rate (fruits/min) 3.3 0.5 12.3 7.9 7.1 5.0 24.8 0.082 6.778 7.1898.826 0.7 13.3 5.330 4.878 0.036 0.333 0.038 0.017 4.3 6.7 22.1 9.4 5.3 6.2 10.3 4 8 5 11 16 4 7 4 6 4 5 2 9 2.0 95 1.1 3 1.8 28 6.7 2.4 22 7.4 2.0 40 8.0 1.6 7 2.9 5.870 0.159 1.4 8 1.6 6.305 1.5 44 7.1 0.2390.611 0.004 4.7 142 29.3 1.545 2.0 52 7.1 0.4313.710 0.015 2.4 33 9.8 14.574 2.5 64 10.7 1.2311.331 0.006 1.3 28 3.1 189.779 11.623 FPV duration (min.) Maximum Mean Nutrition (fruit1 ) Energy (KJ) Protein (g) Nutritional intake (min1 ) Energy (KJ) Protein (g) 37.811 103.986 15.16516.408 115.233 3.09426.511 7.792 5.87415.152 27.214 39.130 3.521 63.635 38.05046.725 33.285 50.112 0.074 0.107 0.099 0.354 0.338 1.763 0.237 0.175

Avg. DBH 28.3 12.7 57.0 26.9 35.2 92.7 6.1 4.2 11.0 12.7 14.2 29.9 5.5 27.9

Tree information Family Tree species Spondias Anacardiaceae purpurea2 Stemmadenia Apocynaceae obovate2 Sciadodendron Araliaceae excelsum1,2 Tabebuia Bignoniaceae ochracea2 Bursera Burseraceae simaruba1,2 Sloanea Elaeocarpaceae ternifolia2 Erythroxylum Erythroxylaceae havenense1,2 Vachellia Fabaceae collinsii1 Casearia Flacourtiaceae arguta2 Casearia sylvestris2 Bunchosia Malpighiaceae ocellata1 Byrsonima crassifolia1,2 Malvaviscus Malvaceae arboreus1 Trichilia Meliaceae martiana1

International Journal of Zoology

Table 1: Continued. Carrying capacity Maximum Mean 7 3.7 Intake Rate (fruits/min) 3.9 7.8 14.5 5.3 16.2 3.9 2.6 12.5 1.3 12.0 0.131 1.359 18.093 1.6763.474 5.9 1.8 1.111 5.448 0.268 0.038 0.035 1.6 0.5 10.4 0.9 4.5 4.2 2.3 15 12 11 13 8 26 8 10 5 7 7 7 8 4 2 1.2 6 1.8 17 2.5 57 13.2 1.9 44 7.0 2.4 17 6.0 1.8 38 4.4 27.96460.462 1.437 1.2 7 1.7 16.801 2.9 91 12.7 0.695 0.010 1.8 28 6.2 14.302 0.254 5.5 117 27.3 3.2 41 11.5 0.128 5.9 177 42.9 5.6 222 46.1 5.7 18 10 5.4 273 46.5 2.261 0.007 33.687 18.593 8.345 26.830 13.98230.231 14.988 17.090 7.53515.621 4.678 12.259 FPV duration (min.) Maximum Mean 12 8.0 Nutrition (fruit1 ) Energy (KJ) Protein (g) 0.098 Nutritional intake (min1 ) Energy (KJ) Protein (g) 0.384 0.104 0.334 0.330 0.120 0.209 0.680 0.253 0.171 0.147

International Journal of Zoology

Family

Avg. DBH 102.4 19.3

129.3 89.1 86.0

120.2 84.2

113.4 12.1 43.6 6.2 20.8 29.9 8.0 29.6 9.5 35.4

Tree information Tree species Ficus bullenei4 Ficus citrifolia Ficus cotinifolia3 Moraceae Ficus goldmani Ficus hondurensis Ficus morazaniana Ficus obtusifolia4 Ficus ovalis Psydium Myrtaceae guajaba1 Karwinskia Rhamnaceae caldronii1 Alibertia edulis1 Genipa Rubiaceae americana1,2 Guettarda macrosperma2 Randia monantha1 Simaruba Simaroubaceae glauca1,2 Solanum Solanaceae hazenii1 Guazuma Sterculiaceae ulmifolia2

Nutritional data from 1 McCabe 2005, 2 Vogel 2006, 3 Jordano 1983, 4 Milton 2008. FPV: fruit patch visit.

