Observation of tool use in striped skunks: how community science and social media help document rare natural phenomena

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1 Observation of tool use in striped skunks: how community science and social media help document rare natural phenomena MARIO B. PESENDORFER, 1,2, SUZANNE DICKERSON, 3 AND JERRY W. DRAGOO 4,5 1 Cornell Lab of Ornithology, Ithaca, New York, USA 2 Smithsonian Migratory Bird Center, National Zoological Park, Washington, D.C., USA 3 Colorado Springs, Colorado, USA 4 Museum of Southwestern Biology, University of New Mexico, Albuquerque, New Mexico, USA Citation: Pesendorfer, M. B., S. Dickerson, and J. W. Dragoo Observation of tool use in striped skunks: how community science and social media help document rare natural phenomena. Ecosphere 9(11):e /ecs Abstract. Tool use, the manipulation of one object to change the state of another, is found in <1% of animal taxa and most often observed in captivity. Here, we report the observation of tentative tool use in a wild striped skunk (Mephitis mephitis), captured by a trail camera in the front yard of a hobby naturalist who shared the photographs on social media. The skunk is shown manipulating a rock in a manner that strongly suggests the goal of breaking the frozen surface of a water bowl to drink. Skunks join other carnivores that innovated tool use and proto-tool use in the context of extractive foraging. Their versatile dexterity and manipulative foraging, likely facilitated by their large relative brain size, provide the ideal context for the innovation of novel foraging techniques. We therefore hypothesize that tool use will be observed in other members of the skunk family (Mephitidae), particularly as the broad availability of trail cameras, and the rapid dissemination of interesting observations via social media will increase the discovery rate of rare natural history phenomena. We encourage our colleagues to strengthen this pipeline to discovery, which reverses the information flow of community science projects, to bring amateur and professional naturalists closer together. Key words: cameras. Carnivora; community science; foraging; innovation; Mephitis mephitis; social media; tool use; trail Received 18 September 2018; accepted 24 September Corresponding Editor: Debra P. C. Peters. Copyright: 2018 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 5 Present address: New Mexico Department of Agriculture - Veterinary Diagnostic Services, Albuquerque, New Mexico, USA. mario.pesendorfer@yahoo.com Tool use, defined as the external employment of an unattached or manipulable attached environmental object to alter more efficiently the form, position, or condition of another object, another organism, or the user itself (Shumaker et al. 2011:10), is a rare phenomenon that is reported for <1% of animal genera, yet is found in diverse taxa ranging from urchins to chimpanzees (Biro et al. 2013). Among mammals, tool use is most commonly observed in primates (41 species), while only 23 non-primate species are reported to have used tools (Bentley-Condit and Smith 2010). The behavior can be limited to a single captive individual of a species or include all members of the global population (e.g., Rutz et al. 2016). Tool use is generally observed in the context of foraging, but also during physical maintenance, courtship, predator defense, or antagonistic interactions (Bentley-Condit and Smith 2010). Despite extensive interest in tool use 1 November 2018 Volume 9(11) Article e02484

2 by animals, however, the taxonomic distribution and evolutionary context of the behavior are still poorly understood. Here, we report an observation of apparent tool use in a striped skunk (Mephitis mephitis), captured on 13 February 2018 by a camera trap installed by one of us (SD) in a suburban front yard of Colorado Springs, Colorado, USA. Nine pictures, taken over a period of 15 s, show an individual using a rock to break through a layer of ice, presumably to drink the water below (Fig. 1). The skunk is shown approaching the water dish while carrying a rock in its left front paw. The rock is then struck onto the ice surface in a dynamic yet controlled manner, as indicated by the left paw s grip combined with the change in posture. Unsuccessful in this attempt, the skunk pulls the rock out of the dish with the same paw. Four seconds later, the skunk is again captured standing on the ice with a rock that resembles the one used previously. The skunk then moves across the dish, likely to drink water. No other animals were recorded on the camera trap that night. Inspection of the water dish the following morning revealed two holes with a diameter of ~2 cm in the ice surface. Skunks (Order Carnivora; Family Mephitidae) are opportunistic generalists, inquisitive and flexible foragers with great dexterity and a manipulative approach to potential prey items (Azevedo et al. 2006). The small- to mediumsized mammals are ubiquitous in North America and among the most familiar mammals throughout their range, mostly due to their unusual use of scent glands as a principal defense mechanism. They tend to be more insectivorous than Fig. 1. Apparent tool use in a striped skunk. Series of nine photographs spanning 15 s, captured using a trail camera on 13 February 2018 in Colorado Springs, Colorado, USA, by Suzanne Dickerson. 2 November 2018 Volume 9(11) Article e02484

