Current Biology Dispatches

Animal Behavior: Ape Curiosity on Camera

Sofia Ingrid Fredrika Forss*, Alba Motes-Rodrigo, and Claudio Tennie Faculty of Science, Department for early prehistory and quaternary ecology, University of Tu¨ bingen, Germany *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.02.055

How respond to novel objects may reflect their overall cognitive and behavioral disposition. A study using camera traps reveals that different of wild ape respond to novelty differently.

How animals react to novel situations, apes. Overall, immatures looked towards humans and our artefacts affect wild foods or objects reflects a balance camera traps the most and individuals in animals’ behavior. between neophobia (novelty avoidance) smaller parties looked at the camera traps The study of Kalan and colleagues [1] and neophilia — the drive to approach for a shorter time than lonely apes. Apes nicely complements previous results and explore, in other words components showed less interest in camera traps the reporting conservative behavior towards of curiosity. As such, animals behave closer they lived to long-term research novelty in wild orangutans. Like African according to the costs and benefits of sites. As such the authors suggest apes, wild orangutans mostly look at novel exploring something new, potentially environmental factors to reflect part of the objects and only touch them in rare dangerous. In a new study in this issue of site variation in responses. Moreover, the cases — after observing humans doing Current Biology, Ammie Kalan, Hjalmar authors propose that the observed so — suggesting orangutans use social Ku¨ hl and colleagues [1] report the species differences in camera trap cues to overcome neophobia [5].The behavioral responses of wild responses are due to variation in social study by Kalan and colleagues [1] also chimpanzees, bonobos and gorillas to structure, such as lack of clear leadership hints to within-species differences camera traps. in bonobo communities contributing to between captive and wild apes. Wild apes It is difficult to study reactions to novelty increased neophobia in this species. spend most of their wake time searching in the wild — usually this was thought to Studies on novelty responses in wild for food, mating partners, or shelter in demand field experiments where one primates are rare, and comparisons natural habitats beset with risks. must be careful not to habituate wild between species are so far lacking Consequently, for wild apes, curiosity can populations, e.g. through food (but, see [2]), making the contribution be much more costly than for their captive provisioning or through association with of Kalan and colleagues [1] highly conspecifics, who benefit from a safer humans. Consequently, studies aiming to valuable. habitat and have more time to invest in address curiosity should best avoid direct Using camera traps as stimuli is a exploration. This within-species human observation. The use of video useful first step to determine how discrepancy is referred to as the captivity camera traps, applied by Kalan and artefacts placed in nature affect wild ape effect [5–7] and explains the increased colleagues [1], is a relatively non-invasive, behaviors. But one could argue that curiosity observed in captive housed apes yet effective approach to obtain genuine the (camouflaged) camera trap itself [8]. The study by Kalan and colleagues [1] reactions to novel items in wild apes. represents a relatively uninteresting novel thus stresses the importance of studying Camera traps also enable researchers to object for wild apes. Accordingly, the curiosity in natural habitats, because solely address novelty responses with the great authors report no real fearful behaviors captive data can generate a biased picture unknown — wild animals that are not (except a few bonobo alarm calls). Thus, of ape curiosity. The between-species habituated to humans. Kalan and the most common recorded responses — differences found by Kalan and colleagues colleagues [1] studied an impressive 43 looking impulses — are best described as [1] in wild apes, where bonobos showed different groups of the three African ape indifference rather than truly neophobic or the highest frequency of neophobic species distributed across 14 sites neophilic. This highlights the importance responses, match with some previous (Figure 1). of what kind of stimulus is used when results from captivity, describing bonobos The authors found that the three assessing novelty response and to be more risk averse than chimpanzees species of African apes differed in their explorative behavior [3,4]. However, [9,10]. However, other studies on novel responses to a novel object: camera using camera traps as stimuli has the food response found that captive traps. Apes rarely touched the camera advantage that it provides a stimulus that chimpanzees show similar food neophobia traps, which indicates that neophilia, or is consistent across different sites. Such a as bonobos and more than gorillas [11,12]. the motivation to explore, was low in low degree of variation (in appearance) is Kalan and colleagues [1] assume both all three species. Compared to generally not possible to achieve when large dietary variation and differences in chimpanzees, bonobos and gorillas were humans (and their behavior) are the innovative abilities across the tested more likely to look at the camera traps. stimuli. Thus, while we also need to use species, as chimpanzees are the most Bonobos were also the most neophobic multiple stimuli when we aim to assess proficient African ape tool users. species, producing more alarm calls and curiosity, camera traps are still Consequently, the authors expected other fearful behaviors than the other informative on how the presence of chimpanzees to show higher neophilia

