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Female-Female Aggression Is Linked to Food Defence in a Poison Frog

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Female-Female Aggression Is Linked to Food Defence in a Poison Frog 1 Female-female aggression is linked to food defence in a poison frog 2 3 4 5 6 7 Heike Pröhl1*§, Martin G. Scherm2§, Santiago Meneses3,4, Corinna E. Dreher1, Ivonne 1 1 8 Meuche , Ariel Rodríguez 9 10 11 12 1 Institute of Zoology, University of Veterinary Medicine, Bünteweg 17, 30559 Hannover, Germany, 13 [email protected], [email protected], [email protected], 14 [email protected] 15 2 Institute of Diabetes Research, Helmholtz Zentrum München, German Research Center for 16 Environmental Health (GmbH), Heidemannstraße 1, 80939 München, Germany, 17 [email protected] 18 3 Smithsonian Tropical Research Institute, Luis Clement Ave., Bldg. 401 Tupper, Balboa Ancon, 19 Panama, Republic of Panama, [email protected] 20 4Department of Biological Sciences, George Washington University, Washington D.C., 20052, USA. 21 22 *Correspondence: Heike Pröhl 23 § These authors contributed equally to this work. 24 25 Total number of words (including references): 6728 1 26 Abstract 27 Habitat occupancy by territorial animals is expected to depend on the distribution of critical 28 resources. Knowledge on female territoriality is scarce but it has been suggested as a 29 mechanism to defend limited resources for reproduction. A previous study showed female 30 intrasexual aggression to be connected to territorial behaviour in the strawberry poison frog 31 Oophaga pumilio, a diurnal aposematic species with complex maternal care. Here we 32 investigate the link between spatial distribution of resources important for reproduction and 33 female distribution and behaviour. We observed focal females in their natural habitat in 34 Costa Rica, and recorded the distribution of ecological predictor variables in a grid system. 35 The data were used for calculating home range and territory sizes and for connecting female 36 habitat use to the distribution of potential resources by computing spatial habitat occupancy 37 models. Even though we found females to occupy large home ranges, they were highly 38 aggressive towards other females only inside a small part of their home range, here termed 39 core area. Among the ecological factors the sustained abundance of ants (as the main food 40 item of the frogs), the presence of leaf litter, and suitable rearing sites for tadpoles predicted 41 female site occupancy patterns. The number of ants was twice as high in the core areas 42 compared to the rest of the female home ranges. Our results suggest that female spacing 43 behaviour is principally driven by the spatial distribution of its main food resource, but that 44 hiding places (leaf litter) and tadpole rearing sites also play a role. The defence of places with 45 high sustained abundance of ants could be relevant for this prolonged-breeding species as 46 egg production and maternal care are energetically highly demanding. Regarding the link 47 between resource defence and maternal care, the reproductive strategy of female 48 strawberry poison frogs resembles that of the females of small mammals comprising same- 49 sex-competition for food and high investment in producing and rearing young. 2 50 51 52 KEYWORDS 53 feeding behaviour, frogs, habitat occupancy, resource distribution, spatial autocorrelation, 54 territoriality 55 1 INTRODUCTION 56 In natural populations individuals compete for limited resources to maximize their fitness. 57 Competitive strategies differ between the sexes, because males and females depend on 58 distinct resources for survival and reproduction, and include a broad repertoire of 59 behavioural components, e.g. aggressive encounters and territoriality (Clutton-Brock & 60 Huchard, 2013). Territoriality, i.e. the defence of a limited area, ensures the territory holder 61 prior access to critical resources like food, water, mates, hiding or nesting places (Wells, 62 1977; Pröhl, 2005; Alcock 2006).Territoriality is associated with time and energetic costs as 63 well as increased conspicuousness to predators and risk of injury (Carpenter & Mcmillen 64 1976; Marler, Walsberg, White & Moore, 1995; Alcock 2006). However, the benefits of 65 territoriality must outweigh the costs (Brown, 1964; Schoener, 1983; Adams, 2001) and the 66 resources must be defensible and limited in time or space (Wilson, 1975). 67 In numerous vertebrate species territoriality is well studied, especially for males (review 68 Wells 1977; Davies, 1991; Alcock, 2005). Males often compete for females and therefore 69 defend resources that females need for reproduction such as breeding sites (Emlen & Oring, 70 1977). When some males are stronger than others they can gain priority access to clumped 3 71 resources and thereby increase their probability for mating with multiple females (mammals: 72 Clutton-Brock, 1989; snakes: Webb, Scott, Whiting & Shine, 2015). 