Can heterothermy facilitate the colonization of new

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Mammal Review ISSN 0305-1838

REVIEW

Can heterothermy facilitate the colonization of new habitats? Julia NOWACK* Department of Animal Ecology and Conservation, Biocentre Grindel, University of Hamburg, Martin-Luther-King Platz 3, 20146 Hamburg, Germany, and Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW 2351, Australia. E-mail: [email protected] Kathrin H. DAUSMANN Department of Animal Ecology and Conservation, Biocentre Grindel, University of Hamburg, Martin-Luther-King Platz 3, 20146 Hamburg, Germany. E-mail: [email protected]

Keywords colonization, heterothermy, Madagascar, rafting, reproduction *Correspondence author. Submitted: 12 October 2014 Returned for revision: 17 December 2014 Revision accepted: 14 January 2015 Editor: KH doi:10.1111/mam.12037

ABSTRACT 1. Increasing evidence shows that torpor in mammals is not only an effective adaptation for surviving predictable seasonal harsh conditions but is also employed as a response to acute emergency situations. This finding leads to the hypothesis that the ability to become heterothermic can also facilitate the colonization of new habitats, when mammals have to cross unsuitable, fragmented and/or food-scarce landscapes. This hypothesis was first suggested in the context of the colonization of Madagascar, and it has never been evaluated in detail. In this review, we discuss the potential of heterothermy to affect colonization possibilities in general and the colonization of Madagascar in particular. 2. We list several points supporting the hypothesis and contend that, unless colonization events coincidentally take place during the hibernation period, spontaneous daily torpor is probably more instrumental for surviving unexpected and severe conditions on a raft or when crossing harsh landscapes than seasonally occurring hibernation. We further propose that torpor can positively affect the establishment of a founder population by enabling reproductive arrest phases until conditions improve. Moreover, if viable offspring are born after arrival, this might abolish the absolute necessity of encountering individuals of the opposite sex. 3. Altogether, it seems therefore consequential that heterothermic mammals with the ability to enter daily torpor are the most likely to arrive in a new habitat in a body condition that allows successful settlement and reproduction. 4. Together with the finding that all recent taxa of terrestrial, non-volant Malagasy mammals or their close relatives include representatives that use heterothermy, this suggests that torpor might indeed have facilitated the colonization of Madagascar.

Heterothermy, the ability of some mammalian and other animal species to lower their energy requirements drastically during torpor (daily torpor or hibernation) by a reduction of metabolic rate and a concurring drop in body temperature, is traditionally seen as an effective adaptation

to predictable seasonal bottlenecks of unproductive, usually cold periods (Lovegrove 2000, Heldmaier et al. 2004). However, over recent years, it became apparent that torpor episodes can also be employed as a response to acute emergency situations and not only as a regular strategy to overcome seasonal bottlenecks (e.g. by the sugar glider Petaurus breviceps: Christian & Geiser 2007, and the African lesser

Mammal Review (2015) © 2015 The Mammal Society and John Wiley & Sons Ltd

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INTRODUCTION

Can heterothermy facilitate colonization events?

bushbaby Galago moholi: Nowack et al. 2010, Nowack et al. 2013b), suggesting that heterothermy can be advantageous for survival during natural disasters that are usually unpredictable. This new finding raises the question of whether the ability to become torpid can also facilitate the colonization of new habitats, when animals have to cross unsuitable, fragmented and/or food-scarce landscapes, and survive inclement weather conditions, by lowering their need for food and water.

THE IDEA BEHIND THE HYPOTHESIS: THE MYSTERY OF MADAGASCAR’S COLONIZATION The hypothesis that physiological adaptations for energy saving might have facilitated a colonization process was first suggested in the context of the colonization of Madagascar by mammals (Martin 1972, Kappeler 2000). Madagascar is the fourth largest island in the world (∼590000 km2), but its fauna is comparatively impoverished and includes only a few extant, non-volant terrestrial mammalian taxa, mainly comprising rodents, carnivores, tenrecs and lemurs (Goodman et al. 2003). Madagascar broke away from what is today the African mainland, along with land that would eventually become India, Australia and Antarctica, 165– 121 million years ago (mya; Rabinowitz et al. 1983), and became an island 88 mya. At this time, no placental mammals were present on the island (Krause 2001, 2010, Krause et al. 2006); thus, ancestors of all Malagasy mammals must have immigrated to the island at some point. Molecular data have confirmed that the closest relatives of the Malagasy mammals occur on the African mainland (Yoder et al. 1996, 2003, Poux et al. 2005), which has been separated from Madagascar by the Mozambique Channel for about 120 million years. The current minimum distance between the land masses of about 430 km (Rabinowitz et al. 1983, Ali & Aitchison 2008) represents an apparently insurmountable barrier for non-volant, terrestrial species (Stankiewicz et al. 2006). Three possible scenarios to explain the presence of terrestrial mammals on Madagascar have been suggested: 1) a temporary reduction in sea level (e.g. Jolly et al. 1984); 2) the presence of a temporary land bridge (e.g. McCall 1997); and 3) rafting on drifting vegetation (e.g. Simpson 1940, Jolly et al. 1984, Kappeler 2000, Ali & Huber 2010, Samonds et al. 2012). However, Simpson (1940) noted that only the rafting hypothesis can explain the comparatively small number of only small-bodied mammalian taxa that successfully colonized Madagascar; the other two scenarios should have led to a greater diversity of African mammals of all body sizes (Kappeler 2000). Moreover, Haq et al. (1987) pointed out that most of the Mozambique Channel is >2000 m deep, so that a reduction in sea level sufficient to 2

