Downloaded from rspb.royalsocietypublishing.org on October 26, 2014 Mammal survival at the Cretaceous−Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs Barry G. Lovegrove, Kerileigh D. Lobban and Danielle L. Levesque Proc. R. Soc. B 2014 281, 20141304, published 22 October 2014 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2014/10/21/rspb.2014.1304.DC1.h tml References This article cites 51 articles, 13 of which can be accessed free http://rspb.royalsocietypublishing.org/content/281/1796/20141304.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections ecology (1791 articles) evolution (1927 articles) physiology (146 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Downloaded from rspb.royalsocietypublishing.org on October 26, 2014 Mammal survival at the Cretaceous– Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs rspb.royalsocietypublishing.org Barry G. Lovegrove, Kerileigh D. Lobban and Danielle L. Levesque† School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa Research DLL, 0000-0003-0132-8094 Cite this article: Lovegrove BG, Lobban KD, Free-ranging common tenrecs, Tenrec ecaudatus, from sub-tropical Madagas- car, displayed long-term (nine months) hibernation which lacked any Levesque DL. 2014 Mammal survival at the evidence of periodic interbout arousals (IBAs). IBAs are the dominant fea- Cretaceous–Palaeogene boundary: metabolic ture of the mammalian hibernation phenotype and are thought to homeostasis in prolonged tropical hibernation periodically restore long-term ischaemia damage and/or metabolic imbal- in tenrecs. Proc. R. Soc. B 281: 20141304. ances (depletions and accumulations). However, the lack of IBAs in http://dx.doi.org/10.1098/rspb.2014.1304 tenrecs suggests no such pathology at hibernation Tbs . 228C. The long period of tropical hibernation that we report might explain how the ancestral placental mammal survived the global devastation that drove the dinosaurs and many other vertebrates to extinction at the Cretaceous–Palaeogene Received: 29 May 2014 boundary following a meteorite impact. The genetics and biochemistry of IBAs are of immense interest to biomedical researchers and space explora- Accepted: 22 September 2014 tion scientists, in the latter case, those envisioning a hibernating state in astronauts for deep space travel. Unravelling the physiological thresholds and temperature dependence of IBAs will provide new impetus to these research quests. Subject Areas: evolution, physiology, ecology Keywords: 1. Introduction mammals, hibernation, Cretaceous– At the Cretaceous–Palaeogene (K-Pg) boundary about 65.5 million years ago Palaeogene boundary, Madagascar, Tenrec (Ma) the ancestor of the placental mammals (Eutheria) survived the meteorite impact at Chicxulub, Mexico [1], which killed the non-avian dinosaurs and ecaudatus many other animals and plants [2–4]. A small (6–245 g), insectivorous ancestor inherited a tropical Earth, along with a few egg-laying mammals (Montremata), some marsupials (Metatheria) and a few lineages (e.g. Multitu- Author for correspondence: berculata) which went extinct during the Cenozoic [2]. Ecological release Barry G. Lovegrove from the vice grip which the dinosaurs held over Mesozoic mammals drove remarkably rapid evolutionary processes within several hundred thousand e-mail: [email protected] years of the extinction event [2]. Four new placental lineages (Xenarthra, Afrotheria, Laurasiatheria and Euarchontoglires) [2] appeared very suddenly, harbouring forms that displayed spectacular new morphological and physio- logical characteristics [5–8]. The long ca. 160 Myr stint of the nocturnal, small, insectivorous mammal was over, and gave way to the age of the mam- †Present address: Institute of Biodiversity and mals, the Cenozoic. Yet, no placental mammal would exist today had this ancestor not survived the global short- and long-term effects of the Chicxulub Environmental Conservation, Universiti Malaysia impact [3,4] and an Indian Ocean meteorite impact 40 000 years later [9]. How Sarawak, 94300 Kota Samarahan, Sarawak, did this placental ancestor, as well as the monotremes and the marsupials, Malaysia. survive when so many other vertebrate groups did not? There is growing debate about whether the ballistic impact ejecta that Electronic supplementary material is available re-entered the Earth’s atmosphere following the Chicxulub impact could have at http://dx.doi.org/10.1098/rspb.2014.1304 or generated an initial infrared heat pulse sufficient to ignite wildfires globally [10–15]. If global wildfires did occur, they