73 In general, female intrasexual competition and territoriality has attracted less scientific 74 attention than male competition (Clutton-Brock, 2007) but is particularly well understood in 75 small mammals (Ostfeld, 1990). Some discussion about the purpose, i.e. the resources 76 defended by females, has stimulated this research area (Wolff & Peterson, 1998). Female 77 territorial behaviour has typically been suggested as a mechanisms to defend food resources 78 (Ostfeld, 1990; Rosvall, 2011), however later studies indicated that females directly defend 79 their young in nest sites with the ultimate purpose to reduce the risk of infanticide by 80 conspecifics (Bonnatto, 2017; Steinmann, Priotto & Polop, 2009). 81 Because of the high importance of resources for reproductive success the distribution of 82 resources should influence the distribution of the sexes, while the resource distribution itself 83 is affected by other ecological factors. The link between ecological factors and distribution of 84 a species can be analysed via habitat occupancy models. These models normally analyse the 85 distribution of one or several species over larger landscapes (e.g. Joseph, Preston & Johnson, 86 2016). The questions addressed often involve which ecological factors influence the 87 presence/habitat selection and reproduction of species in a patchy landscape. Hereby spatial 88 autocorrelation often plays a role, because the proximity to other (sub-) populations or 89 occupied habitat produces emigrants and has an effect on habitat choice and therefore 90 occupancy of this habitat (e.g. Miró, O’Brien, Hall & Jehle, 2017). Here we use a habitat 91 occupancy model to relate resource distribution to the distribution and behaviour of females 92 in a frog species. 93 In frogs, defence of resources in territories occurs mainly in species with longer breeding 94 periods. Territoriality was mainly observed in males of aquatic, arboreal as well as terrestrial 4 95 egg layers (review: Wells, 2007). The resources the males defend are mostly those that 96 females need for successful reproduction such as oviposition sites. These are aggressively 97 protected against other males in ponds or streams, or other sheltered places. For the poison 98 frog family Dendrobatidae complex resource-based mating systems have been described 99 (review: Wells, 2007; Pröhl, 2005). Males often defend all-purpose territories for longer time 100 periods containing feeding, shelter, oviposition, calling and breeding sites (e.g. Roithmair, 101 1992; Poelmann & Dicke, 2008). Within anurans, female territoriality was only reported for 102 this family. Female territoriality seems to be mainly connected to defence of food and retreat 103 sites (e.g. Mannophryne trinitatis (Test, 1954; Wells, 1980a); Colostethus panamansis (Wells, 104 1980b)). 105 The strawberry poison frog (Oophaga pumilio) is a diurnal species which inhabits 106 Caribbean lowland rainforests in Nicaragua, Costa Rica and Western Panama (Myers & Daly 107 1983; Savage, 2002). Both sexes are polygamous (Bunnell, 1973; Pröhl & Hödl 1999; Meuche, 108 Linsenmair & Pröhl, 2011) and their ecology and complex reproductive behaviour are well 109 studied (e.g. Rudh, Rogell, Håstad & Qvarnström, 2013). Since females provide eggs for 110 mating and unfertilized eggs as a food source for their tadpoles, female reproduction and 111 especially maternal parental care are associated with higher energetic and temporal costs 112 than reproduction in males which only provide sperm and moisten the eggs (Limerick, 1980; 113 Weygoldt 1980; Pröhl & Hödl 1999). The diet of the strawberry poison frog consists mainly of 114 ants and mites (Donnelly, 1991), from which the frogs accumulate toxic alkaloids into their 115 skin (Saporito, Donnelly, Spande & Garraffo, 2012). Together with their aposematic 116 coloration, toxicity provides an effective protection from potential predators (Daly, Myers & 117 Whittaker, 1987; Saporito, Zuercher, Roberts, Gerow & Donnelly, 2007). 5 118 The main purposes for aggressive male territorial behaviour in O. pumilio seem to be the 119 availability of calling sites, access to females, which are the limiting sex in this species, and 120 place for courtship and oviposition (Pröhl, 2003; Pröhl & Berke 2001; Meuche, Linsenmair & 121 Pröhl 2012). Males also spend more time feeding in the core areas of their territories, but no 122 more insect prey has been found in these areas than outside of their territories (Staudt, 123 Meneses Ospina & Pröhl, 2010). Recent studies showed that also the females of O. pumilio 124 exhibit aggressive behaviour (Haase & Pröhl, 2002) particularly in the intensely used core 125 areas of their home ranges (Meuche, Linsenmair & Pröhl,
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