J. Nowack and K. H. Dausmann

allow animals to cross the channel, perhaps by wading, is unlikely. The largest eustatic reduction in sea level since the Palaeocene has probably only amounted to a maximum of a few hundred meters (Haq et al. 1987), and even a greater reduction in sea level would have still necessitated overwater dispersal between islands. The existence of a land bridge is equally doubtful. First of all, a number of authors have pointed out that this hypothesis is not supported by geological data (Rabinowitz & Woods 2006, Ali & Krause 2011), and secondly, even if a land bridge existed, it would have been likely to contain gaps that would still have necessitated over-water dispersal (Ali & Huber 2010). Another important point conflicting with both hypotheses is that the estimated dispersal times argue against a synchronous dispersal of the different taxa, as would be the case with a transient land bridge or a reduction in sea level, but indicate three to four independent colonization events over a time span of about 56 million years (between 14 and 70 mya; Poux et al. 2005). The rafting hypothesis, on the other hand, has often been perceived as implausible because today’s currents in the Mozambique Channel flow from Africa towards Antarctica and not to Madagascar (Stankiewicz et al. 2006). However, a recent study has established that during the Eocene, the currents did indeed travel towards Madagascar, especially in January, when cyclones, and thus the break-off of larger rafts of matted vegetation, are most likely in the area (Ali & Huber 2010). With flow rates as fast as 20 m-s, travel durations of less than four weeks would have been possible between Africa and Madagascar (Ali & Huber 2010). However, even a journey of a few weeks without food or with only very limited access to food and, even more importantly, without fresh water would be more than challenging for small euthermic mammals with their relatively high energy and water demands and low fat stores. This line of reasoning led to the original suggestion that heterothermy might have played an important role in the colonization of the island (Martin 1972, Kappeler 2000). In this review, we integrate new insights on energy-saving strategies and the employment of heterothermy in a variety of mammalian species throughout the world, and re-evaluate the potential of this physiological strategy to affect the probability of colonization on a raft across the ocean or across unhospitable landscapes in general, and the colonization of Madagascar in particular.

EVIDENCE OF COLONIZATION EVENTS VIA RAFTING In the context of species’ dispersal, the puzzle of island colonization in particular has intrigued scientists for decades. In particular, islands of volcanic origin have provoked many questions regarding the settlement of non-volant, terrestrial species, although any inhospitable landscape can act as a Mammal Review (2015) © 2015 The Mammal Society and John Wiley & Sons Ltd


barrier for the colonization of enclosed habitat patches. Oceanic dispersal is assumed for amphibians (Measey et al. 2007), a number of reptiles (Censky et al. 1998, Calsbeek & Smith 2003) and some mammals (e.g. Malagasy mammals: Simpson 1940; platyrrhine monkeys in South America: Schrago & Russo 2003). DNA sequencing of two frog species found on Mayotte island in the Comoro Archipelago (Indian Ocean) has provided evidence that overseas dispersal of amphibians takes place, even though amphibians were thought to be unable to disperse over ocean barriers because they do not tolerate the osmotic stress of salt water (Vences et al. 2003). Analogous to the discussuion about the colonization of Madagascar, the origin of New World monkeys (Platyrrhini) in South America has been extensively debated, and overwater dispersal seems to be the most likely scenario (Houle 1999). Although Houle (1999) discussed the survival chances of protoplatyrrhine monkeys during a journey by raft from Africa to South America without available drinking water, the option of heterothermy has not been considered. To date, there is no indication of heterothermy in platyrrhine monkeys; however, torpor is considered likely to occur in tarsiers, which belong to the same suborder (Lovegrove 2012b, Lovegrove et al. 2014a). To our knowledge, there are no direct observations of any mammalian species successfully colonizing an island through rafting. Due to their generally lower metabolic costs, successful rafting seems more likely for ectothermic animals, and indeed, the only proven colonization events via rafting have been described for reptiles. A successful raft has, for example, been reported for the green iguana Iguana iguana in the Caribbean (Censky et al. 1998). This, in turn, lends indirect support for the hypothesis that heterothermic mammals with the ability to lower their energy requirements are more likely than homeothermic mammals to arrive in a new habitat in a body condition that allows successful settlement and reproduction.


Torpor is usually employed in response to acute or potential energy or water limitation (Lovegrove 2000), and a number of mammalian species are known to increase torpor use during the winter, in response to reduced food availability, bad weather (reduced foraging) or droughts (Körtner & Geiser 2000, Turbill et al. 2003, Turner et al. 2012). Geiser and Brigham (2012) pointed out that torpor not only enhances survival during phases of limited food and water availability but also serves a number of other functions. For example, it has been suggested that daily torpor allows heterothermic species to maintain their territories during winter (Körtner et al. 2000, Geiser & Brigham 2012) when

many homeothermic species have to abandon their habitats and migrate to warmer regions, and hibernating species have to retreat into their hibernacula. Daily torpor further allows migrating species to enhance fat storage prior to the migration phase and reduces predation pressure, by allowing animals to remain inactive and hidden (Karpanty & Wright 2007, Geiser & Brigham 2012). Generally, torpor facilitates a ‘slow-paced’ life history tactic by increasing life spans and enabling animals to spread their production of offspring over more reproductive efforts, thereby improving the survival of their progeny (Turbill et al. 2011, Ruf et al. 2012). This theory is supported by findings in the edible dormouse Glis glis. This species undergoes extended periods of inactivity during summer, despite food being available, presumably as a mechanism to avoid predation in nonbreeding years (Bieber & Ruf 2009), and indeed, it has been shown that survival rates are highest during the hibernation season (Lebl et al. 2011). Similarly, Blanco and Godfrey (2013) showed that life histories of dwarf lemurs Cheirogaleus spp. vary in accordance with their use of energy-saving strategies. Some authors even argue that heterothermic species are less often subject to extinction than homeothermic species (Geiser & Turbill 2009). Besides the common ‘seasonal heterothermy’, recent examples, such as the use of emergency torpor in the African lesser bushbaby, have shown that heterothermy can also be employed in response to emergency situations. The African lesser bushbaby is physiologically capable of employing daily torpor but does so only under adverse conditions and instead stays homeothermic whenever possible. In this species, torpor has only been found in very few individuals, only on singular occasions, and some individuals showed unusual difficulties in rewarming to normothermic levels on cold days (Nowack et al. 2010, 2013c). The African lesser bushbaby possesses brown adipose tissue and the ability to produce heat via non-shivering thermogenesis (Nowack et al. 2013a), suggesting that rewarming difficulties may be related to low energy reserves. Individuals seem to enter torpor when their internal energy stores are already depleted, and have to rely on exogenous passive heating to reach sufficient body temperature to become active again (Nowack et al. 2013a,b). The ability to use torpor as a last resort strategy may indeed increase the chance of survival when animals are faced with non-seasonal food and water scarcity during the dispersal phase, supporting the notion that heterothermy also facilitates the colonization of new habitats. However, one has to keep in mind that hibernation and daily torpor might not be equally helpful for the survival of unexpected, severe conditions. Although from a functional point of view daily torpor and hibernation are to a large extent similar, they are distinct expressions of heterothermy (Geiser & Martin 2013). Daily torpor can be employed


