Research Article: Torpor on Demand: Heterothermy in the Non-Lemur Primate Galago moholi

Date Published: May 24, 2010

Publisher: Public Library of Science

Author(s): Julia Nowack, Nomakwezi Mzilikazi, Kathrin H. Dausmann, Craig R. White.

Abstract: Hibernation and daily torpor are energy- and water-saving adaptations employed to survive unfavourable periods mostly in temperate and arctic environments, but also in tropical and arid climates. Heterothermy has been found in a number of mammalian orders, but within the primates so far it seems to be restricted to one family of Malagasy lemurs. As currently there is no evidence of heterothermy of a primate outside of Madagascar, the aim of our study was to investigate whether small primates from mainland Africa are indeed always homeothermic despite pronounced seasonal changes in weather and food availability.

One of the nearest relatives of Malagasy lemurs, the African lesser bushbaby, Galago moholi, which inhabits a highly seasonal habitat with a hot wet-season and a cold dry-season with lower food abundance, was investigated to determine whether it is capable of heterothermy. We measured skin temperature of free-ranging individuals throughout the cool dry season using temperature-sensitive collars as well as metabolic rate in captured individuals. Torpor was employed by 15% of 20 animals. Only one of these animals displayed heterothermy in response to natural availability of food and water, whereas the other animals became torpid without access to food and water.

Our results show that G. moholi are physiologically capable of employing torpor. However they do not use it as a routine behaviour, but only under adverse conditions. This reluctance is presumably a result of conflicting selective pressures for energy savings versus other ecological and evolutionary forces, such as reproduction or territory defence. Our results support the view that heterothermy in primates evolved before the division of African and Malagasy Strepsirhini, with the possible implication that more primate species than previously thought might still have the potential to call upon this possibility, if the situation necessitates it.

Partial Text: Hibernation and daily torpor are traditionally seen as energy-saving adaptations to survive unfavourable periods in temperate and arctic climates. However, heterothermy is also known to occur in mammals living in tropical and arid habitats and has been observed in Australasian, Neotropical and Afrotropical animals [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11], [12]. Heterothermy has been found in a number of mammalian orders. Whereas in some groups a large number of species show heterothermy [13], within the primates it seems to be restricted to one family of small (30–500 g), nocturnal Malagasy lemurs, the Cheirogaleidae (incidence is confirmed in Microcebus murinus, M. berthae, M. ravelobensis, M. rufus, Mirza coquereli and Cheirogaleus medius, and suspected in most others) [4], [5], [7], [8], [11], [14]. Since the Cheirogaleidae are the most primitive of the lemur families, and heterothermy is so widespread within this family, it seems likely that the first primate inhabitants of Madagascar also exhibited this trait. Furthermore the capacity of lemurs to use heterothermy is believed to be a prerequisite for the successful colonization of Madagascar by lemurs from mainland Africa via rafting [15], [16]. Accordingly, torpor should be a plesiomorphic character and heterothermy should also be found in mainland relatives (Lorisiformes: Lorisidae & Galagidae), if it was not secondarily lost. However, there is no published evidence of heterothermy of a primate outside Madagascar.

Our study presents the first confirmation of heterothermy in a primate outside Madagascar, showing that G. moholi does indeed have the ability to employ torpor and thereby decrease energy expenditure by up to 90%. In contrast to the Malagasy lemurs where most individuals enter torpor or hibernation at some point during winter only a very small proportion of the Galagos became torpid. In fact, only one animal was torpid under undisturbed, free-ranging conditions. The other animals became torpid in the metabolic chamber, presumably in response to food and water deprivation over a 24-hr period. Evidently, G. moholi has the potential to enter torpid states, but probably only does so under especially adverse conditions, so torpor bouts are relatively rare. These results, together with earlier studies on free living G. moholi that did not find any incidence of torpor [19], demonstrate the potential flexibility of physiological parameters within one population. Physiological plasticity with regard to thermoregulatory adaptations was found to depend on Ta and body weight which might also be the case for G. moholi[4], [20], [23]. All animals found to use heterothermy in this study were either sub adults or even born within the study year. Therefore, torpor seems to be restricted to or at least more common in younger G. moholi. Adult G. moholi might either be better adapted to cope with unfavorable conditions such as cold climate and food scarcity (e.g. because of their greater body weight), or they can simply not afford to become torpid, e.g. not to compromise reproduction or territory defense.