International Journal of Zoology

Table 2: Ethogram of the behaviour classes recorded during behavioural scan samples of Cebus capucinus in Sector Santa Rosa, ACG, Costa Rica. Behaviour class Extractive foraging fruit Fruit foraging Visually foraging fruit Feeding on fruit Extractive foraging invertebrate Insect foraging Visually foraging invertebrate Feeding on invertebrate Other foraging Feeding on other Resting Low Intensity Social Directed travel Active Other Type Description Extracting edible part of fruit from husk/shell within a fruit patch Scanning for or consuming bite-sized fruit within a fruit patch Dedicated feeding (duration > 1 sec) on fruit within a fruit patch Extracting invertebrates from bark, branches, leaves; stationary insect foraging Scanning for and consuming bite-sized invertebrates, often coincident with slower group travel Dedicated feeding (duration > 1 sec) on invertebrates; stationary insect feeding Dedicated feeding (duration > 1 sec) on vertebrates or woody plant parts Sitting or lying down; not in physical contact with other group members Resting in contact; giving/receiving grooming; playing with other group members Directed travel at high rate of speed; does not include visual foraging Intergroup encounters, predator alarms/mobbing

Foraging behaviours

Nonforaging behaviours

10:00

11:00

12:00

13:00

14:00

15:00

16:00

Time of day

3.2. Eect of Figs on Ranging Behaviour. Our study groups traveled 2357 506 m daily (range: 12003892 m). Day range lengths varied signicantly among group size classes (F = 7.13, N = 186, df = 2, 11, P = 0.0103) and between the wet and dry seasons (F = 5.17, N = 186, df = 1, 11, P = 0.0440). Day range lengths were 110 m shorter on average on g days, but this was not a statistically signicant difference (F = 0.42, N = 186, df = 1, 11, P = 0.53). There was considerable variation in the time that capuchin groups spent stationary during our study. Occasionally (N = 21 days) we observed the capuchins to remain stationary for more than ve half-hour intervals per day while on other days (N = 34) the groups did not stop travelling for even one interval. We did nd a signicant eect of g visits on stationary time. The capuchins spent nearly twice as much time stationary on days when they visited gs, than nong days (F = 19.26, N = 186, df = 1, 179, P < 0.0001). Capuchin groups traveled 13.2 metres/hour faster on g days, although the eect was not signicant (F = 0.02, df = 1, 11, P = 0.8841) because of the large intradaily varia-

Fig FPVs Fig day Nong day

Figure 1: Average travel distance and g fruit patch visit (FPV) frequency by time of day for Cebus capucinus in Sector Santa Rosa, Costa Rica.

tion in travel speed. Capuchins travelled further in 30minute intervals (i.e., more quickly) in the early morning, when g visitation rates were the highest, and more slowly as midday approached relative to days on which gs were not visited (Figure 1). Travel rates during the latter half of the day were more similar between g days and nong days. 3.3. Eect of Figs on Activity Budgets. Time spent in foraging versus nonforaging behaviours was not aected by whether the group went to a g tree. However, among the foraging behaviours, capuchins dedicated signicantly more time to fruit foraging (F = 28.85, N = 114, df = 1, 111, P < 0.0001) and correspondingly less time to invertebrate foraging on

17:00

5:00

6:00

7:00

8:00

9:00

species is signicantly lower than the other three species, but also because we only observed capuchins foraging for F. citrifolia twice and in both cases very few of the gs were ripe. The average feeding rate for ripe conspicuous gs was 14.5 gs per minute. Feeding rates for cryptic gs were lower (ranks 39, 48, and 60 for F. goldmani, F. morazaniana, and F. obtusifolia, respectively), averaging 4.9 gs per minute. At the level of an individual fruit, Ficus cotinifolia gs are not exceptionally nutritious (Table 1). However, given the high feeding rates, gs are at par with most other fruits for energy uptake rate given the nutrition of the pulp. Importantly, however, gs also contain g wasps and other animal matter, which contain a relatively high amount of energy and increase the protein content by up to 30% [20].

60 50 Frequency of g FPVs 40 30 20 10 0

160 Half-hour travel distance (m) 140 120 100 80 60 40

International Journal of Zoology

35 30 Proportion of scans 25 20 15 10 5 0 EFF EFI FEF FEI FEO OTH RES SOC TRA VFF VFI Behaviour class Fig day Nong day