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The study by Kalan and colleagues [1] draws attention to the fact that, so far, no single hypothesis can explain the variation in exploration tendency and neophobia in great apes. Ideally, future studies can disentangle environmental and social factors to clarify the relationship between exploration drive and neophobia and the conditions that elicit curiosity. Understanding curiosity in non-human primates will also shed light on the arguably extreme case of human exploration and innovation ability. Finally, natural habitats are fast changing due to human activity, causing wild populations to face new challenges. For species conservation purposes, it is now more urgent than ever to understand how different species react when faced with habitat modifications incorporating exposure to novelty. Figure 1. Gorilla on camera. Nkombe, an adult female from the Atananga Group in Gabon, taking a break from feeding. Photo: Martha REFERENCES Robbins/Loango Gorilla Project.

1. Kalan, A.K., Hohmann, G., Arandjelovic, M., Boesch, C., McCarthy, M.S., Agbor, A., than bonobos and gorillas, but in fact due to the limited field of view it is not Angedakin, S., Bailey, E., Balongelwa, C.W., chimpanzees showed the least interest in always clear how many others are around. Bessone, M., et al. (2019). Novelty response of the camera traps. This would suggest that Camera traps focusing on other camera wild African apes to camera traps. Curr. Biol. 29, 1211–1217. neophilia is not solely responsible for traps and their surroundings might help in innovation ability. In fact, it has been such cases. It would be good to know 2. Bergman, T.J., and Kitchen, D.M. (2009). Comparing responses to novel objects in wild suggested that species with strong whether any exploration event of the baboons (Papio ursinus) and geladas behavioral flexibility maintain a balance camera traps triggered other individuals (Theropithecus gelada). Anim. Cogn. 12, between neophobia and exploration to approach. Of course, sociality can have 63–73. tendency [13, 14], although the exact the opposite effect as well. In gregarious 3. Carter, A.J., Marshall, H.H., Heinsohn, R., and mechanism for this paradoxical species individuals may be busy Cowlishaw, G. (2012). How not to measure boldness: Novel object and antipredator combination is not yet fully understood. maintaining social bonds and keeping responses are not the same in wild baboons. The ‘social information hypothesis’ track of social events, which might hinder Anim. Behav. 84, 603–609. predicts that long lived, large brained them to invest in individual exploration. 4. Greggor, A.L., Thornton, A., and Clayton, N.S. species — such as great apes — are This might explain why individuals (2015). Neophobia is not only avoidance: influenced by social cues when deciding included in the study by Kalan and improving neophobia tests by combining cognition and ecology. Curr. Opin. Behav. Sci. what in their environment to attend to, colleagues [1] looked for a shorter time in 6, 82–89. followed by individual learning of the social situations. 5. Forss, S.I., Schuppli, C., Haiden, D., Zweifel, characteristics of the socially discovered The ‘dangerous niche’ hypothesis [13] N., and Van Schaik, C.P. (2015). Contrasting novel item [15]. That young individuals predicts that the level of neophobia responses to novelty by wild and captive looked longer at camera traps, but did not echoes the risk level of the habitat. Quite orangutans. Am. J. Primatol. 77, 1109–1121. necessarily touch them, suggests that the reverse was found by Kalan and young apes indeed showed interest in the colleagues [1], namely fewer neophobic 6. Haslam, M. (2013). ‘Captivity bias’ in tool use and its implications for the evolution of novelty but simultaneously were too responses in populations where hunting hominin technology. Philos. Trans. R. Soc. neophobic to interact with something new pressure was higher. This potentially Lond. 368, 20120421. and potentially risky. Similarly, young reflects that individuals of such 7. Van Schaik, C.P., Burkart, J., Damerius, L., apes are more cautious than adults to populations are more familiar with Forss, S.I., Koops, K., van Noordwijk, M.A., ingest novel food items [11,12]. It would human artifacts (extending to camera and Schuppli, C. (2016). The reluctant innovator: Orangutans and the phylogeny of be interesting to see whether young traps). Furthermore, following the creativity. Philos. Trans. R. Soc. B. Biol. Sci. individuals would proceed with physical dangerous niche hypothesis, beyond 371, 20150183. exploration of the camera traps if they human threats, there are likely to be 8. Damerius, L.A., Forss, S.I., Kosonen, Z.K., would have witnessed adults interact with more ecological hazards that could Willems, E.P., Burkart, J.M., Call, J., Galdikas, them first. account for variation in novelty response B.M., Liebal, K., Haun, D.B., and van Schaik, C.P. (2017). Orientation toward humans Using camera traps makes it hard to between the different species and predicts cognitive performance in orang- oversee the complete social situation, populations. utans. Sci. Rep. 7, 40052.

