Mamm Res (2015) 60:285–292 DOI 10.1007/s13364-015-0236-y ORIGINAL PAPER When prey provide more than food: mammalian predators appropriating the refugia of their prey William J. Zielinski 1 Received: 30 September 2014 /Accepted: 20 July 2015 /Published online: 31 July 2015 # Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland (outside the USA) 2015 Abstract Some mammalian predators acquire both food and predators) may play disproportionately important roles in their shelter from their prey, by eating them and using the refugia communities. the prey construct. I searched the literature for examples of predators that exhibit this behavior and summarize their taxo- Keywords Predator–prey . Dens . Herbivore . Behavior . nomic affiliations, relative sizes, and distributions. I hypothe- Habitat . Resting . Foraging sized that size ratios of species involved in this dynamic would be near 1.0, and that most of these interactions would occur at intermediate and high latitudes. Seventeen species of Introduction Carnivorans exploited at least 23 species of herbivores as food and for their refugia. Most of them (76.4 %) were in the Mammals require food and most require shelter, either to pro- Mustelidae; several small species of canids and a few tect them from predators or from thermal stress. Carnivorous herpestids were exceptions. Surprisingly, the average mammals are unique in that they subsist on mobile food predator/prey weight ratio was 10.51, but few species of pred- sources which, particularly if these sources are vertebrates, ators were more than ten times the weight of the prey whose may build their own refuges to help regulate their body tem- refugia they exploit. This may be why the long and thin peratures or to hide. Predators have the following options for Mustelines commonly exploit this habit. A number of preda- the source of their shelter; they can either (1) create their own tors appropriate the refugia of their key prey during winter refuge, (2) use a vegetation or a geologic feature (e.g., tree when their prey occupies thermally secure nests. Indeed, most hollow, rock crevice), or (3) use or appropriate the refuge of the predator–prey pairs that engage in this relationship oc- originally created by another species. Many mammalian car- cur in intermediate and high latitudes, though there may be a nivores use the first option and have the capability of digging reporting bias. Predators that depend on prey as food and for their own burrows or dens in soil or snow (e.g., European shelter, and whose fates are linked strongly to a few key prey badger, Meles meles [Dunwell and Killingley 1969]; species, may be particularly vulnerable to changes in climate American badger, Taxidea taxus [Lindzey 2003]; wolverine, that affect the subnivean habitats of their prey. Mammals that Gulo gulo [Copeland and Whitman 2003]). Others use natural create refugia that can be used by other species (among them cavities in trees or rocks (e.g., common genet, Genetta genetta [Lariviére and Calzada 2001]; ringtail, Bassariscus astutus [Gehrt 2003]; gray fox, Urocyon cinereoargenteus [Cypher Communicated by: Karol Zub 2003]). This review, however, is focused on understanding the frequency and circumstances that occur in the third case, * William J. Zielinski when mammalian predators appropriate the refuges of prey for [email protected] their own use, sometimes after having killed the occupant. Accounts of predators using the refugia of other species 1 Redwood Sciences Laboratory, USDA Forest Service, Pacific remain few, largely unquantified, and based primarily on ca- Southwest Research Station, 1700 Bayview Drive, sual sightings and reports (Murdoch et al. 2013). I sought to Arcata, CA 95521, USA highlight the prevalence of this behavior, since it has not been 286 Mamm Res (2015) 60:285–292 formally brought to the attention of the scientific community. resting pattern than reported here. Thus, I describe the In this paper, I review the species of carnivores that appear to taxonomic affiliation, geographic location, and relative have evolved a habit of preying on species that also provide body sizes of species that exhibit such a relationship them shelter when they co-opt their refuges (e.g., nests, bur- with the goal of identifying characteristics that may rows, dreys, dens). I review the taxonomic distribution of the make it easier to predict whether other species, that occurrence of this behavior and I hypothesize that size ratios are more poorly studied, may also be among them. I of species involved in this dynamic would be near 1.0. This is summarize the species of mammalian carnivores that expected for two reasons. First, to be able to physically occu- appropriate the refuges of their frequent prey and dis- py the refuge of a prey species, the predator must not be that cuss the variation in the behavior across taxa and some much larger than the prey. Second, to be able to