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CAN HETEROTHERMY FACILITATE THE COLONIZATION OF NEW HABITATS?


seasonally but can also be used fairly spontaneously without restriction to specific seasons. Indeed, daily torpor may be expressed opportunistically throughout most of the year in a number of daily heterotherms (white-footed mouse Peromyscus leucopus: Lynch et al. 1978; African woodland dormouse Graphiurus murinus: Webb & Skinner 1996; sugar glider: Körtner & Geiser 2000). Hibernation, on the other hand, is an adaptation to seasonal bottlenecks that cannot be entered without extensive preparations. For example, hibernating species have to store substantial amounts of energy reserves (usually in the form of body fat) to survive the months without energy intake before the start of the hibernation season (Carey et al. 2003). However, a few hibernating species also show short to prolonged torpor bouts (up to three days) during the hibernation season (e.g. the reddish-grey mouse lemur Microcebus griseorufus; Kobbe et al. 2011) or opportunistically throughout the year (e.g. the edible dormouse; Wilz & Heldmaier 2000; we are not referring to extended hibernation into summer but solely to opportunistic use of torpor bouts). Unless rafting events coincidentally take place during the hibernation season, daily or opportunistic torpor is probably more instrumental than seasonal hibernation for surviving unexpected, harsh conditions or for lowering energy expenditure during a journey through harsh landscapes or on a raft, on the way to a new habitat. On the other hand, hibernation might be helpful once an animal arrives in a new habitat as it may enable the colonization of seasonally unsuitable habitats.

DISPERSAL OF PREGNANT FEMALES Successful colonization requires the foundation of a new population, and for that, more than one individual, or at least one pregnant female, is needed. A scenario where several individuals migrate to a new habitat together, or are washed into a river and later into the ocean on a raft, is more likely for highly social animals but doubtful for solitary species, such as most carnivores. But how could a pregnant female mammal survive a dispersal journey of a few weeks through unsuitable habitats, possibly with low food and water availability? During pregnancy, nutritional and energetic demands are even higher than during nonreproductive phases, and at least for some rodents, heterothermy and reproduction have been found to be mutually exclusive (e.g. Darrow et al. 1988, Fietz et al. 2004). Similarly, Tøien et al. (2011) described a pregnant female black bear Ursus americanus that only entered hibernation after she had lost her pup. The peculiarity of the Malagasy lesser hedgehog tenrec Echinops telfairi to abandon its extensive heterothermy only during breeding also points in this direction (Poppitt et al. 1994, Lovegrove & Génin 2008, Wein 2010). In contrast, daily torpor during 4


reproduction has been reported in pregnant monotremes (Morrow & Nicol 2009), pregnant and lactating marsupials (Geiser & Masters 1994), bats (e.g. Willis et al. 2006, Daniel et al. 2010), primates under food restriction (Canale et al. 2012), and even incubating hummingbirds (Vleck 1981). The ultimate causes and benefits of torpor during pregnancy are still being discussed, but, in the case of the hoary bat Lasiurus cinereus, daily torpor seems to be employed to delay parturition during spring storms until conditions improve (Willis et al. 2006). For similar reasons, torpor can be used to prolong sperm storage by females (suggested for bats, Geiser & Brigham 2012). Prolonged sperm storage as well as delayed parturition can be considered beneficial if seen in the context of colonization. In both cases, torpor would allow a female to start a new population immediately after arrival and without the pressing need for an individual of the opposite sex. In general, torpor during reproduction seems to be employed by mammalian species that spread their reproductive effort and the associated energetic costs over a longer time period. This may not only further slow the rate of foetal development but may also increase the probability of offspring survival (Willis et al. 2006). In the case of the grey mouse lemur Microcebus murinus, however, daily torpor during pregnancy and lactation is only employed in acute emergencies (e.g. if food is restricted by 40–80%) and is insufficient to compensate for greater food shortages during lactation, leading to weight loss of the mother and a lack of increase in the pup’s body mass. Accordingly, Microcebus females avoid torpor during gestation and lactation, giving priority to foetal growth up to a critical level of food shortage (Canale et al. 2012). It can be assumed that heterothermy during breeding can be employed as a last resort strategy not only by lemurs but probably also by other heterothermic mammals in similar situations. For example, daily torpor during pregnancy was suggested as an explanation for variations in gestation periods in the largeeared tenrec Geogale aurita (Stephenson & Racey 1993a).

COULD HETEROTHERMY HAVE ENABLED RAFTING TO MADAGASCAR? Torpor has been found in a number of lemur and tenrec species on Madagascar, which had led to the original suggestion that this physiological adaptation might have played an important role in the colonization of the island (Martin 1972, Kappeler 2000). So far, the focus of these considerations has been on one specific group, the lemurs. It was argued that the estimated size of the Lemuriformes and lemuroid ancestor (∼2 kg) is well outside the range of most mammals employing heterothermy and that it is therefore unlikely that the ancestor of today’s lemurs was able to become torpid (Masters et al. 2007). Heterothermy is Mammal Review (2015) © 2015 The Mammal Society and John Wiley & Sons Ltd



Table 1. Malagasy mammalian species for which heterothermy has been reported; H, hibernation; n.k., not known; T, daily torpor Family and species Lemuridae Cheirogaleus Cheirogaleus medius Cheirogaleus major Cheirogaleus crossleyi Cheirogaleus sibreei Microcebus Microcebus murinus Microcebus griseorufus Microcebus berthae* Microcebus rufus Microcebus ravelobensis Mirza Mirza coquereli Allocebus Allocebus trichotis Tenrecidae Echinops Echinops telfairi Hemicentetes Hemicentetes nigriceps Hemicentetes semispinosus Geogale Geogale aurita Tenrec Tenrec ecaudatus Microgale Microgale dobsoni Microgale talazaci Setifer Setifer setosus

Common name

T/H

Citation

Fat-tailed dwarf lemur Greater dwarf lemur Furry-eared dwarf lemur Sibree’s dwarf lemur

H H H H

Dausmann et al. (2004) Lahann (2007) Blanco and Rahalinarivo (2010) Blanco et al. (2013)

Grey mouse lemur Reddish-grey mouse lemur Madame Berthe’s mouse lemur Brown mouse lemur Grey brown mouse lemur

T/H T/H T T/H T

Schmid (2000), Schmid and Speakman (2000) Kobbe and Dausmann (2009), Kobbe et al. (2011) Ortmann et al. (1997), Schmid et al. (2000) Atsalis (1999), Randrianambinina et al. (2003) Lovegrove et al. (2014a)

Coquerel’s mouse lemur

T

Dausmann (2008)

Hairy-eared dwarf lemur

T/H

Reviewed by Dausmann (2014)

Lesser hedgehog tenrec

T/H

Lovegrove and Génin (2008)

Highland streaked tenrec Lowland streaked tenrec

H? H?

