American Journal of Primatology 77:1109–1121 (2015)

RESEARCH ARTICLE Contrasting Responses to Novelty by Wild and Captive Orangutans SOFIA I. F. FORSS*, CAROLINE SCHUPPLI, DOMINIQUE HAIDEN, NICOLE ZWEIFEL, AND CAREL P. VAN SCHAIK* Anthropological Institute and Museum, University of Z€ urich, Z€ urich, Switzerland

Several studies have suggested that wild primates tend to behave with caution toward novelty, whereas captive primates are thought to be less neophobic, more exploratory, and more innovative. However, few studies have systematically compared captive and wild individuals of the same species to document this “captivity effect” in greater detail. Here we report the responses of both wild and captive orangutans to the same novel items. Novel objects were presented to wild orangutans on multiple platforms placed in the canopy and equipped with motion-triggered video cameras. The same and different novel objects were also presented to orangutans in two different zoos. The results demonstrate extreme conservatism in both Bornean and Sumatran wild orangutans, who gradually approached the novel objects more closely as they became familiar, but avoided contact with them over many encounters spanning several months. Their zoo-living conspecifics, in contrast, showed an immediate neophilic response. Our results thus confirm the “captivity effect.” To the various ecological explanations proposed before (reduced risk and increased time and energy balance for captive individuals relative to wild ones), we add the social information hypothesis, which claims that individuals confronted with novel items preferentially rely on social cues whenever possible. This caution toward novelty disappears when human caretakers become additional role models and can also be eroded when all experience with novelty is positive. Am. J. Primatol. 77:1109–1121, 2015. © 2015 Wiley Periodicals, Inc. Key words:

novelty response; orangutans; wild; zoo; captivity effect

INTRODUCTION In recent years, interest in novelty response has soared because it is generally seen as a major source of behavioral innovations and creativity [Auersperg et al., 2011; Greenberg, 1990; Kaufman & Kaufman, 2004; Kaufman et al., 2011; Mettke-Hofmann et al., 2002; Reader, 2003], which in turn are regarded as a good measure of cognitive abilities [Reader & Laland, 2002; Reader et al., 2011]. Novelty response is usually described by two main outcomes, neophilia and neophobia, which are generally considered two independent mechanisms [Carter et al., 2012; Greenberg, 2003; Greenberg & Mettke-Hofmann, 2001; Hughes, 2007; Mettke-Hofmann, 2014; Mettke-Hofmann et al., 2002; Miranda et al., 2013; Pisula et al., 2012; Russell, 1973; Sabbatini et al., 2007]. While neophilia refers to the seeking, approaching, and exploration of novelty, neophobia refers to avoidance of, reluctance to approach, or even fear of, novelty [Greenberg, 1990; Mettke-Hofmann et al., 2006; Mettke-Hofmann, 2014]. The aim of this study was to examine how wild and captive orangutans respond to novel artifacts. As what is novel is highly context dependent, responses may differ both qualitatively and quantitatively [Heyser & Chemero, 2011; Mettke-Hofmann et al.,

© 2015 Wiley Periodicals, Inc.

2006]. Because we could not measure the subjects’ internal state [Mettke-Hofmann et al., 2006], and thus could not estimate distress and fear, our focus here is on the observable behaviors. Various other studies have also estimated neophilia/neophobia as approach rates to novel artifacts and/or willingness to feed near them [Benson-Amram et al., 2013;

Contract grant sponsor: Waldemer von Frenckell’s Foundation; contract grant sponsor: Paul Schiller Foundation; contract grant sponsor: A. H. Schultz Foundation; contract grant sponsor: Ella and Georg Ehrnrooths Foundation; contract grant sponsor: International Primatological Society 

Correspondence to: Sofia Ingrid Fredrika Forss, Anthropological Institute & Museum, University of Z€ urich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland. E-mail: [email protected]  Correspondence to: Carel P. van Schaik, Anthropological Institute & Museum, University of Z€ urich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland. E-mail: [email protected] Received 22 April 2015; revised 18 May 2015; revision accepted 16 June 2015 DOI: 10.1002/ajp.22445 Published online 26 June 2015 in Wiley Online Library (wileyonlinelibrary.com).

