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The Evolution of Anterior Coloration in Carnivorans

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The Evolution of Anterior Coloration in Carnivorans Behav Ecol Sociobiol (2017) 71:177 https://doi.org/10.1007/s00265-017-2402-5 ORIGINAL ARTICLE The evolution of anterior coloration in carnivorans Tim Caro 1 & Hannah Walker2 & Sharlene E. Santana3 & Theodore Stankowich2 Received: 11 July 2017 /Revised: 27 October 2017 /Accepted: 2 November 2017 # Springer-Verlag GmbH Germany, part of Springer Nature 2017 Abstract in mustelids, viverrids, and herpestids. Facial complexity Some carnivorans have striking patches of fur on their faces of viverrid and herpestid species was significantly or mar- (spots, bands, eye masks) and blazes on their chests that are ginally related to a mammal-based diet. In ursids, facial primarily visible from a frontal view. We tested five hypothe- contrast appeared less variable in species living in greater ses to explain the evolution of the complexity and contrast of sympatry with other bears. Facial and chest coloration in these color patches. These were: signals of species identity to Carnivora appears to have evolved under different selec- avoid hybridization, communication between conspecifics, tion pressures in different families. signals used to warn of defensive anal secretions, signals of belligerence or pugnacity, and camouflage-related coloration Significance statement used to break up the outline and facial features of the predator The reasons that many carnivorans have colorful and memo- when approaching prey. Using phylogenetically controlled rable faces and chests are not yet understood. Here, we pit five multifactorial analyses in six different families of carnivorans, different hypotheses against each other: species recognition, examined separately, our analyses uncovered significant advertising either toxic anal defenses or pugnacity, recog- positive associations between measures of color pattern nizing group members, and trying to remain concealed complexity and sociality across herpestid faces and canid when approaching mammalian prey. We find that measures chests, suggesting use in social communication. Mustelid of facial and chest complexity and contrast have evolved facial color complexity was associated with ability to direct for different reasons depending on the carnivoran family. anal secretions accurately at predators, and facial markings Anterior coloration appears to be involved with social were significantly or marginally associated with pugnacity communication in herpestids and canids; facial coloration is associated noxious secretions in mustelids, with pugnac- ity in mustelids, viverrids and herpestids; with reliance on Communicated by M. Festa-Bianchet a mammal-based diet in viverrids and herpestids; and with avoiding hybridization in bear species. There is no over- Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00265-017-2402-5) contains supplementary riding evolutionary explanation for varied facial and chest material, which is available to authorized users. pelage coloration across carnivorans. * Tim Caro Keywords Carnivores . Chests . Color complexity . [email protected] Contrast . Faces 1 Department of Wildlife, Fish and Conservation Biology, University of California, Davis, CA 95616, USA Introduction 2 Department of Biological Sciences, California State University, Long Beach, CA 90840, USA To understand the evolutionary significance of external color- 3 Department of Biology and Burke Museum of Natural Hosry and ation in animals, we often focus on overall appearance be- Culture, University of Washington, Seattle, WA 98195, USA cause protective coloration, for example, will usually involve 177 Page 2 of 8 Behav Ecol Sociobiol (2017) 71:177 the whole animal being either cryptic, so as not to be detected, In this paper, we examine carnivoran anterior coloration or conspicuous so as to signal to a predator or conspecific using two measures: the number of different shades (pattern from a distance. Yet head coloration often differs from the rest complexity), and the contrast among those shades, in six dif- of the body in many vertebrates, including reef fish, agamid ferent families of carnivorans. Across this extensive sample lizards, marmosets, and parrots, as well as invertebrates such (31 canids, 44 mustelids, 35 felids, 8 ursids, 19 viverrids, and as paper wasps and caterpillars. In some of these species, 22 herpestids), we test several hypotheses that could explain coloration and patterns on parts of the head are known to the evolution of facial and chest coloration within the context function as signals to conspecifics, conveying information of interactions with both conspecifics and heterospecifics. about individual identity, physiological state or species First, we test the hypothesis that