Journal of Mammalogy, 99(5):1128–1136, 2018 DOI:10.1093/jmammal/gyy100 Published online August 24, 2018 Trophic ecology of marsupial predators in arid Australia following reshaping of predator assemblages Downloaded from https://academic.oup.com/jmammal/article-abstract/99/5/1128/5078686 by University of New England user on 09 December 2018 CHRIS R. PAVEY,* CHRIS J. BURWELL, GERHARD KÖRTNER, AND FRITZ GEISER CSIRO Land and Water, PMB 44, Winnellie, Northern Territory 0822, Australia (CRP) Queensland Museum, P.O. Box 3300, South Brisbane, Queensland 4101, Australia (CJB) Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, New South Wales 2351, Australia (GK, FG) Environmental Futures Research Institute and Griffith School of Environment, Griffith University, Nathan, Queensland 4111, Australia (CJB) * Correspondent: [email protected] The extirpation of marsupial predators and their replacement by eutherian carnivores are likely to have cascading ecological impacts on the trophic structure of arid Australia. Here, we assessed the diet and characterized the trophic role of the 3 largest remaining carnivorous marsupials (< 200 g body mass) in arid Australia: crest- tailed mulgaras (Dasycercus cristicauda), kowaris (Dasyuroides byrnei), and brush-tailed mulgaras (Dasycercus blythi). The species show a high level of trophic connectivity; each is highly interactive, being predator or prey of numerous species across multiple phyla. The prey base of each of the predator species was broad and included vertebrates, invertebrates, and plants. Crest-tailed mulgaras consumed the most vertebrates including prey up to the size of the southern marsupial mole (Notoryctes typhlops). Kowaris consumed prey up to the size of the European rabbit (Oryctolagus cuniculus). Although capable of capturing or scavenging vertebrates, the diet of each species was dominated by arthropods < 2 g in body mass. Key words: arthropod, carnivore, extinction, niche, vertebrate A dramatic mammal extinction event of global magnitude, that (Johnson and Roff 1982) and is now confined to southwestern is ongoing, has unfolded across Australia over the past 200 years Australia (Glen et al. 2010). The red-tailed phascogale (body (Johnson 2006; Woinarski et al. 2015). A consequence of the mass: 38–68 g) also retracted to southwestern Australia over extinction event has been a changeover in mammalian preda- a similar time period (Kitchener 1981). In contrast, a suite of tors. In arid and semiarid Australia, an area that occupies 70% mid-range (body mass < 200 g) carnivorous marsupials, that of the continent (Warner 2004), this process has involved the are an order of magnitude smaller than the western quoll, extirpation of the largest carnivorous marsupial, the west- persisted in arid Australia during this extinction event. The ern quoll (Dasyurus geoffroii), and a mid-range carnivorous species are the crest-tailed mulgara (Dasycercus cristicauda; marsupial, the red-tailed phascogale (Phascogale calura). As 65–185 g), kowari (Dasyuroides byrnei; 70–175 g), and brush- these species contracted in range, the region was colonized by tailed mulgara (Dasycercus blythi; 60–110 g). These species 2 introduced eutherian carnivores, the red fox (Vulpes vulpes) occur sparsely over a broad geographic area and are the largest and feral house cat (Felis catus). The top mammalian preda- remaining marsupial predators in arid Australia (e.g., Morton tor, the Australian dingo (Canis dingo), has remained in arid 1982). The kowari occupies stony desert; the crest-tailed mul- Australia during this period and appears to have been present gara, sand ridges; whereas the brush-tailed mulgara occurs for over 3,000 years (Fillios et al. 2012). on sand plains and stony desert (Morton 1982; Van Dyck and At the time of European settlement, the western quoll Strahan 2008; Pavey et al. 2011). The kowari and crest-tailed was the largest carnivorous marsupial (Dasyuromorphia: mulgara are listed nationally as vulnerable under Australia’s Dasyuridae) in arid Australia (body mass: 615–2,185 g); Environment Protection and Biodiversity Conservation Act however, it was extirpated from the arid zone in the 1960s of 1999. © 2018 American Society of Mammalogists, www.mammalogy.org 1128 PAVEY ET AL.—TROPHIC ECOLOGY OF ARID MARSUPIALS 1129 There is limited information on the trophic ecology of mid- Dietary analysis.