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Bergman & Kitchen, 2009; Mettke-Hofmann et al., 2002; Webster & Lefebvre, 2001]. In primates, most studies of novelty response conducted on captive groups describe neophilia [Addessi et al., 2007; Chamove, 1983; Ehrlich, 1970; Glickman & Sroges, 1966; Joubert & Vauclair, 1986; Visalberghi, 1988]. In contrast, the few available studies of wild primates report cautiousness toward novel artifacts [Menzel, 1966; Visalberghi et al., 2003]. To ensure that this difference reflects the contrast between wild and captive conditions, withinspecies comparisons are required. We know of only two such comparisons with primates. First, after a habituation phase of banana provisioning on platforms, Visalberghi et al. [2003] investigated reactions toward novel food and objects in a group of freeranging capuchin monkeys, Cebus apella. In contrast to captive capuchins [Visalberghi, 1988; Visalberghi & Fragaszy, 1995], wild capuchins consumed very little of the novel food presented to them; furthermore, they delayed approaching both novel food and objects compared to familiar food. A second study, involving rhesus macaques, Macaca mulatta, compared captive with semi-free ranging individuals, with similar results [Johnson, 2000]. Thus, in contrast to the curiosity and neophilia reported from captivity, among wild primates novelty seems to elicit avoidance. Among non-primates, the only such comparison involves spotted hyenas, Crocuta crocuta, again with the same outcome [Benson-Amram et al., 2013]. Moreover, among primates, there is growing evidence for social influences on the integration of novel food items into feeding repertoires [Addessi et al., 2007; Leca et al., 2007; Schuppli et al., 2012; Ueno & Matsuzawa, 2005; Visalberghi & Addessi, 2000; Visalberghi & Fragaszy, 1995], suggesting that upon encounter with novelty, primates use social cues rather than risk-independent exploration. Other differences between wild and captive primates in the cognitive domain are consistent with differential responses to novelty, although they may also have other causes. Some primate species are known to use tools only in captivity, and some species using tools in the wild only manufacture them in captivity [Haslam, 2013; van Schaik et al., 1999]. Wild orangutans (Pongo spp.), for instance, use a handful of simple tools, such as sticks and leaves, whereas their captive counterparts have a broader tool repertoire, perhaps because humaninduced artifacts create a broader range of opportunities than possible with naturally occurring objects [Byrne & Russon, 1998; Russon & Galdikas, 1993; Shumaker et al., 2011]. Moreover, captive baboons, Papio anubis, performed better in problemsolving tasks than wild conspecifics [Laidre, 2007], a pattern also confirmed in spotted hyeans [BensonAmram et al., 2013]. This captivity effect has mostly been explained with reference to environmental factors. Reduced

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predation and foraging pressure provide captive individuals with a risk-free environment, abundant free time, and excess energy [Benson-Amram et al., 2013; Haslam, 2013; Kummer & Goodall, 1985; Laidre, 2007]. In addition, it has been suggested that the exposure to man-made objects reduces neophobia and enhances object handling [BensonAmram et al., 2013; Laidre, 2007; van de Waal & Bshary, 2010]. Further, in some species the social environment also differ in captivity not only resulting in increased social contacts with conspecifics [Haslam, 2013], but also social influence on behavior caused by the ability to attend to humans [Fredman & Whiten, 2008; Hirata et al., 2009]. It is therefore worth exploring the role of novelty response in the overall cognitive differences between wild and captive conspecifics. The purpose of this study was to compare the novelty response between wild and zoo-living orangutans in order to examine to what extent we could replicate the “captivity effect” in novelty reactions within this species. We tested novelty responses in two wild populations, one on Sumatra (Pongo abelii) and one on Borneo (Pongo pygmaeus wurmbii). We also did two different kinds of zoo controls, one in which the exact same items were used and one in which other novel items were used.