Gould and Eisenberg (1966), Stephenson and Racey (1994) Gould and Eisenberg (1966), Stephenson and Racey (1994)

Large-eared tenrec

n.k.

Gould and Eisenberg (1966)

Tailless tenrec

T/H

Gould and Eisenberg (1966), Nicoll (1986), Lovegrove et al. (2014b)

Dobson’s shrew tenrec Talazac’s shrew tenrec

n.k. n.k.

Stephenson and Racey (1993b) Stephenson and Racey (1993b)

Greater hedgehog tenrec

T/H

Reviewed by Geiser (2004), Lovegrove et al. (2014a)

*Also published as Microcebus myoxinus.

indeed mainly employed by small mammals, but several examples, such as hibernation in the black bear (females ∼80 kg, males ∼120 kg; Tøien et al. 2011), in the shortbeaked echidna Tachyoglossus aculeatus (∼3–10 kg; Grigg et al. 1989) and in various marmot species (2.5–4 kg; reviewed by Geiser 2004), and the finding of short torpor bouts in the American badger Taxidea taxus (∼9 kg; Harlow 1981), show that a higher body mass does not necessarily exclude the possibility of torpor. To evaluate how likely it is that the necessary preadaptation existed in the ancestral species, we summarize the occurrence of heterothermy in the relevant Malagasy and African species of the taxa lemurs, tenrecs, carnivores, rodents and Eulipotyphla. Within the five lemur families, heterothermy has been confirmed in only one, the Cheirogaleidae, but it occurs in the majority of species within this family (Table 1). The only genus of the Cheirogaleid family without any evidence of heterothermy is Phaner. The species of this genus have a highly specialized

diet and feed on self-generated gum resources that are available throughout the year (Schülke 2003), which might obliterate the need for heterothermy (Dausmann 2008). Most of the other Cheirogaleid species exhibit a considerable spectrum of heterothermy, from daily torpor to prolonged torpor and hibernation (e.g. Dausmann et al. 2004; Table 1). Notably, under free-ranging conditions, all of these species only become heterothermic during the cold–dry season; it can only be speculated whether they would also be able to undergo daily torpor throughout the year under especially adverse conditions. As just stated, the closely related Strepsirrhine species on the African mainland, the African lesser bushbaby, uses daily torpor as a strategy to survive emergency situations (Nowack et al. 2010, 2013b). Although torpor has only been observed during the cold– dry season, Galago moholi does not show seasonal fattening, and its use of torpor to deal with emergencies is likely to be possible at any time of the year, depending on conditions (Nowack et al. 2013b). Thus, it is conceivable that the


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ancestor of today’s lemurs was also able to undergo daily or prolonged torpor year round or in emergency situations. Most of the non-Cheirogaleid lemur species have higher body masses, corresponding lower mass-specific energy requirements, and life history strategies that do not necessitate energy-saving mechanisms, such as daily torpor or hibernation. Lemuridae species are diurnal, group-living animals that huddle during cold nights when temperatures are low and rest during the warmer daytime (e.g. Ostner 2002). The aye-aye Daubentonia madagascariensis has a comparably high body mass and a diet that is sufficient to meet its physiological requirements throughout the year (Sterling et al. 1994), and most species of the Indriidae and Lepilemuridae are folivorous and so have high year-round availability of forage. Thus, these species could have lost their ability or propensity to use torpor, without any loss in biological fitness. The second Malagasy animal group in which torpor occurs is the Malagasy tenrecs (order Afrosoricidae), which includes at least eight heterothermic species from three subfamilies and in six out of the 10 genera (Table 1). The lesser hedgehog tenrec displays daily torpor throughout the year, and normothermic phases seldom last more than 24 hours. Only during reproduction is heterothermy temporarily abandoned. This form of relaxed thermoregulation is considered the most primitive within the mammals (Lovegrove & Génin 2008, Wein 2010). A recent study in the tailless tenrec Tenrec ecaudatus revealed uninterrupted hibernation (passively following the ambient temperature without active arousal phases) for up to nine months (Lovegrove et al. 2014b). In the closest relatives of this group on the African mainland, heterothermy is also known from four species of Afrosoricidae in the family Chrysochloridae (Cape golden mole Chrysochloris asciatica, Grant’s golden mole Eremitalpa granti, Hottentot golden mole Amblysomus hottentotus longiceps, Juliana’s golden mole Neamblysomus julianae; reviewed by McKechnie & Mzilikazi 2011), e.g. daily torpor in Juliana’s golden mole (Jackson et al. 2009), and prolonged torpor for up to four days in the Hottentot golden mole (Scantlebury et al. 2008). The Madagascan pygmy shrew Suncus madagascariensis (family Soricidae) is the only known representative of the order Eulipothyphla on Madagascar. Torpor has not yet been studied in this small species (∼3.5 g) but has been found in other Soricidae species, such as in the Etruscan shrew Suncus etruscus in Europe (Atsalis 1999) and in the African shrews the greater red musk shrew Crucidura flavescens and Jouvenet’s shrew Crucidura jouvenetae (Lovegrove et al. 2014a). Furthermore, hibernation is commonly found in hedgehogs, which are closely related to the Soricidae (Fielden et al. 1990). Hibernation has long been known for the European species (Kristoffersson & Soivio 1964, Thaeti 1987), and recently, hibernation with