3 other members of the order Carnivora (Dragoo 2009). To date, striped and spotted skunks (Spilogale spp.) were categorized as proto-tool users because they often drop food items during extractive foraging (Shumaker et al. 2011). In captivity, they have been observed opening eggs by throwing them between their legs at hard objects (Stebler 1938, Van Gelder 1953, J. Dragoo personal observations). Similarly, skunks overcome the defenses of Tenebrionid beetles that produce toxic chemical secretions when disturbed by rolling the prey in dirt until a tentative bite confirms that the insect has become palatable (Slobodchikoff 1978). The observation of rock pounding or throwing provides plausible evidence for tool use; it involves a mobile, external object, the rock, which is manipulated to change the condition of the ice surface to access an important resource, a drink of water. Other carnivores regularly use tools, but the behavior is most frequently observed in captivity and only rarely reported for wild animals (Bentley-Condit and Smith 2010). Polar bears (Ursus maritimus) have been reported to throw chunks of ice or rocks onto resting pinnipeds, often successfully injuring their prey (Harington 1962). Spectacled bears (Tremarctos ornatus) re-arrange large trees in their cages in order to reach desired food (Lang 1974), while Alaskan brown bears (Ursus arctos) and giant pandas (Ailuropoda melanoleuca) use objects from their environment to scratch their skin and maintain their fur (Eisenberg and Kleiman 1977, Deecke 2012). Several mongoose species, including ring-tailed (Galidia elegans), dwarf (Helogale parvula), and crab-eating (Herpestes urva) mongoose, are all proto-tool users that extensively manipulate objects to extract food (Bentley-Condit and Smith 2010). Banded mongoose (Mungos mungo), like skunks, are known for throwing rocks between their hind legs to break ostrich (Struthio camelus) eggs (van Lawick Goodall 1970). Tool use and proto-tool use are particularly common in the family Mustelidae (weasels, badgers, and sea otters), closely related to Mephitidae. California sea otters (Enhydra lutris) use rocks to break shells of mussels (Mytilus californianus), sea urchins (Strongylocentrotus spp.), and spiny lobsters (Panulirus interruptus; Hall and Schaller 1964). North American badgers (Taxidea taxus) use rocks, clay bricks, and wood blocks to cut off escape routes for ground squirrels (Urocitellus spp.) before attempting capture (Michener 2004). In contrast to the egg throwing between the hind legs observed in mongoose, yellow-throated martens (Martes flavigula) lift eggs up vertically and drop them directly in front of themselves (Wemmer and Johnson 1976). Except in the case of sea otters, our knowledge of tool use in carnivores has generally been based on single observations or repeated observations of single individuals, often in captivity (Bentley-Condit and Smith 2010). The skunk s ice-breaking behavior, best described as rock pounding or throwing, therefore joins that of other carnivores using tools in the context of food extraction or capture. It shares the uniting feature of foraging carnivore (proto-) tool users the need to access inaccessible resources by overcoming physical barriers. Such complex problem-solving tends to be associated with increased cognitive ability found in animals with large relative brain size. Among carnivores, experiments show that species with large residual brain size (i.e., larger brains than expected for their body weight) and extensive behavioral repertoires are more successful in opening artificial puzzle boxes to extract food (Benson-Amram et al. 2016). Furthermore, broad comparative analyses across carnivores show that animals in the families Mephitidae and Mustelidae evolved a steeper allometric relationship between body mass and brain volume, so that larger species also have greater relative brain sizes (Finarelli and Flynn 2009). Interestingly, brain size variation in mammals is often associated with group size, yet this relationship does not hold for carnivores (Finarelli and Flynn 2009). Instead, problem-solving and behavioral flexibility in novel environments appear to be important drivers of brain size variation (Sol et al. 2005, 2008). Striped skunks, who are among the heaviest members of Mephitidae (~5 kg; Wade-Smith and Verts 1982, Dragoo 2009), are therefore strongly encephalized which likely provides the neural substrate for their complex behavioral repertoire. As generalist opportunists with high dexterity, they are primed to develop sophisticated foraging strategies, including tool use, in novel environments of suburban backyards (Sol et al. 2008, Benson- Amram et al. 2016). We hypothesize that several other species of carnivores have the capacity to 3 November 2018 Volume 9(11) Article e02484

