Temperature ISSN: 2332-8940 (Print) 2332-8959 (Online) Journal homepage: http://www.tandfonline.com/loi/ktmp20 Marsupials don't adjust their thermal energetics for life in an alpine environment Christine E. Cooper, Philip C. Withers, Andrew Hardie & Fritz Geiser To cite this article: Christine E. Cooper, Philip C. Withers, Andrew Hardie & Fritz Geiser (2016) Marsupials don't adjust their thermal energetics for life in an alpine environment, Temperature, 3:3, 484-498, DOI: 10.1080/23328940.2016.1171280 To link to this article: http://dx.doi.org/10.1080/23328940.2016.1171280 © 2016 The Author(s). Published with license by Taylor & Francis Group, LLC© 2016 Christine E. Cooper, Philip C. Withers, Andrew Hardie, and Fritz Giesser. Accepted author version posted online: 30 Mar 2016. Published online: 30 Mar 2016. Submit your article to this journal Article views: 220 View related articles View Crossmark data Citing articles: 1 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ktmp20 Download by: [University of Western Australia] Date: 02 November 2016, At: 23:12 TEMPERATURE 2016, VOL. 3, NO. 3, 484–498 http://dx.doi.org/10.1080/23328940.2016.1171280 RESEARCH PAPER Marsupials don’t adjust their thermal energetics for life in an alpine environment Christine E. Coopera,b, Philip C. Withersa,b, Andrew Hardiea, and Fritz Geiserc aDepartment of Environment and Agriculture, Curtin University, Bentley, Western Australia, Australia; bAnimal Biology M092, University of Western Australia, Crawley, Western Australia, Australia; cZoology, University of New England, Armidale, New South Wales, Australia ABSTRACT ARTICLE HISTORY Marsupials have relatively low body temperatures and metabolic rates, and are therefore considered Received 15 February 2016 to be maladapted for life in cold habitats such as alpine environments. We compared body Revised 20 March 2016 temperature, energetics and water loss as a function of ambient temperature for 4 Antechinus Accepted 23 March 2016 species, 2 from alpine habitats and 2 from low altitude habitats. Our results show that body KEYWORDS temperature, metabolic rate, evaporative water loss, thermal conductance and relative water alpine; Antechinus; body economy are markedly influenced by ambient temperature for each species, as expected for temperature; evaporative endothermic mammals. However, despite some species and individual differences, habitat (alpine water loss; marsupial; vs non-alpine) does not affect any of these physiological variables, which are consistent with those metabolism; thermal for other marsupials. Our study suggests that at least under the environmental conditions conductance experienced on the Australian continent, life in an alpine habitat does not require major physiological adjustments by small marsupials and that they are physiologically equipped to deal with sub-zero temperatures and winter snow cover. Introduction during winter appears to impact on their survival, and Marsupials generally have a low body temperature prevents their range expanding further northwards. (Tb) and basal metabolic rate (BMR) compared to pla- Opossums are reliant on urbanisation in cold cli- 5,14,15 cental mammals. Resting Tb is typically 2.5 C lower mates. However, as this species is recently for marsupial compared with placental mammals, and derived from neotropical didelphids,16 it is not unex- BMR of marsupials is on average only 70% of that of pected that Ta appears to restrict its northern equivalently-sized placental mammals.1-8 The conse- distribution. quences of this low BMR (and other physiological dif- In South America, several marsupials of the families ferences such as a lack of functional brown fat9) have Caenolestidae, Microbiotheriidae and Didelphidae been postulated to include inferior competition with inhabit high latitudes and/or altitudes with seasonally placental mammals (especially for species occupying cold conditions.5,14,17 For Lestodelphes and Dromi- high-energy niches), restricted reproductive rates, and ciops, the key to survival appears to be heterothermia; poor thermoregulatory ability.3,4,10-13 they use multiday torpor or hibernation to avoid sea- McNab3,4,14 suggested that the limited thermogenic sonal climatic extremes.18-24 Similarly, the small (57 g) and reproductive capacity of marsupials results in Australian mountain pygmy possum (Burramys par- their being excluded from energy-demanding environ- vus), a marsupial restricted to alpine habitats, also ments or niches, such as high altitudes or latitudes, uses hibernation during winter months, remaining and high energy food sources. Indeed, most marsu- inactive in sheltered subnivian hibernacula until more pials appear