7 that g intake rates are one of the highest among all fruits eaten by white-faced capuchins and are comparable to previously published g consumption rates for howler monkeys and capuchins [21, 25, 44]. Three conspicuous g species rank within the top 10 of our list of 76 fruits for which we could calculate feeding rates. Although the small single fruits from Ficus cotinifolia contain little energy (2.26 KJ; [24]) capuchins obtain substantial amounts of energy in short periods of time from these gs due to high intake rates. Perhaps the most important feature of g trees is their ability to provide an abundant source of food for entire groups of capuchin monkeys in SSR. Ficus trees have high visitation rates, the longest foraging visit durations, and the highest monkey carrying capacities of any fruit source in SSR, which ensures that most or all of the group members can feed in the same location. Compared to smaller canopy trees, capuchin feeding rates in gs are less aected by aggression levels and are only slightly higher for dominant individuals than for subordinates [44]. When capuchins forage in large-crowned trees, individuals are able to spread out and reduce competition and aggression [45, 46]. Therefore, in large food patches, like g trees, the form of feeding competition may shift from contest to scramble with dominant individuals feeding in areas of the tree with higher concentrations of easily consumable fruits [21]. The energy obtained through the easy acquisition and low processing times of g fruits by entire capuchin groups supports the claim that gs are the most important resource for tropical frugivores [2]. 4.3. Eect of Figs on Ranging Behaviour. Foraging on gs does not aect the ranging behaviour of white-faced capuchins per se. Capuchin groups travel similar distances and at the same average speed on g and nong days. Travel speed and distance may be aected by other factors such as access to water and territorial monitoring and intergroup encounters [47], but the time spent stationary by capuchins is signicantly aected by trips to g trees. Capuchin groups spend signicantly more time stationary on g days. With constant day range lengths, we would expect capuchins to travel faster on g days to make up the distance lost during their long stationary bouts. The likely explanation is in the distribution of half-hour travel speeds. Many primates eat fruits early in the day to ensure they acquire the energy that will sustain their behaviour later in the day [22]. Capuchins travel their furthest distances during the rst few hours of the day (Figure 1). On g days, capuchin groups travel even faster during these hours and travel slower over the next few hours than they do on nong days. The early morning also coincides with the highest rate of visits to g trees, which suggests that capuchins travel directly to reach g trees as early as possible in the day. 4.4. Eect of Figs on Activity Budget. While a large amount of time spent in a large fruit patch is not unexpected [29], the behaviour dierences on g versus nong days are noteworthy. Capuchins increase their fruit foraging by ten percent on g days, which corresponds with a ten percent decrease in invertebrate foraging. This dietary shift could have several

Figure 2: Proportion of scan samples taken at 30-minute intervals dedicated to dierent behaviour classes by white-faced capuchin monkeys in Sector Santa Rosa, ACG, Costa Rica. EFF: extractive foraging fruit; EFI: extractive foraging invertebrate; FEF: feeding fruit; FEI: feeding invertebrate; FEO: feeding other; OTH: other behaviour; RES: resting; SOC: social; TRA: traveling; VFF: visually foraging fruit; VFI: visually foraging invertebrate.

g days (Figure 2). Among the nonforaging behaviours, capuchins spent more time in directed travel (F = 5.46, N = 113, df = 1, 97, P = 0.0215) on g days (Figure 2). The proportion of time dedicated to dierent low-intensity behaviours (resting, social) was not signicantly aected by g day (F = 0.23, N = 113, df = 1, 110, P = 0.6291).

4. Discussion
4.1. Figs Are more than a Fallback Resource for Cebus monkeys. The eight g species in Santa Rosa supply 31% of the fruit in the capuchin diet. This is similar to the proportion of gs in the diet of Cebus albifrons (37.5%), but higher than in the tufted capuchin, Cebus apella (20%; [6]). 87% of capuchin g-foraging time dedicated to conspicuous gs [8] and more than half of this time was spent consuming gs from Ficus cotinifolia [42]. We recorded 365 visits to Ficus trees over a period of 22 months and Ficus trees were visited in each month of the year, during which time the overall availability of fruits eaten by capuchins varies considerably (Santa Rosa capuchin database, unpubl. data). Thus, we conclude that gs are consistently important resources in the diet of whitefaced capuchins in SSR due to their year-round consumption by capuchins, and we would not characterize them as fallback foods for capuchins. 4.2. Energy Obtained during Foraging Visits to Figs. Some previous nutritional studies have downplayed the importance of gs to Neotropical primates due to their low nutritional content [20]. However, these studies have not taken into account the high feeding rates of primates in g trees, and other researchers have found that gs represent a relatively well-rounded nutritional source [43]. We found

International Journal of Zoology

Table 3: Energy, fat, and protein intake rates for Ficus cotinifolia and common invertebrate prey of capuchins in Sector Santa Rosa, ACG, Costa Rica. Species Invertebrates Cockroach (Blaberus giganticus)1 Cicada (Fidicina spp.)1 Small shelled insects (Insecta spp.)1 Caterpillars (Lepidoptera spp.)1 Grasshoppers/Katydids (Orthoptera spp.)1 Ants (Formicidae spp.)1 Scorpions (Scorpiones spp.)1 All invertebrates Figs Ficus cotinifolia (pulp only)2 Ficus cotinifolia (pulp + animal matter)2,3 Intake/h KJ/h Energy 2.437 2.319 43.396 4.279 11.556 0.033 0.134 64.150 2021.220 2099.823 g/h Fat 0.020 0.010 0.192 0.025 0.118 <0.000 0.001 0.367 3.576 4.184 Protein 0.089 0.083 1.371 0.112 0.404 0.001 0.005 2.064 6.258 7.581

