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Evaluating the Responses of a Territorial Solitary Carnivore to Potential Mates and Competitors Received: 22 February 2016 Maximilian L

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Evaluating the Responses of a Territorial Solitary Carnivore to Potential Mates and Competitors Received: 22 February 2016 Maximilian L www.nature.com/scientificreports OPEN Evaluating the responses of a territorial solitary carnivore to potential mates and competitors Received: 22 February 2016 Maximilian L. Allen1,2, Veronica Yovovich1 & Christopher C. Wilmers1 Accepted: 17 May 2016 Successful communication is critical to the fitness of individuals and maintenance of populations, Published: 02 June 2016 but less is known regarding the social contexts and reactions to scent marking by other individuals in solitary carnivores, including pumas. We evaluated the responses of resident male pumas to visitation and scent marking by potential competitors (other male pumas) and potential mates (female pumas) by capturing and marking 46 pumas (Puma concolor), and documenting scent marking behaviours using motion-triggered video cameras. By comparing resident male puma visitation rates and communication behaviours in response to either male or female visitors, we found that their visitation and communication behaviours were best explained by the combination of visitation by both competitors and potential mates. Resident males returned to scent marking sites more quickly and increased their rate of flehmen response after visitation by a females, while they increased their rate of visitation and duration of visits in response to other males. Male pumas also visited less frequently in summer and autumn when female visitation rates were lower, but males created nearly twice as many scrapes during these visits. This study suggests that advertising for mates when scent marking may sometimes overshadow the importance of deterring competitors and claiming territory. Communication is an integral element of animal behaviour, and scent marking is one of the most frequent forms of communication for many mammal species. As secondary sexual characteristics, scent marks are considered reliable indicators of an individual’s health and viability as a mate1,2. Due to their spatially dispersed populations, solitary carnivores rely on scent marking as an indirect method of conspecific communication (e.g. ref.3–6 ). The predominance of communication via scent marking has led to many explanations regarding the function of this behaviour in solitary carnivores. The main functions are thought to include asserting dominance7,8, selecting mates4,9,10, and maintaining territories3,11–13. Scent marking may also be used to determine the identity and relat- edness of individuals14, to mark and defend food resources15,16, and to possibly avoid infanticide6. Given the many different purposes attributed to scent marking, understanding the dynamics influencing this behaviour will help us understand its use in social contexts. The two most important functions of scent marking in solitary carnivores may be to advertise their reproduc- tive status to potential mates and to assert dominance and maintain territories over their competitors. For solitary carnivore species with a defined breeding season, scent marking increases during the breeding season4,5,11,17, which suggests that scent marking plays an important role in advertising for potential mates. However, scent marking also occurs throughout the year3,4,6,12,18, suggesting it has an on-going role in maintaining territories, and may therefore play an essential role in social organization stability. Many communication systems, including among solitary carnivores, are mark-countermark systems, whereby one individual marks, and another then marks in response3,12. The infrequency of encounters among solitary carnivores makes it more likely for individ- uals to respond when they come across intraspecific communication attempts, whether through investigation, scent marking, or another response. The utilities of scent marking in solitary carnivores could be further under- stood by determining how they respond to competitors and potential mates. In contrast to the majority of carnivore species, many large felids breed throughout the year17,18. This makes them ideal species to discern the relative importance between scent marking purposes, including whether indi- viduals react more strongly to visitation and scent marking by potential mates or by potential competitors. Like other solitary felids, pumas are territorial18,19, and communicate most frequently through scent marking18,20,21. 