Torpor Patterns in Desert Hedgehogs (Paraechinus Aethiopicus) Represent Another New Point Along a Thermoregulatory Continuum
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445 Torpor Patterns in Desert Hedgehogs (Paraechinus aethiopicus) Represent Another New Point along a Thermoregulatory Continuum Justin G. Boyles1,* We suggest that this family (Erinaceidae) and order (Eulipo- Nigel C. Bennett2,3 typhla) may be important for understanding the evolution of Osama B. Mohammed2 thermoregulatory patterns among Laurasiatheria and mammals Abdulaziz N. Alagaili2 in general. 1Cooperative Wildlife Research Laboratory, Department of Zoology, Southern Illinois University, Carbondale, Illinois; Keywords: body temperature, Ethiopian hedgehog, Eulipo- 2King Saud University Mammals Research Chair, Department typhla, heterothermy, hibernation. of Zoology, College of Science, King Saud University, PO Box 2455, Riyadh 11451, Saudi Arabia; 3Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa Introduction Accepted 2/13/2017; Electronically Published 4/12/2017 Describing variation in thermoregulatory and body tempera- — ture (Tb) patterns and determining the distribution both phylo- genetically and geographically—of those patterns in mammals ABSTRACT and birds is vital to understanding the evolutionary history of Documenting variation in thermoregulatory patterns across endothermy. Of special interest is how various derivations of phylogenetically and geographically diverse taxa is key to un- heterothermy relate to the evolutionary history of endothermy. derstanding the evolution of endothermy and heterothermy in Patterns of heterothermy have often been considered distinct birds and mammals. We recorded body temperature (Tb)in (Geiser 1998), with daily heterothermy and hibernation (seasonal free-ranging desert hedgehogs (Paraechinus aethiopicus)across heterothermy) differentiated by parameters including length of ’ 7– three seasons in the deserts of Saudi Arabia. Modal Tb s(35 torpor bouts and metabolic rate during torpor (Geiser and Ruf 36.57C) were slightly below normal for mammals but still warmer 1995). Increased interest in the topic and advances in technology than those of other hedgehogs. The single maximum Tb recorded have led to an increase in research on species from tropical, sub- 7 ’ was 39.2 C,whichiscoolerthanmaximumTb s recorded in tropical, and desert regions, and exceptions that fall in-between most desert mammals. Desert hedgehogs commonly used tor- the normal classifications of heterothermy are common enough por during winter and spring but never during summer. Torpor (Lovegrove et al. 2001; Lovegrove and Genin 2008; Geiser and bouts occurred frequently but irregularly, and most lasted less Mzilikazi 2011; Geiser and Martin 2013) that many researchers than 24 h. Unlike daily heterotherms, desert hedgehogs did now view the metabolic plasticity between normothermy and occasionally remain torpid for more than 24 h, including one hibernation as a continuum (Canale et al. 2012; Boyles et al. 2013; bout of 101 h. Body temperatures during torpor were often van Breukelen and Martin 2015) arising from ancestral hetero- within 27–37C of ambient temperature; however, we never re- thermy (Lovegrove 2012a). corded repeated boutsof long, predictable torporpunctuated by Differentiating between the two competing views of hetero- brief arousal periods similar to those common among seasonal thermy (distinct categories vs. a continuum) will become easier hibernators. Thus, desert hedgehogs can be included on the as more data on Tb of phylogenetically and geographically di- ever-growing list of species that display torpor patterns inter- verse species become available. One such phylogenetically im- mediate to traditionally defined hibernators and daily hetero- portant order is the Eulipotyphla (solenodons, shrews, moles, therms. Extant hedgehogs are a recent radiation within an an- hedgehogs, and moonrats), which occupy an interesting (albeit cient family, and the intermediate thermoregulatory pattern contentious) position in the mammalian phylogeny (Mouchaty displayed by desert hedgehogs is unlike the deeper and more et al. 2000; Douady et al. 2002). They are most commonly placed regular torpor seen in other hedgehogs, suggesting that this may sister to the rest of Laurasiatheria (Douady et al. 2002; Bininda- be a derived—as opposed to ancestral—trait in this subfamily. Emonds et al. 2007), diverging 75–85 million years ago (Douady and Douzery 2003; Hallström and Janke 2010). The Eulipo- typhla have been singled out as important in understanding the *Corresponding author; e-mail: [email protected]. evolution of heterothermy in mammals because of their early Physiological and Biochemical Zoology 90(4):445–452. 2017. q 2017 by The divergence from the other laurasiatherians (Lovegrove 2012b). University of Chicago. All rights reserved. 