minimum body temperatures around 1 °C has also been found in the African hedgehog Atelerix frontalis (Hallam & Mzilikazi 2011). There is virtually no information available on thermoregulatory patterns of any of the Malagasy carnivore and rodent species, and thus, we can only resort to other species of these two taxa to evaluate the possibility of the ancestors’ capability to become heterothermic. The Malagasy carnivores comprise 10 rather small-bodied species in two subfamilies (Galidiinae, Euplerinae), including the fossa Cryptoprocta ferox and various mongoose species. Malagasy carnivores are a monophyletic group and are closely related to the African Herpestidae (Yoder et al. 2003, Poux et al. 2005). To date, there are no reports of any African or Malagasy carnivore species becoming heterothermic, and indeed, carnivores are generally not known for their pronounced propensity to enter torpor. However, heterothermy has been demonstrated in bears (Hissa et al. 1994, Tøien et al. 2011), several species of badger (Harlow 1981, Fowler & Racey 1988, Tanaka 2006), striped skunks Mephitis mephitis (Hwang et al. 2007) and raccoon dogs Nyctereutes procyonoides albus (Kitao et al. 2009). Only bears and Japanese and European badgers hibernate for several months; the other species show daily or prolonged torpor (up to 29 h in American badgers; Harlow 1981). Carnivores are mostly large species, and thus, due to lower mass-specific metabolic rates, potential energy savings by heterothermy are smaller than in small-bodied species. Furthermore, large bodies have a higher thermal inertia, and the lowest body temperature recorded in a carnivore is about 26 °C (in striped skunks; Hwang et al. 2007), which makes detection of heterothermy in these species by measurement of body temperature alone challenging. Studies in the black bear, however, show that despite the fact that their body temperature typically remains above 30 °C, savings of energy expenditure during hibernation can reach up to 50% (Tøien et al. 2011). All of the Malagasy rodents belong to the family Nesomyidae, and molecular data suggest that these rodents might have come from Asia, first invaded Madagascar and then invaded Africa from Madagascar (Jansa & Weksler 2004). Nevertheless, members of the family Nesomyidae can today only be found on Madagascar and on the African mainland. No studies on the thermoregulation of Malagasy rodent species are available; however, torpor is known to occur in various rodent species (Shehab et al. 2003, 2009, Geiser 2004) distributed over various habitats on the American, Australian, African, Asian and European continents. Studies on the African mainland revealed at least seven species from four families (Myoxidae, Muridae, Nesomyidae and Bathyergidae) that show daily torpor and two species that undergo hibernation (reviewed by McKechnie & Mzilikazi 2011). Three of the species entering daily torpor (pouched mouse Saccostomus campestris, fat

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mouse Steatomys pratensis, pygmy rock mouse Petromyscua coliinus) belong to the same family as the Malagasy rodents (Nesomyidae). However, anecdotal observations by the authors of accidentally trapped Eliurus spp. during the cold–dry season in Madagascar indicate that they cannot enter torpor. In summary, all taxa of terrestrial, non-volant mammals that inhabit Madagascar include representatives that are able to become heterothermic, either on Madagascar itself, or on other continents. Mostly, these belong to phylogenetically more basic clades, possibly reflecting an ancestral condition of thermoregulation, and we can therefore conclude that all taxa in principle could have originated from heterothermic ancestors. Furthermore, in the last 15 years, we have seen increasing evidence of tropical species, including primates, using heterothermy as an adaptation to energetically and/or climatically demanding situations. Thus torpor is now known to occur in species living in arctic, temperate and arid habitats, as well as in tropical regions (reviewed by Heldmaier et al. 2004, Geiser & Körtner 2010, McKechnie & Mzilikazi 2011, Dausmann 2014). This widespread distribution promotes the long-standing idea of heterothermy as a retained characteristic of mammals (Johnson 1931, Kayser 1961); heterothermy is now widely seen as a plesiomorphic trait that probably evolved early in mammalian evolution (Grigg et al. 2004, Lovegrove 2012a,b). Therefore, basic prerequisites for heterothermy should be shared by most mammalian species, if they have not been secondarily lost. Though we demonstrate that heterothermy could indeed have facilitated the colonization of Madagascar via rafting, this is not the only possible explanation for the colonization of Madagascar. For example, the timing of the origin of primates and strepsirrhines is still under discussion, and it was suggested that they may have originated much earlier than previously thought (Martin 2000). It is conceivable that strepsirrhine primates originated even before Madagascar split from India. This thought is supported by the finding of the primate fossil Bugtilemur mathesonigen in India, which was assigned to the Malagasy Cheirogaleidae (Marivaux et al. 2001). The affiliation of this fossil to the Malagasy lemurs is not generally accepted (e.g. Godinot 2006); however, if this fossil does indeed belong to the Malagasy lemurs, this could indicate that Madagascar was colonized over land before it became an island after all.


may help to maintain the body condition of a travelling individual, enabling its successful settlement and reproduction after arrival in a new habitat. Torpor can further facilitate a colonization process by delaying parturition or prolonging sperm storage, by enabling reproductive arrest phases until conditions improve and by allowing females to reach the new habitat with unborn offspring. This might abolish the absolute necessity of the arrival of more than one individual of the same species, and could positively affect the establishment of a founder population in a new habitat. Physiological evidence for torpor has been found in representatives of all terrestrial Malagasy mammal taxa or their close relatives, suggesting that torpor may indeed have facilitated colonization by increasing the probability of colonizing individuals surviving the journey over the ocean. Furthermore, torpor might have even helped the founder population, allowing it to survive during unfavourable times after arrival in the highly seasonal climate of Madagascar. Even though this hypothesis is controversial, at present, the rafting hypothesis is the most likely explanation for the colonization of Madagascar by terrestrial mammals.

ACKNOWLEDGEMENTS We thank the members of the research group Animal Ecology and Conservation of the University of Hamburg for their support.

REFERENCES

Our review emphasizes that daily or opportunistic torpor in mammals is an effective energy-saving strategy not only to counter seasonal, predictable bottlenecks but also to reduce energy requirements during acute emergency situations, and possibly during a journey towards a new habitat. This

Ali JR, Aitchison JC (2008) Gondwana to Asia: plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through latest Eocene (166–35 Ma). Earth-Science Reviews 88: 145–166. Ali JR, Huber M (2010) Mammalian biodiversity on Madagascar controlled by ocean currents. Nature 463: 653–656. Ali JR, Krause DW (2011) Late Cretaceous bioconnections between Indo-Madagascar and Antarctica: refutation of the Gunnerus Ridge causeway hypothesis. Journal of Biogeography 38: 1855–1872. Atsalis S (1999) Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. International Journal of Primatology 20: 883–910. Bieber C, Ruf T (2009) Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften 96: 165–171. Blanco M, Rahalinarivo V (2010) First direct evidence of hibernation in an eastern dwarf lemur species (Cheirogaleus crossleyi) from the high-altitude forest of Tsinjoarivo, central-eastern Madagascar. Naturwissenschaften 97: 945–950.