METHODS The Wild Populations The experiments on novelty response were conducted on wild orangutans in Indonesia at two study sites: Suaq Balimbing on Sumatra and Tuanan on Borneo. The study site of Suaq Balimbing is situated in the Kluet region of the Gunung Leuser National Park in the province of Nanggroe Aceh Darussalam (03°390 N, 97°250 E). The Tuanan research site is located in the Mawas Reserve in the Central Kalimantan province (2°090 S, 114°260 E). At Suaq, the experiment was conducted between November 2010 and April 2011, and at Tuanan between August 2010 and April 2011. During these periods, 28 orangutans were followed as focal subjects and regularily seen in the study area of Suaq Balimbing; eight adult females, two flanged males, four unflanged males, seven adolescents, and seven infants. At Tuanan, 28 individuals were regular subjects of focal follows; seven adult females, seven flanged males, two unflanged males, five adolescents, and seven infants. The procedures for these experiments were approved by the Department of Forestry and Nature Conservation (PHKA) of the Republic of Indonesia and complied with the American Society of Primatologists’ (ASP) Principles for the Ethical Treatment of Primates. During the time period of these experiments we exposed the orangutans in their natural habitat to

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Fig. 1. Platforms and novel objects presented to the wild orangutans: A fresh made orangutan night nest (a); a platform nest made to present the novel objects in the forest (b); a quadratic red Swiss flag presented together with plastic fruits (c, d); plastic flowers (e), and an orangutan doll (f).

items they had never encountered before. The novel materials presented were placed upon naturallooking platforms high in the canopy at various sites in the center of the study area, where the home ranges of many known females overlap. Because wild orangutans are occasionally seen exploring old nests in search of insects or re-building them for their own resting purpose, the platforms were established on a rattan base covered with leaves and branches of familiar tree species woven together to resemble orangutan nests, so the subjects would react toward the novel items rather than the construction itself (Fig. 1a and b).

In Suaq, 15 such platforms were placed at the most common travel height of orangutans within this habitat, 15–30 m [Prasetyo et al., 2009], in four different tree species: Tetramerista glabra, Horsfieldia polyspherulla, Parastemon urophyllus, and Sandoricum beccarianum. The tree species and exact location for the platforms were selected based on ranging patterns and most visited feeding trees, where the orangutans passed by on a regular basis (Fig. 2). In Tuanan, where the forest canopy is lower, ten platforms were put up on a height of 10–15 m in the following species in the center of the study area (Fig. 2): Syzygium sp., Notophoebe umbeliflora,

Fig. 2. a and b: Suaq Balimbing and Tuanan: orangutan travel routes and passes by the platform locations (30 m, 60 m and 90 m) during the experimental time period 2010–2011. c and d: Suaq Balimbing and Tuanan: travel routes and passes by the platform locations (no platform) during the control period (Suaq Balimbing: 2013–2014, Tuanan: 2012–2013).

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Shorea parvistipulata, Dyera lowii, Neoscortechinia kingii, Sandoricum borneense, and Payena leerii. The novel objects presented on the platforms were yellow, white, or pink plastic flowers, a small red quadratic flag (Swiss) in combination with plastic fruits and a small plush orangutan doll (40 cm) (Fig. 1c–f). Plastic flowers were chosen because their colors stood out against the otherwise green canopy but also might be visually recognized from a distance as a potential food item. Orangutans occasionally feed on flowers from multiple different species familiar to them. The red quadratic flag represented a shape–color combination not naturally occurring in orangutan habitats. It was placed above the platform in order to draw attention to the location and the explorable plastic fruits on the platform below it. The orangutan doll could potentially at a distance resemble an infant sitting on a nest, but at closer proximity perceived as a novel stimulus. During focal follows at both Suaq Balimbing and Tuanan throughout the experimental period, we recorded all approaches toward a platform within 30 m (the approximate distance at which objects can be seen in the mid-canopy) using standardized focal protocols and ad libitum data [Martin & Bateson, 2007]. Focal methods basically followed van Schaik [1999]; a complete description can be found at: www. aim.uzh.ch/Research/orangutannetwork.html. At Suaq Balimbing, we additionally recorded all approaches to

Contrasting responses to novelty by wild and captive orangutans.

Several studies have suggested that wild primates tend to behave with caution toward novelty, whereas captive primates are thought to be less neophobi...
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