subdue and implications for the conservation of these species under kill the prey species, the predator must not be that much small- changing environmental conditions. er than the prey. I also expected most of these interactions would occur at intermediate and high latitudes because these regions are colder in winter and a predator that usurps the refuge of their prey will also reap the thermal benefits. Materials and methods In cases where a predator kills and appropriates the refuge of its prey, the prey species represents an important habitat I reviewed the literature via internet searches (Google resource for the predator. This is distinct from the situation Scholar™, Web of Science™)usingthesearchterms that occurs when predators search the refugia of prey but do Bpredator prey,^ Bforaging,^ Bdens,^ Brest sites,^ and not appropriate the prey’s resting sites for their own or when a Brefugia,^ entered separately or in combination with predator occupies the refuge of an herbivore that is not includ- common and/or scientific names of individual taxa. I also ed in its diet. I exclude these circumstances from consider- searched my own extensive library of literature on carni- ation. For example, the Pallas’scat(Otocolobus manul)and vore ecology and consulted with colleagues to discover corsac fox (Vulpes corsac) use the burrow system of the information on species of carnivores that appropriate the Siberian marmot (Marmota sibirica) for resting, but do not refugia of their prey. I reviewed information about the diet prey on this species (Murdoch et al. 2010;Rossetal.2010a, of predators and resting habitats of predators and prey b). Similarly, non-trophic relationships occur between the red because knowledge of each was necessary to understand fox (Vulpes vulpes) and woodchucks (Marmota monax)and how these ecological characteristics are related. My goal between meerkats (Suricata suricatta) and Cape ground squir- was to reveal from the published literature as many rels (Xerus inauris)(Stanley1963;vanStaaden1994). instances of appropriation of prey refugia as possible. Carnivores can also use termitaries as refuges without eating Not all species have been studied sufficiently to know their termites (e.g., common dwarf mongoose, Helogale parvula habits in this respect and not all the literature may have [Rasa 1983]; striped weasel, Poecilogale albinucha been available for electronic searches. Thus, my discover- [Lariviére 2001]). The converse is also true: a termite-eating ies are but a sample of them, revealed using all the means Carnivoran, the aardwolf (Proteles cristatus), enlarges the at my disposal. burrow of the springhare (Pedetes capensis) to use as its The nature of the evidence necessary to determine if den, but does not prey upon it (Anderson and Richardson a species of predator kills and then appropriates its 2005). A number of other species of carnivores use abandoned refuge is usually circumstantial. For example, even dens (usually burrows in soil) of species that they do not hunt, though predator x is found using a refuge created by presumably to avoid the energetic cost of creating their own. its prey y, it rarely can be determined that x killed the Finally, I consider in this review primarily prey and predators particular individual of species y that created the species that have evolved together; exotic or invasive species specific refuge that is being occupied by the predator. are not generally considered. The predator may have searched the refuge and found it I predict that only species of predator that are relatively unoccupied and simply used it from that point forward. small, compared to their prey, may be able to exploit the use However, I assumed that when a predator occupies the of their prey’s refugia. Thus, I also report the weights of pred- refuge created by a prey species frequently enough to ators and prey, and their ratios. And, because this phenomenon be reported in the literature, and when that prey species may be more important to species of predators that require has been demonstrated to be an important food item in refugia in cold climates, I also report the latitudinal distribu- the predator’s diet, that the predator has developed a tion of pairs of species that have been described as engaging in unique foraging strategy that exploits the combined this dynamic. Because the literature is uneven on the depth of benefits of food and shelter provided by a prey species. published ecology and behavior for mammals, I assume that These species and their prey are reported here. All body there are more mammals that exhibit this unique foraging and weights were taken from a published database of Mamm Res (2015) 60:285–292 287 weights of late quaternary mammals, averaged between The second most common taxon reported appropriating the sexes (Smith et al. 2003). refugia of their prey are species within the subfamily Martinae (e.g., martens, sables).