anterior coloration is in- identity (Hill 2015; Tibbetts et al. 2017), or as signals to volved in conspecific recognition and maintaining reproduc- heterospecifics conveying information about species iden- tive isolation. We predict that the complexity of facial color tity or defenses (Caro and Allen 2017). On the other hand, patterns is associated with extent of species’ sympatry at the coloration patterns might break up the outline of the face family level (e.g., number of congeneric sypatric species), as to reduce the probability of the animal being recognized previously reported in primates. Conspecific recognition asapredatororprey(Cott1940). could be a concern for carnivorans because free-living Certain orders of mammals have notably colorful facial and heterospecifics can interbreed (e.g., coyotes Canis latrans chest pelage patterns, particularly primates, carnivorans, and and wolves Canis lupus in the northeast USA; Lehman et al. some artiodactyls (Caro 2013); however explicit tests of adap- 1991). Second, we test whether anterior coloration varies in a tive hypotheses to explain these patterns are scarce (Caro way that is consistent with uses for intraspecific communica- 2009). To summarize briefly what we know at present: plat- tion, in particular individual recognition. We predict that facial yrrhine neotropical primate (Santana et al. 2012), Old World coloration is associated with species’ sociality (e.g., Santana catarrhine (Santana et al. 2013), and cercopithecine guenon et al. 2012) such that species living in larger groups exhibit (Allen et al. 2014) species all show greater facial color pattern more complex facial coloration. Third, we reexamine whether complexity when living with a greater number of species be- anterior coloration is used as a warning to potential predators longing to the same genus or family. Whereas neotropical or competitors signaling extent of toxic anal defenses or of primates show greater facial color pattern complexity in spe- pugnacious behavior (see Ortolani and Caro 1996;Ortolani cies that live in smaller groups (Santana et al. 2012), catar- 1999). We predict that facial contrast and complexity is asso- rhines show greater facial complexity in more gregarious spe- ciated with noxious anal secretions, and then with pugnacity. cies (Santana et al. 2013). These independent effects suggest Finally, we examine whether facial and chest coloration diver- facial coloration serves as a species marker that may reduce sity in carnivorans is consistent with strategies for crypsis, in risk of hybridization and possibly help in individual identifi- which facial coloration breaks up the outline of the carnivoran cation within social groups. and makes it more difficult to recognize when approaching Dark-faced artiodactyls live in intermediate or large groups visually oriented prey. We predict that facial coloration is and are also pursued by coursing predators, suggesting that more complex and contrasting in those species that principally facial coloration may function in various forms of intra- and capture mammalian prey. We run analyses within carnivoran interspecific communication. Artiodactyls with white faces families as only closely related species present a danger as are diurnal, live in bushland or grassland habitats, and in potential breeding partners. intermediate-sized groups, so it is unclear whether their facial colors may be involved in signaling to conspecifics, aid in thermoregulation, or both (Stoner et al. 2003). Methods Some carnivoran species that are pugnacious or employ noxious anal secretions (e.g., mustelids and mephitids) Dependent variables have conspicuous facial coloration (Stankowich et al. 2011;Caroetal.2017). Furthermore, carnivorans with HWextracted up to 10 photographs of 164 terrestrial Carnivora facial stripes are middle sized, are dangerous to confront, species from books and reputable internet sites in which spe- and are more likely to use burrows or dens (Newman et al. cies identification was listed along with scientific name and, 2005; Stankowich et al. 2011) where only their faces may often, location (see supplementary material for full datset). be visible. Nonetheless, other carnivoran species have even Because photographs mined from the internet and books carry more intricate and chromatic anterior coloration (see Fig. 1 little information about camera sensors or illumination, we for examples), and the complexity of such patterns on the used several photographs of different individuals of each spe- chests and faces suggests that they could be used for pur- cies. Calibrated photographs of museum specimens were not poses other than aposematism, especially since families used because facial patches and patterns are distorted by the like ursids do not use anal secretions for defense. preparation process
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