—We broadly followed the methods out- range carnivorous marsupials in arid Australia and it is not lined in Pavey et al. (2009) for fecal analysis. Fifty scats were known whether these species overlap in diet and prey prefer- analyzed for each species except crest-tailed mulgaras (46 ences. This knowledge is important to gain an understanding scats). We placed each scat in a petri dish and added 4–5 drops of their role in the functioning of arid ecosystems in Australia. of 10% KOH directly to it, before teasing it apart with fine dis- Downloaded from https://academic.oup.com/jmammal/article-abstract/99/5/1128/5078686 by University of New England user on 09 December 2018 It is also needed to inform management options in the likely secting needles and covering it in 70% ethanol. We systemati- event of the reintroduction of the western quoll. The quoll cally searched each scat for identifiable material under a low has been reintroduced to a number of temperate and semiarid power (6.4 to 40 magnification) binocular microscope. locations within its former range with varying levels of suc- Prey fragments were identified to the lowest taxonomic level cess (Morris et al. 2003; Commonwealth of Australia 2015) possible. Material was identified by reference to collections in and attention has expanded to potentially return the species to the Queensland Museum, Brisbane. Mammal hair was collected arid Australia. A sound understanding of the trophic ecology and sent for specialist identification (Barbara Triggs, Euroa, of the extant mid-range carnivorous marsupials will assist in Victoria, Australia). The volume of each prey item in each scat identifying potential negative impacts from reintroductions of was calculated by spreading all the identifiable fragments in a quolls. petri dish with graph paper underneath and estimating for each Here, we quantify the diet of a population of each of the 3 prey item the space (area) occupied by its fragments, including mid-range carnivorous marsupials and characterize the trophic exoskeleton, hair, scales, and feathers. Material was assigned role of these predators in arid Australian ecosystems. We pre- to a taxon only if it clearly belonged to that taxon. A single scat dict that these 3 species will have broad diets because these could contain material of a species and of the genus to which marsupial predators are resident with relatively stable popu- the species belonged; it was not concluded that all material in lations in arid regions through peaks and troughs of resource the scat belonged to a species even if some identifiable parts availability (Masters 1998; Pavey et al. 2011; Masters and were present in the scat. Dickman 2012; Körtner et al. 2016), whereas other arid verte- Percent volume was estimated to the nearest 5%. Taxa that brate species exhibit marked changes in occurrence and popu- contributed less than 2.5% were not included in percent volume lation size (e.g., Pavey et al. 2008a, 2008b). We consider that estimates for a given scat. this ability to persist is enhanced by a broad diet. Analysis of data.—We calculated the mean percent volume of each prey item in the diet for each species. We also cal- culated the frequency of occurrence (also known as percent MATERIALS AND METHODS occurrence or percent frequency of occurrence), which is the Study sites.—Scats of each species were collected from indi- number of scats containing a specific prey taxon divided by viduals captured in traps from populations that were the focus the total number of scats analyzed. We tested for sampling of research projects undertaken from 2007 to 2010. Trapping completeness by generating sample-based diet component (and all other procedures) was undertaken in accordance with accumulation curves (1,000 randomizations) using the dietary the American Society of Mammalogists guidelines (Sikes et al. items in Table 1 run in EstimateS version 9.1.0 (Colwell 2013). 2016), and was approved by the University of New England We chose the 1st-order Jackknife richness estimator for this Animal Ethics Committee and Charles Darwin University purpose. The percentage of dietary sampling completeness Animal Ethics Committee. was calculated for each species as Sobs/Sest × 100, where Sobs is The research took place during the low (or “bust”) phase of the number of dietary categories observed, and Sest is the num- small mammal population cycles in the study areas. This phase ber of dietary categories estimated. features the most typical environmental conditions that the We calculated dietary breadth for each species using the marsupial predators experience and coincides with periods of percent volume dietary data. Levins’ standardized formula for low rainfall (e.g., Pavey and Nano 2013). The low phase can niche breadth (Krebs 1999) was used to calculate diet breadth: 2 occupy up to 8.5 years of each 10-year period in our study sys- BA = (1/∑pi ) − 1/n − 1, where pi = proportion of occurrence tem (Pavey et al. 2014). of each prey category in the predator’s diet; and n = number We collected scats of the 2 mulgara species during a of prey categories in the predator’s diet. BA ranges from 0 long-term monitoring project at Andado Station (25°41′S, to 1, where a value close to 0 represents a narrow niche and 135°29′E), southeast Northern Territory (Pavey et al. 2014). one close to 1, a broad niche. The percent volume data were Brush-tailed mulgara scats were collected from May 2008 to converted to proportions for the analysis. To calculate dietary December 2010 and crest-tailed mulgara scats were collected breath, we used data at an ordinal level except that termites from November 2007 to December 2010.