1522-2152/2017/9004-6169$15.00. Among the Eulipotyphla, the thermal physiology of hedge- DOI: 10.1086/691542 hogs (subfamily Erinaceinae) has long interested researchers 446 J.G.Boyles,N.C.Bennett,O.B.Mohammed,andA.N.Alagaili (Dmi’el and Schwarz 1984; Soivio et al. 1968). Hedgehogs typi- first collection period was in summer 2013 (June 2013). The 7 7 cally maintain normothermic Tb between 33 and 35 C (Shkolnik second collection period was in winter 2013–2014 (November and Schmidt-Nielsen 1976; Fowler and Racey 1990; Król 1994; 2013). We captured 20 animals in each season. Hallam and Mzilikazi 2011), which is intermediate between We temporarily housed the hedgehogs in an animal facility monotremes, metatherians, and more basal placental mammals at the Department of Zoology of King Saud University in Ri- 7– 7 (Tb of 30 33 C; Grant 1983; Grigg et al. 2003; Nicol and An- yadh. We used temperature-sensitive data loggers set to re- derson 2006; Lovegrove and Genin 2008) and the more typical cord at 1-h intervals (0.06257C resolution, iButtons, DS1922L, 7– 7 mammalian Tb of 37 38 C. Even among the Eulipotyphla, hedge- 4.2gwithwax,MaximSemiconductors,Dallas)tomeasurecoreTb. hogs display unusually low Tb (Whittowetal.1977;Campbell We did not have proper equipment available to fully calibrate et al. 1999). While a large body of literature exists on thermo- data loggers. Previous experience with this model of data logger regulation of hedgehogs, relatively little work has been pub- indicates that most are accurate within values claimed by the 7 lished on Tb patterns of this taxon in the wild, especially in arid manufacturer (0.5 C) and that precision within a batch is high environments. Laboratory and semicaptive studies suggest that (J. G. Boyles, personal observation). However, a weakness of this the European hedgehog (Erinaceus europaeus) probably under- model is that a small proportion of them deviate outside these goes the longest and deepest torpor bouts among hedgehogs values. Therefore, before implanting the data loggers, we com- (Dmi’el and Schwarz 1984; Soivio et al. 1968; Fowler and Racey pared their recorded temperatures to measured air temperatures 1990; Webb and Ellison 1998), but other hedgehog species also to remove any data loggers with a clear offset. Thus, we are fi 5 7 display relatively long torpor bouts characterized by low Tb (Hal- con dent that our measurements are within 0.5 C of actual Tb lam and Mzilikazi 2011; Mouhoub-Sayah et al. 2012). The four values.We then coated the data loggerswith biologically inert wax species for which Tb data are available come from a variety of and had them implanted intraperitoneally by a licensed veteri- climates (temperature and subtropical) and habitats (woodlands narian following standard procedures. The veterinarian im- and grasslands), and all use torpor. planted data loggers after anesthetizing animals with isoflurane We recorded Tb of free-ranging desert hedgehogs (Paraechi- and sutured the incision with absorbable catgut. Animals were nus aethiopicus) across three seasons in a harsh desert environ- given a long-acting, broad-spectrum antibiotic (Oxytetracy- ment. Desert hedgehogs are unusual among the hedgehogs be- cline, Pfizer) to minimize chances of postsurgery infection and cause of their adaptations to extremely arid environments; thus, were held for at least 7 d to ensure recovery from surgeries. Fi- their thermoregulation is likely to be unusual as well. Given that nally, to facilitate recapture, we clipped a few spines and glued heterothermy seems ubiquitous among the hedgehogs, we ex- (Torbot Liquid Bonding Cement, Torbot) radio transmitters (RI- pected heterothermy in desert hedgehogs as well. However, given 2B, 10 g, Holohil Systems) to the dorsal skin. Combined, the data the unusual ecology of this species relative to other hedgehogs, we logger and transmitter were well below 5% body mass of all in- had no a priori expectations about the form of heterothermy. dividuals. We released the animals in the same area where we had captured them and attempted to recapture them approx- Methods imately 2 mo after the first capture period and 5 mo after the second capture period. The first period was completed wholly Study Species during summer. The second period began in early winter and The desert hedgehog (150–600 g) is an arid-adapted insectivore ended in late spring/early summer. Recapture was lower during found throughout the nonmountainous regions of the Arabian summer because hedgehogs more commonly left the area or Peninsula and in extreme northern Africa. Relatively little is were killed on roads. We euthanized animals using ether to re- known about the natural history, behavior, and ecology of this trieve data loggers. These capture procedures were conducted