7

CONCLUSION



Blanco MB, Godfrey LR (2013) Does hibernation slow the ‘pace of life’ in dwarf lemurs (Cheirogaleus spp.)? International Journal of Primatology 34: 130–147. Blanco MB, Dausmann KH, Ranaivoarisoa JF, Yoder AD (2013) Underground hibernation in a primate. Scientific Reports 3: 1768. Calsbeek R, Smith TB (2003) Ocean currents mediate evolution in island lizards. Nature 426: 552–555. Canale C, Perret M, Henry P-Y (2012) Torpor use during gestation and lactation in a primate. Naturwissenschaften 99: 159–163. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiological Reviews 83: 1153–1181. Censky EJ, Hodge K, Dudley J (1998) Over-water dispersal of lizards due to hurricanes. Nature 395: 556. Christian N, Geiser F (2007) To use or not to use torpor? Activity and body temperature as predictors. Naturwissenschaften 94: 483–487. Daniel S, Korine C, Pinshow B (2010) The use of torpor in reproductive female Hemprich’s long-eared bats (Otonycteris hemprichii). Physiological and Biochemical Zoology 83: 142–148. Darrow J, Duncan M, Bartke A, Bona-Gallo A, Goldman B (1988) Influence of photoperiod and gonadal steroids on hibernation in the European hamster. Journal of Comparative Physiology A 163: 339–348. Dausmann KH (2008) Hypometabolism in primates: torpor and hibernation. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in Animals: Hibernation, Torpor and Cryobiology, 327–336. Pietermaritzburg, South Africa, Interpak. Dausmann KH (2014) Flexible patterns in energy savings: heterothermy in primates. Journal of Zoology 292: 101–111. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Physiology: hibernation in a tropical primate. Nature 429: 825–826. Fielden L, Waggoner J, Perrin M, Hickmann G (1990) Thermoregulation in the Namib Desert golden mole, Eremitalpa granti namibensis (Chrysochloridae). Journal of Arid Environments 18: 221–237. Fietz J, Schlund W, Dausmann KH, Regelmann M, Heldmaier G (2004) Energetic constraints on sexual activity in the male edible dormouse (Glis glis). Oecologia 138: 202–209. Fowler PA, Racey PA (1988) Overwintering strategies of the badger, Meles meles, at 57 °N. Journal of Zoology 214: 635–651. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annual Review of Physiology 66: 239–274. Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a Seasonal World, 109–121. Springer Berlin, Heidelberg, Germany.

Geiser F, Körtner G (2010) Hibernation and daily torpor in Australian mammals. Australian Zoologist 35: 204–215. Geiser F, Martin G (2013) Torpor in the Patagonian opossum (Lestodelphys halli): implications for the evolution of daily torpor and hibernation. Naturwissenschaften 100: 975–981. Geiser F, Masters P (1994) Torpor in relation to reproduction in the Mulgara, Dasycercus cristicauda (Dasyuridae: Marsupilia). Journal of Thermal Biology 19: 33–40. Geiser F, Turbill C (2009) Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96: 1235–1240. Godinot M (2006) Lemuriform origins as viewed from the fossil record. Folia Primatologica 77: 446–464. Goodman SM, Ganzhorn JU, Rakotondravony D (2003) Introduction to the mammals. In: Goodman SM, Benstead JP (eds) The Natural History of Madagascar, 1159–1186. Chicago University Press, Chicago, USA. Gould E, Eisenberg JF (1966) Notes on the biology of the Tenrecidae. Journal of Mammalogy 47: 660–686. Grigg G, Beard L, Augee M (2004) The evolution of endothermy and its diversity in mammals and birds. Physiological and Biochemical Zoology 77: 982–997. Grigg GC, Beard LA, Augee ML (1989) Hibernation in a monotreme, the echidna (Tachyglossus aculeatus). Comparative Biochemistry and Physiology. Part A, Physiology 92: 609–612. Hallam SL, Mzilikazi N (2011) Heterothermy in the southern African hedgehog, Atelerix frontalis. Journal of Comparative Physiology B 181: 437–445. Haq BU, Hardenbol J, Vail PR (1987) Chronology of fluctuating sea levels since the triassic. Science (New York, N.Y.) 235: 1156–1167. Harlow HJ (1981) Torpor and other physiological adaptations of the badger (Taxidea taxus) to cold environments. Physiological Zoology 54: 267–275. Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respiratory Physiology and Neurobiology 141: 317–329. Hissa R, Siekkinen J, Hohtola E, Saarela S, Hakala A, Pudas J (1994) Seasonal patterns in the physiology of the European brown bear (Ursus arctos arctos) in Finland. Comparative Biochemistry and Physiology. Part A, Physiology 109: 781–791. Houle A (1999) The origin of platyrrhines: an evaluation of the Antarctic scenario and the floating island model. American Journal of Physical Anthropology 109: 541–559. Hwang YT, Larivière S, Messier F (2007) Energetic consequences and ecological significance of heterothermy and social thermoregulation in striped skunks (Mephitis mephitis). Physiological and Biochemical Zoology 80: 138–145. Jackson CR, Setsaas TH, Robertson MP, Scantlebury M, Bennett NC (2009) Insights into torpor and behavioural thermoregulation of the endangered Juliana’s golden mole. Journal of Zoology 278: 299–307.