0.054 0.108 27.42 12.46 0.987 0.230 0.014

894 894

Source: 1 McCabe 2005, 2 Jordano 1983, 3 Urquiza-Haas et al. 2008. Nutritional values for animal matter in F. cotinifolia are estimated from the percentage dry weight of animal matter in F. perforata.

implications for the health and nutrition of capuchins. First, invertebrate foraging is an energy-expensive behaviour. Although, individually, invertebrates are high in protein and fat [19], they are much more dicult to acquire than fruit. Capuchins utilize many techniques to acquire invertebrate prey, including breaking and chewing through branches, chasing and catching, and sifting through leaf litter, all of which are sure to be more energy expensive than g foraging. Second, invertebrate foraging is potentially more dangerous for capuchins. Defense tactics of some invertebrate prey (e.g., stinging scorpions, biting ants, and acid-releasing beetles) aside, invertebrate foraging likely increases the risk of predation to capuchins. In SSR, capuchins often forage for invertebrates on, or near, the forest oor, especially when fruit availability is low [48], which increases their susceptibility to predation by terrestrial hunters, including snakes, cats, and other carnivorous mammals. Third, invertebrate capture rates are quite low compared to fruit intake rates in general, and to g intake rates specically. Usually capuchins supplement their frugivorous diet with invertebrate prey, but they may require less supplementation if the protein intake at g trees is high enough. For example, the protein acquired by consumption of a scorpion is equivalent to only six minutes of g foraging based on published nutritional estimates [19, 20, 24] and invertebrate intake rates (Table 3). Similarly, it takes only 50 seconds of g foraging to equal the protein intake for a small, shelled invertebrate (e.g., stink bug), the capuchins most common invertebrate prey. We calculated that capuchins ingest 2.1 g protein per hour from invertebrates and 6.3 g per hour of protein from gs. Therefore, g foraging may allow the capuchins to signicantly decrease the amount of time spent searching for and capturing invertebrates. Capuchins spent signicantly more time involved in directed travel on g days. Directed travel is dened as fast-speed movement (adults walk/jump quickly or lope, and juveniles usually run) that does not include visual

foraging. During other group movement, capuchins often travel more slowly and forage for invertebrates while moving between fruit trees, water sources, or favourite rest trees. This foraging locomotion is decreased on g days. Although directed travel is expected to have higher thermoregulatory costs than foraging travel, it is noteworthy that the highest travel speeds occur early in the morning and later in the day, when thermoregulation costs of travelling in a tropical environment are decreased [33].

5. Conclusions
Fig trees are one of the most important resources for whitefaced capuchins in the tropical dry forests of Costa Rica. They provide a superabundance of food, simultaneous foraging space for many group members and lower predation risk, allowing monkeys to spend less time in solitary searching for invertebrates close to the forest oor. Additionally, group cohesiveness and close proximity in g trees allows for better vigilance and protection from aerial predators. The fruit biomass in g trees provides enough energy to satiate an entire capuchin group, despite the fact that energy uptake rates from Ficus cotinifolia are not signicantly higher than other fruit species. Finally, gs fruit asynchronously and year round, making them a dependable resource for capuchins living in a tropical dry forest where fruit availability is highly seasonal.

Acknowledgments
The authors extend great thanks to Adri n Guadamuz for his a help with tree identication. They also thank Roger Blanco Segura and the sta of the Area de Conservacion Guanacaste for help with the project and the Ministerio de Ambiente y Energa (MINAE) for permission to conduct research in a Costa Rican national park. The authors are grateful to

International Journal of Zoology Adrienne Blauel, Fernando Campos, Brandon Kl g, Mike u Lemmon, Krisztina Mosdossy, and Laura Weckman for their hard work and assistance with data collection and to John Addicott for programming our behavioural data parsers and assistance with analyses and databases. Financial support was provided by the Government of Alberta (NP), the Alberta Ingenuity Fund (ADM) and The Leakey Foundation (ADM), and the Natural Sciences and Engineering Research Council of Canada (ADM & LMF) and the Canada Research Chairs Program (LMF). The University of Calgary funded the presentation of a portion of this study at the 32nd Meeting of the American Society of Primatologists.

9
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