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Evolution: The Battle of the First Animals

Allison C. Daley* and Jonathan B. Antcliffe Institute of Earth Sciences, University of Lausanne, Geopolis, CH-1015 Lausanne, Switzerland *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.02.031

Ctenophores or ‘comb-jellies’ are marine animals whose relationship to other phyla is uncertain, yet important for understanding major steps in animal evolution. Fossil ctenophores from the indicate that ctenophores may have evolved from a sessile, cnidarian-like ancestor.

The origin and earliest evolution of issue of Current Biology by Yang Zhao, radially-arranged tentacles covered in animals has been the subject of open Jakob Vinther and colleagues [8] rows of hair-like protrusions, or cilia [8,9]. warfare in the natural sciences in recent describes bizarre Cambrian fossils and Siphusauctum was previously identified as decades. One important battlefield has places them in the ctenophore stem a bilaterian but could not be placed in any been the unresolved relationship between lineage, forming a close alliance between specific phylum [9]. Another taxon that has five animal groups — ctenophores, ctenophores and cnidarians (Figure 1). yet to find a home in any animal phylum is cnidarians, placozoans, poriferans and The fossils of the Cambrian explosion, Dinomischus, which is also tulip-like bilaterians (essentially all other animals). found at sites such as and but has a sclerotized organic skeleton This (phylogenetic) Battle of the Five Chengjiang, are renowned not only for their not found in the entirely soft-bodied Armies is as cacophonous and confusing exquisite preservation of soft-bodied Siphusauctum [9].ThenewtaxonDaihua as anything that Peter Jackson produced animals in fine anatomical detail, but also and the previously described Xianguangia in recent years [1]. Yet an uneasy truce because of their enigmatic nature. The [10] are both stalkless, but have a has recently emerged concerning the most famous of these are the ‘bizarre crab’ sclerotized organic skeleton supporting an position of the sponges (Porifera), Anomalocaris and the ‘mind-bending’ expanded body region with long tentacles returning to the antebellum state with a Hallucigenia. The fossils described by bearing pinnules with rows of cilia [8]. monophyletic group of sponges at the Zhao and colleagues [8] are just as Xianguangia had previously been placed in base of animal evolution [2–5]. Otherwise, enigmatic, marking this work as an the stem lineage of Cnidaria [10]. there is little resolution. These five animal important contribution to the field owing to By comparing these enigmatic fossil groups are highly derived, with over the detailed descriptions and images of a taxa with definitive ctenophores, the 500 million years separating their new taxon, Daihua sanqiong,andof phylogenetic analysis of Zhao and origination from their modern anatomy. enlightening new specimens of previously colleagues [8] places Xianguangia, The ctenophores are particularly rogue described taxa, including Xianguangia, Daihua, Dinomischus and Siphusauctum and querulous, with their molecular Dinomischus and Siphusauctum.Thislast in the stem lineage to ctenophores. The sequence seemingly switching sides so taxon has colloquially been called the ‘tulip resulting scenario of evolution suggests often that its true allegiance is difficult to animal’, which is a fairly accurate visual that ctenophores originated from sessile discern [6,7]. Fortunately, we also have description of its overall anatomy [9].The benthic, sea anemone-like ancestors, fossils. These provide another tangible tulip-shaped body of Siphusauctum with Xianguangia then Daihua branching record of evolution and are particularly consists of a narrow stem topped by a off basally, followed by the stalked abundant and well preserved during the rounded, bulbous main body chamber, Siphusauctum and Dinomischus, before first major burst of animal evolution, the which contains the mouth and gut, and is the evolution of pelagic ctenophores. This Cambrian explosion. A new study in this adorned with ‘petals’ represented by six sequence of events requires numerous

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