8




Jansa SA, Weksler M (2004) Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Molecular Phylogenetics and Evolution 31: 256–276. Johnson GE (1931) Hibernation in mammals. The Quarterly Review of Biology 6: 439–461. Jolly A, Albignac R, Petter JJ (1984) The lemurs. In: Jolly A, Oberle P, Albignac R (eds) Key Environments: Madagascar, 183–203. Pergamon Press, Oxford, UK. Kappeler PM (2000) Lemur origins: rafting by groups of hibernators? Folia Primatologica 71: 422–425. Karpanty S, Wright P (2007) Predation on lemurs in the rainforest of Madagascar by multiple predator species: observations and experiments. In: Gursky S, Nekaris KAI (eds) Primate Anti-Predator Strategies, 77–99. Springer, New York, USA. Kayser C (1961) The Physiology of Natural Hibernation. Pergamon, Oxford, UK. Kitao N, Fukui D, Hashimoto M, Osborne PG (2009) Overwintering strategy of wild free-ranging and enclosure-housed Japanese raccoon dogs (Nyctereutes procyonoides albus). International Journal of Biometeorology 53: 159–165. Kobbe S, Dausmann KH (2009) Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Naturwissenschaften 96: 1221–1227. Kobbe S, Ganzhorn J, Dausmann KH (2011) Extreme individual flexibility of heterothermy in free-ranging Malagasy mouse lemurs (Microcebus griseorufus). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 181: 165–173. Körtner G, Geiser F (2000) Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia). Oecologia 123: 350–357. Körtner G, Brigham RM, Geiser F (2000) Metabolism: winter torpor in a large bird. Nature 407: 318. Krause DW (2001) Fossil molar from a Madagascan marsupial. Nature 412: 497–498. Krause DW (2010) Biogeography: washed up in Madagascar. Nature 463: 613–614. Krause DW, O’Connor PM, Rogers KC, Sampson SD, Buckley GA, Rogers RR (2006) Late Cretaceous terrestrial vertebrates from Madagascar: implications for Latin American biogeography. Annals of the Missouri Botanical Garden 93: 178–208. Kristoffersson R, Soivio A (1964) Hibernation of the hedgehog (Erinaceus europaeus L.). The periodicity of hibernation of undisturbed animals during the winter in a constant ambient temperature. Annales Academiae Scientiarum Fennicae. Series A. IV. Biologica 80: 1–22. Lahann P (2007) Biology of Cheirogaleus major in a littoral rain forest in Southeast Madagascar. International Journal of Primatology 28: 895–905. Lebl K, Bieber C, Adamík P, Fietz J, Morris P, Pilastro A et al. (2011) Survival rates in a small hibernator, the edible

dormouse: a comparison across Europe. Ecography 34: 683–692. Lovegrove B (2000) Daily heterothermy in mammals: coping with unpredictable environments. In: Heldmaier G, Klingenspor M (eds) Life in the Cold: 11th International Hibernation Symposium, 29–40. Springer, Berlin, Germany. Lovegrove BG (2012a) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biological Reviews 87: 128–162. Lovegrove BG (2012b) A single origin of heterothermy in mammals. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a Seasonal World: Thermoregulatory and Metabolic Adaptations: 14th Hibernation Symposium, 3–11. Springer Berlin, Heidelberg, Germany. Lovegrove BG, Génin F (2008) Torpor and hibernation in a basal placental mammal, the lesser hedgehog tenrec Echinops telfairi. Journal of Comparative Physiology, B: Biochemical, Systematic, and Environmental Physiology 168: 303–312. Lovegrove BG, Canale CI, Levesque DL, Fluch G, Reháková-Petru˚ M, Ruf T (2014a) Are tropical small mammals physiologically vulnerable to Arrhenius effects and climate change? Physiological and Biochemical Zoology 87: 30–45. Lovegrove BG, Lobban KD, Levesque DL (2014b) Mammal survival at the Cretaceous–Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs. Proceedings of the Royal Society B: Biological Sciences 281: 20141304. Lynch GR, Vogt FD, Smith HR (1978) Seasonal study of spontaneous daily torpor in the white-footed mouse, Peromyscus leucopus. Physiological Zoology 51: 289–299. McCall RA (1997) Implications of recent geological investigations of the Mozambique Channel for the mammalian colonization of Madagascar. Proceedings of the Royal Society of London. Series B: Biological Sciences 264: 663–665. McKechnie AE, Mzilikazi N (2011) Heterothermy in Afrotropical mammals and birds: a review. Integrative and Comparative Biology 51: 349–363. Marivaux L, Welcomme J-L, Antoine P-O, Métais G, Baloch IM, Benammi M et al. (2001) A fossil lemur from the Oligocene of Pakistan. Science 294: 587–591. Martin RD (1972) Review lecture: adaptive radiation and behaviour of the Malagasy lemurs. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 264: 295–352. Martin RD (2000) Origins, diversity and relationships of lemurs. International Journal of Primatology 21: 1021–1049. Masters JC, Lovegrove BG, de Wit MJ (2007) Eyes wide shut: can hypometabolism really explain the primate colonization of Madagascar? Journal of Biogeography 34: 21–37. Measey JG, Miguel V, Drewes RC, Chiari Y, Melo M, Bourles B (2007) Freshwater paths across the ocean: molecular


9



phylogeny of the frog Ptychadena newtoni gives insights into amphibian colonization of oceanic islands. Journal of Biogeography 34: 7–20. Morrow G, Nicol SC (2009) Cool sex? Hibernation and reproduction overlap in the echidna. PLoS ONE 4: e6070. Nicoll ME (1986) Diel variation in body temperature in Tenrec ecaudatus during seasonal hypothermia. Journal of Mammalogy 67: 759–762. Nowack J, Mzilikazi N, Dausmann KH (2010) Torpor on demand: heterothermy in the non-lemur primate Galago moholi. PLoS ONE 5: e10797. Nowack J, Dausmann KH, Mzilikazi N (2013a) Nonshivering thermogenesis in the African lesser bushbaby, Galago moholi. The Journal of Experimental Biology 216: 3811–3817. Nowack J, Mzilikazi N, Dausmann KH (2013b) Torpor as an emergency solution in Galago moholi: heterothermy is triggered by different constraints. Journal of Comparative Physiology B 183: 547–556. Nowack J, Wippich M, Mzilikazi N, Dausmann KH (2013c) Surviving the cold, dry period in Africa: behavioral adjustments as an alternative to heterothermy in Galago moholi. International Journal of Primatology 34: 49–64. Ortmann S, Heldmaier G, Schmid J, Ganzhorn JU (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschaften 84: 28–32. Ostner J (2002) Social thermoregulation in redfronted lemurs (Eulemur fulvus rufus). Folia Primatologica 73: 175–180. Poppitt SD, Speakman JR, Racey PA (1994) Energetics of reproduction in the lesser hedgehog tenrec, Echinops telfairi (Martin). Physiological Zoology 67: 976–994. Poux C, Madsen O, Marquard E, Vieites DR, de Jong WW, Vences M (2005) Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Systematic Biology 54: 719–730. Rabinowitz P, Coffin M, Falvey D (1983) The separation of Madagascar and Africa. Science 220: 67–69. Rabinowitz PD, Woods S (2006) The Africa–Madagascar connection and mammalian migrations. Journal of African Earth Sciences 44: 270–276. Randrianambinina B, Rakotondravony D, Radespiel U, Zimmermann E (2003) Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur (Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur (Microcebus rufus) in Eastern Madagascar. Primates; Journal of Primatology 44: 321–331. Ruf T, Bieber C, Turbill C (2012) Survival, aging, and life-history tactics in mammalian hibernators. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a Seasonal World, 123–132. Springer Berlin, Heidelberg, Germany. Samonds KE, Godfrey LR, Ali JR, Goodman SM, Vences M, Sutherland MR et al. (2012) Spatial and temporal arrival patterns of Madagascar’s vertebrate fauna explained by