4 innovate while foraging, including the potential to learn how to use tools. We also predict that the discovery of tool use in other carnivore species will occur at an accelerated rate because of the broad use of remote sensing technology, particularly trail cameras by community scientists and lay people, and the dissemination of animal behavior videos in social media. COMMUNITY SCIENCE AND SOCIAL MEDIA: A RECIPE FOR THE DISCOVERY OF RARE PHENOMENA? This case study highlights the emerging synergy between broad public access to technology developed for specific audiences,in this case scientists and hunters, and social media in their contribution to the understanding of the natural history of understudied species or phenomena. While community science (often called citizen science) is usually based on a pre-existing question stated by scientists (Newman et al. 2012), the flow of information was reversed in our study. SD first acquired a commercially available camera trap in 2008 with the aim of documenting the wildlife that resides on a remote small-acreage lot. She recorded a diverse animal community, including black bears (Ursus americanus), coyotes (Canis latrans), elks (Cervus canadensis), and ground squirrels (Spermophilus sp.). Curious to learn more, she installed more units in her yard. To achieve her goal of obtaining a close-up portrait of her nightly visitors, she eventually bought better cameras, lenses, and even engineered her own battery wiring to improve longevity. But with whom to share her bounty? Family and friends soon tired of the wildlife photographs, even after she gifted many with cameras. Through a friend, SD discovered a Twitter community that centers around showcasing animals captured on trail cameras and also provides feedback on equipment or techniques used to obtain high-quality images.inthiscontext,sdinquiredaboutprevious reports of skunk tool use, which was shared and liked widely ( Sue/status/ ). The post elicited responses from several animal behavior researchers, including the first author, and SD quickly agreed to co-author a publication on her discovery. Other researchers have used observations shared on social media to obtain relevant data on rare phenomena or species. Rutz and Deans (2018), for example, report the observation of tool use in Eurasian nuthatches (Sitta europaea), which was recorded by a birdwatcher, posted online, discovered, and published by a scientist. Schachner et al. (2009) studied vocal mimicry and entrainment (dancing) in parrots by analyzing contributions posted on the social video platform YouTube. Davies et al. (2012) supplemented the data from a community science platform ( by searching the photo platform Flickr and YouTube for whale shark images and videos captured in their study area. The synergy between broadly distributed technology and social media provides a powerful discovery tool for rare phenomena and species. The challenge for scientists seeking such data is now to develop information pipelines that connect self-motivated community scientists and incidental observers of animal behavior with their professional counterparts. While there are several community science projects that invite users to post their camera trap images, continued work in science communication to connect lay people with specialists should ultimately catalyze discoveries that expand our understanding of natural history. We predict that the rate of discoveries of rarely witnessed behavior, such as that of tool use in uncommon species, will increase as scientists and enthusiasts become more connected online. ACKNOWLEDGMENTS We thank Knut Kielland, Christian Rutz, Rhiannon Crain, and Janis Dickinson for insightful comments on the manuscript. The authors declare no conflict of interest. LITERATURE CITED Azevedo, F. C. C., V. Lester, W. Gorsuch, S. Lariviere, A. J. Wirsing, and D. L. Murray Dietary breadth and overlap among five sympatric prairie carnivores. Journal of Zoology 269: Benson-Amram, S., B. Dantzer, G. Stricker, E. M. Swanson, and K. E. Holekamp Brain size predicts problem-solving ability in mammalian carnivores. Proceedings of the National Academy of Sciences of the United States of America 113: November 2018 Volume 9(11) Article e02484

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