to spatially or temporally avoid cold win- favorable environmental conditions in spring.25,26 ter conditions at high altitudes and latitudes. The Despite the general spatial or temporal avoidance of North American opossum (Didelphis virginiana; harsh winter conditions by marsupials, some species »1000 g) is a well-known example of a marsupial of Australian marsupial do remain active in alpine with a cold (latitudinal) distribution limit; low Ta and subalpine habitats year-round, and must be able CONTACT Philip C. Withers [email protected] School of Animal Biology M092, University of Western Australia Crawley, Western Australia, Australia, 6009 Australia. © 2016 Christine E. Cooper, Philip C. Withers, Andrew Hardie, and Fritz Giesser, published with license by Taylor & Francis. This is an Open Access article distributed under the terms of the Creative Commons Attribution-Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which per- mits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The moral rights of the named author(s) have been asserted. TEMPERATURE 485 to physiologically cope with these harsh environmen- our study was to compare the physiology of alpine tal conditions. The Australian landmass does not have dusky and agile antechinus with low-elevation brown extreme altitudes or very high latitudes, with the high- antechinus (A. stuartii; 28 g) and yellow-footed ante- est point, Mt Kosciuszko, being 2,228 m above sea chinus (A. flavipes; 25g), to determine whether small level, and the most southerly point of Tasmania being marsupial species that are active in alpine and sub- only 433803700S. Nevertheless, parts of south-eastern alpine environments year round have an increased Australia, including the Australian Alps and the Cen- BMR or other physiological specializations to facilitate tral Highlands Bioregion of Tasmania, have alpine survival in cold habitats. and sub-alpine habitats that are characterized by sub- zero temperatures and snow cover for at least 4 months of the year. For example, the Australian Alps Methods are characterized by a mean annual temperature of 3 to 12C, minimum average monthly temperature of Wild antechinus were captured between April and June ¡7to¡0.4C, and snowfall for 4–6 months per using Elliott aluminum cage traps baited with rolled oats year.27 These alpine environments undoubtedly place and peanut butter, sometimes with attractants such as considerable physiological demands on the small honey, cat food and/or sardines. Eight yellow-footed mammals that inhabit them. antechinus (4 males, 4 females) were captured at Dryan- Examining the physiology of small marsupials that dra Woodland, Western Australia (32 4770S, 116 550E; are active year round in Australian alpine and sub- elevation 327 m) and 8 brown antechinus (6 males, 2 alpine habitats will address the question of whether females) were caught at Arthursleigh Station, near Maru- these alpine marsupial species have particular physio- lan, New South Wales (34 240S, 149 580E; elevation logical adaptations that enhance survival in cold, 642 m). Seven dusky antechinus (3 males, 4 females) harsh climates. For the larger species (e.g. common were measured, 2 from Werrikimbe National Park, New wombats, Vombatus ursinus, 26 kg) thermoregulatory South Wales (31 120S, 152 14’E; elevation 975 m), and demand is reduced considerably by a large body mass 5 from Smiggins Holes, Kosciuszko National Park, New and relatively thick insulating fur, along with behav- South Wales (36 240S, 148 250E; elevation 1680 m). ioral adaptations such as semi-fossoriality, that buffer Eight agile antechinus (6 females, 2 males) were also climatic extremes.28 Moderately-sized species such as caught near Smiggins Holes. Antechinus were housed in the Tasmanian devil (Sarcophilus harrisii; 10 kg) and large plastic crates and fed a diet of cat food, kangaroo quolls (Dasyurus spp., 525–5,500 g) presumably face a mince and live invertebrates (mealworms, crickets), with more substantial metabolic demand during the winter, ad lib.water. but they can maintain homeothermy and do not seem Oxygen consumption (VO2), carbon dioxide pro- 29 to reduce activity levels during cold periods. The duction (VCO2) and evaporative water loss (EWL) eastern quoll (780 g) does however have a significantly were measured using flow-through respirometry at higher BMR than other quolls, which approximates a ambient temperatures (Ta) ranging from 10 Cto general placental level of BMR.13 This elevated BMR 35C. Measurements commenced within a week of has been attributed to its cold habitat and the necessity capture, and the order of experimental temperatures of increased scope for thermogenesis.