1Center for Integrated Spatial Research, Environmental Studies Department, University of California, Santa Cruz, USA. 2Department of Forest and Wildlife Ecology, University of Wisconsin, 1630 Linden Drive, Madison, WI 53704, USA. Correspondence and requests for materials should be addressed to M.L.A. (email: [email protected]) SCIENTIFIC REPORTS | 6:27257 | DOI: 10.1038/srep27257 1 www.nature.com/scientificreports/ Male pumas actively compete for territories that encompass resources, including access to potential mates, and scent mark throughout their territories19. Some puma populations, including in our area, show a birth pulse in summer22, with a related peak in mating season in late winter or spring. The most frequent form of scent marking by pumas is scraping18,20,21 (Supplementary Video 1), which is con- centrated in areas called ‘community scrapes’ (e.g. ref. 20) or ‘shared scrapes’ (e.g. ref. 18). We use the term ‘com- munity scrapes’ hereafter. These are defined as a location in which multiple pumas create scrapes in a small area (>3 scrapes in 9 m2) that is not associated with a kill or resting site20. Male visitation and scent marking at commu- nity scrapes occurs regularly throughout the year10,18. In contrast, female visitation occurs in short bouts of activ- ity that can be at any time of the year, which most likely correlate with breeding and estrus10,18. Pumas also exhibit other communication behaviours at community scrapes such as olfactory investigation (Supplementary Video 2), the flehmen response (Supplementary Video 3), body rubbing (Supplementary Video 4), and caterwauling or other vocalizations (e.g. ref. 10,20,21,23). Little research has been conducted as to which stimuli elicit communi- cation behaviours, or how these behaviours and their frequency are affected by interactions with potential mates and competitors. We monitored a puma population with 46 marked individuals from 2011–2014 in order to better understand how male pumas respond to visitation and scent marking by male competitors and potential female mates. We deployed motion-triggered video cameras at community scrapes to record communication behaviours. Our spe- cific objectives were to: 1) determine whether seasonal variation occurred in visitation and scent marking of male pumas at community scrapes. We hypothesized that if visitation and scent marking were based on competitors they would not vary throughout the year, while if they were based on potential mates than visitation rates would be most frequent and the most scrapes would be created in spring to coincide with the perceived peak in the mating season. 2) Determine how male visitation and behaviours changed in response to visitation by possible mates and competitors. We hypothesized that male pumas would visit and exhibit behaviours more frequently after a recent visit by both potential mates and competitors. Additionally, we hypothesized that if potential mates drive male communication, their visitation and display of behaviours would increase in response to visitation by potential mates rather than to visitation by competitors. 3) Determine whether male pumas display stronger responses to visitation by potential mates, competitors, or whether it is a combination of both. We hypothesized that while visitation and scent marking is likely affected by the combination of both, the function of visitation and scent marking may be more affected by potential mates, as they may be the rarest resource in a male’s territory. Results We monitored 28 community scrape areas for a mean of 596 (± 45 SE) days. We recorded 724 visits by mature males, and 198 visits by mature females traveling without cubs. We used the 533 visits by the 11 known (collared) mature males in our analyses. Seasonal Variation in Visitation. Male visitation behaviours varied among seasons; including the days until next visit (F3, 445 = 3.17, p =​ 0.02), the number of scrapes created (F3, 519 = 5.60, p <​ 0.01), and the duration of visits (F3, 519 = 3.00, p =​ 0.03). The days until next visit for males in spring was nearly 2 times more frequent than in summer (p =​ 0.01) (Fig. 1a). In summer, males created 35% more scrapes than in spring (p =​ 0.02), and 30% more than in winter (p =​ 0.01). In autumn, males created 13% more scrapes than in spring (p =​ 0.04) and 9% more than in winter (p =​ 0.01) (Fig. 1b). The duration of male visits in summer was 25% longer than in spring (p =​ 0.05), and marginally longer than in winter (19%, p = 0.08) (Fig. 1c). A post hoc test showed that the seasonal mean for days until next visit had strong inverse correlations with 2 2 both the number of scrapes made during visits (r 1, 3 = 0.94, p <​ 0.01), and visit duration (r 1, 3 = 0.93, p = 0.04). The inverse relationship between the number of scrapes created and days between visits suggests that male pumas create more scrapes during seasons with less frequent visitation (Fig. 2). The inverse relationship between the visit duration and days between visits suggests that males spend longer durations at the scrape during seasons with less frequent visitation. Influences on male visitation and behaviours. Male days until next visit and visit duration increased in response to visitation by other pumas, while their number of scrapes created did note vary significantly (Table 1). The mean time between visits for male pumas was 37% more frequent when another male was present within 28 days (F1, 447 = 12.09, p <​ 0.01), and 34% more frequent when another male was present within 7 days (F1, 447 = 7.34, p =​ 0.01). The mean time between visits for males was 29% more frequent when a female was present within 28 days (F1, 447 = 18.80, p <​ 0.01), and also 29% more frequent when a female was present within 7 days (F1, 447 = 15.68, p <​ 0.01).
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