distance, ocean currents, and ancestor type. Proceedings of the National Academy of Sciences 109: 5352–5357. Scantlebury M, Lovegrove B, Jackson C, Bennett N, Lutermann H (2008) Hibernation and non-shivering thermogenesis in the Hottentot golden mole (Amblysomus hottentottus longiceps). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 178: 887–897. Schmid J (2000) Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance. Oecologica 123: 175–183. Schmid J, Speakman JR (2000) Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor. Journal of Comparative Physiology B 170: 633–641. Schmid J, Ruf J, Heldmaier G (2000) Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. Journal of Comparative Physiology B 170: 59–68. Schrago CG, Russo CAM (2003) Timing the origin of new world monkeys. Molecular Biology and Evolution 20: 1620–1625. Schülke O (2003) To breed or not to breed – food competition and other factors involved in female breeding decisions in the pair-living nocturnal fork-marked lemur (Phaner furcifer). Behavioral Ecology and Sociobiology 55: 11–21. Shehab AH, Mouhra O, Baker MAA, Amr ZS (2003) Observations on the forest dormouse, Dryomys nitedula (Pallas, 1779) (Rodentia: Gliridae), in Syria. Zoology in the Middle East 29: 4–12. Shehab AH, Asaad M, Mamkhair I (2009) Morphology and distribution of the Asian garden dormouse, Eliomys melanurus Wagner, 1840, in Syria. Zoology in the Middle East 48: 3–12. Simpson GG (1940) Mammals and land bridges. Journal of the Washington Academy of Sciences 30: 137–163. Stankiewicz J, Thiart C, Masters JC, de Wit MJ (2006) Did lemurs have sweepstake tickets? An exploration of Simpson’s model for the colonization of Madagascar by mammals. Journal of Biogeography 33: 221–235. Stephenson PJ, Racey PA (1993a) Reproductive energetics of the Tenrecidae (Mammalia: Insectivora). I. The large-eared tenrec, Geogale aurita. Physiological Zoology 66: 643–663. Stephenson PJ, Racey PA (1993b) Reproductive energetics of the Tenrecidae (Mammalia: Insectivora). II. The shrew-tenrecs, Microgale spp. Physiological Zoology 66: 664–685. Stephenson PJ, Racey PA (1994) Seasonal variation in resting metabolic rate and body temperature of streaked tenrecs, Hemicentetes nigriceps and H. semispinosus (Insectivora: Tenrecidae). Journal of Zoology 232: 285–294. Sterling EJ, Dierenfeld ES, Ashbourne CJ, Feistner ATC (1994) Dietary intake, food composition and nutrient intake in wild and captive populations of Daubentonia madagascariensis. Folia Primatologica 62: 115–124. Tanaka H (2006) Winter hibernation and body temperature fluctuation in the Japanese badger, Meles meles anakuma. Zoological Science 23: 991–997.

10




Thaeti H (1987) Seasonal differences in O2 consumption and respiratory quotient in a hibernator (Erinaceus europaeus). Annales Zoologici Fennici 15: 69–75. Tøien Ø, Blake J, Edgar DM, Grahn DA, Heller HC, Barnes BM (2011) Hibernation in black bears: independence of metabolic suppression from body temperature. Science 331: 906–909. Turbill C, Law BS, Geiser F (2003) Summer torpor in a free-ranging bat from subtropical Australia. Journal of Thermal Biology 28: 223–226. Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proceedings of the Royal Society B: Biological Sciences 278: 3355–3363. Turner JM, Körtner G, Warnecke L, Geiser F (2012) Summer and winter torpor use by a free-ranging marsupial. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 162: 274–280. Vences M, Vieites DR, Glaw F, Brinkmann H, Kosuch J, Veith M et al. (2003) Multiple overseas dispersal in amphibians. Proceedings of the Royal Society of London. Series B: Biological Sciences 270: 2435–2442. Vleck C (1981) Hummingbird incubation: female attentiveness and egg temperature. Oecologia 51: 199–205.

Webb PI, Skinner JD (1996) Summer torpor in African woodland dormice Graphiurus murinus (Myoxidae: Graphiurinae). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 166: 325–330. Wein J (2010) Effects of Ambient Temperature on Tropical Hibernation in the Lesser Hedgehog Tenrec, Echinops telfairi. PhD thesis, University of Hamburg, Hamburg, Germany. Willis CR, Brigham RM, Geiser F (2006) Deep, prolonged torpor by pregnant, free-ranging bats. Naturwissenschaften 93: 80–83. Wilz M, Heldmaier G (2000) Comparison of hibernation, estivation and daily torpor in the edible dormouse, Glis glis. Journal of Comparative Physiology B 170: 511–521. Yoder A, Cartmill M, Ruvolo M, Smith K, Vilgalys R (1996) Ancient single origin for Malagasy primates. Proceedings of the National Academy of Sciences of the United States of America 93: 5122–5126. Yoder AD, Burns MM, Zehr S, Delefosse T, Veron G, Goodman SM et al. (2003) Single origin of Malagasy Carnivora from an African ancestor. Nature 421: 734–737.


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