would undoubtedly have been via http://rspb.royalsocietypublishing.org. responsible for the extermination of all mammals that could not seek safe refuge from the short- and long-term effects of the fires. Indeed, it is the & 2014 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from rspb.royalsocietypublishing.org on October 26, 2014 differential survival of vertebrates following the impact sub-adults of undetermined sex (312–467 g). All animals were 2 which currently provides one avenue of support for the wild- caught by hand, by walking the established trails in the area at rspb.royalsocietypublishing.org fires notion [3,11]. No large-sized, non-marine reptile, bird or night with local guides. Individuals were located, captured and mammal, that is, a vertebrate too large to seek refuge under- transported back to the research camp where they were housed ground, in tree cavities or underwater, survived the K-Pg in plastic containers lined with paper towels and provided with live insects and tinned sardines. Fifteen animals were surgi- boundary extinction event [3]. The predominant hypothesis cally implanted with a combination of radio transmitter and is that small mammals survived both the short- and long- body temperature data logger (see ‘Procedures’), and released term effects of the impact by hibernating in a safe refuge, back into the wild within several days of capture. Animals that typically, underground [3,16]. were not implanted were either small males (184–374 g) or It has been estimated that the long-term effects of the were individuals in poor condition heavily infected with internal impact lasted for a year or more [3,4]. However, in extant tro- parasites. The fate of the implanted and released tenrecs varied; pical placental mammals there is no known hibernation three were killed by feral dogs, two by unknown natural preda- Proc. R. Soc. B phenotype that would allow such long periods of hiber- tors, three by Malagasy boas (figure 1), three disappeared from nation. Long-term hibernation (more than six months) is the study area either through poaching or natural movement, typically associated with mammals which inhabit temperate, one hibernated for eight months in the same site, emerged and high-latitude and/or high-altitude, highly seasonal cold then left the study area, and three were excavated from their hibernacula after nine months of austral winter hibernation 281 environments [17]. For example, year-long hibernation has (see ‘Results’). These data confirm the high rates of mortality : 20141304 been reported in captive mountain pygmy possums (a at Ankarafantsika by feral dogs, snakes, natural predators and marsupial) [18]. Cold environments appeared in the Late poachers [35], as reported also for greater hedgehog tenrecs, Cenozoic only, and certainly did not exist at the K-Pg Setifer setosus [24]. boundary [19,20]. Indeed, until relatively recent reports of hibernation in Malagasy primates [21,22] and tenrecs [23,24], and in the echidna (a monotreme) from semi-tropical (b) Study site Queensland, Australia, [25,26], it was thought that hiber- The study was conducted over two rainy seasons, from Novem- nation was a physiological capacity limited to high latitude, ber 2009 to November 2011 in the Jardin Botanique A research area adjacent to the Ampijoroa Forestry Station in Ankarafantiska temperate mammals only [17]. National Park (168190 S, 468480 E), Madagascar. The study site has In this study, we report a plesiomorphic (ancestral) been described by Levesque et al. [37]. Detailed ambient tempera- capacity for long-term hibernation that exists in an extant, phy- ture (Ta) data were recorded at various locations throughout the logenetically basal, tropical placental mammal, the common study site using DS1922L Thermochron iButtons (Dallas Semicon- tenrec, Tenrec ecaudatus. The Tenrecidae belong to the superor- ductor, Dallas, TX, USA) programmed to record once every der Afrotheria, which includes elephants, dugongs and 30 min at a resolution of 0.06258C. DS1922L iButtons are inexpen- manatees, hyraxes, golden moles, elephant-shrews (sengis) sive data loggers that measure and record temperature at user- and the aardvark [27]. The tenrecs colonized Madagascar defined rates which are being used increasingly in physiological from Africa ca. 47 Ma and underwent spectacular adaptive and ecological research [38]. iButtons are encased in a stainless radiation on the island thereafter [28]. We measured the core steel cap and communicate with a host computing device through a serial