Mammal survival at the Cretaceous-Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs.

Free-ranging common tenrecs, Tenrec ecaudatus, from sub-tropical Madagascar, displayed long-term (nine months) hibernation which lacked any evidence of periodic interbout arousals (IBAs). IBAs are the dominant feature of the mammalian hibernation phenotype and are thought to periodically restore long-term ischaemia damage and/or metabolic imbalances (depletions and accumulations). However, the lack of IBAs in tenrecs suggests no such pathology at hibernation Tbs > 22°C. 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 boundary following a meteorite impact. The genetics and biochemistry of IBAs are of immense interest to biomedical researchers and space exploration 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.

The energetics of a Malagasy rodent, Macrotarsomys ingens (Nesomyinae): a test of island and zoogeographical effects on metabolism.

This study provides first insights into the energetics of the Nesomyinae, a subfamily of rodents endemic to Madagascar. The ancestral nesomyine colonized Madagascar from Africa ca. 30-15 mya at the onset of Oligocene global cooling. We tested the hypothesis that, contrary to what might be expected from Island Biogeography theory, post-colonization character displacement of thermoregulatory traits was constrained by phylogenetic inertia through climate adaptation. The study was conducted in the Parc National d'Ankarafantsika, Madagascar. We measured the basal metabolic rate (BMR) and body temperature (T b) patterns of naturally warm-acclimated, freshly captured adult long-tailed big-footed mice Macrotarsomys ingens (67.4 g). The mean ± SD BMR of M. ingens was 0.298 ± 0.032 Watts (n = 12), 31.7 % lower than that predicted by a phylogenetically independent allometric equation. Body mass was correlated with BMR. The lower critical limit of thermoneutrality (T lc) was 30.7°C. The mean ± SD T b = 36.1 ± 0.8°C (n = 12) compared well with the mean T b values for myomorph rodents from the Afrotropical zone, but was lower than those of the Neotropical and Palearctic zones. M. ingens became pathologically hypothermic when exposed to ambient temperatures lower than 18°C. The soil temperature at depths of 250 mm and deeper did not decrease below 22°C throughout the austral winter. The thermoregulatory data for M. ingens did not differ from those that characterize mainland Afrotropical rodents. However, BMR and T b were lower than those of Holarctic rodents. Thus, contrary to expectations of Island Biogeography theory that rapid character displacement often occurs in morphological and behavioural traits when mammals colonize islands, M. ingens displayed climate-related physiological traits indicative of phylogenetic inertia. Presumably the tropical conditions that prevailed on Madagascar at the time of colonisation differed very little from those of the African mainland, and hence there was no strong driving force for change. Unlike small tenrecs and lemurs that radiated on Madagascar prior to the Oligocene, traits associated with an insular existence, such as daily torpor and hibernation, were not evident in M. ingens.

Effects of reproductive status and high ambient temperatures on the body temperature of a free-ranging basoendotherm.

Tenrecs (Order Afrosoricida) exhibit some of the lowest body temperatures (T b) of any eutherian mammal. They also have a high level of variability in both active and resting T bs and, at least in cool temperatures in captivity, frequently employ both short- and long-term torpor. The use of heterothermy by captive animals is, however, generally reduced during gestation and lactation. We present data long-term T b recordings collected from free-ranging S. setosus over the course of two reproductive seasons. In general, reproductive females had slightly higher (~32 °C) and less variable T b, whereas non-reproductive females and males showed both a higher propensity for torpor as well as lower (~30.5 °C) and more variable rest-phase T bs. Torpor expression defined using traditional means (using a threshold or cut-off T b) was much lower than predicted based on the high degree of heterothermy in captive tenrecs. However, torpor defined in this manner is likely to be underestimated in habitats where ambient temperature is close to T b. Our results caution against inferring metabolic states from T b alone and lend support to the recent call to define torpor in free-ranging animals based on mechanistic and not descriptive variables. In addition, lower variability in T b observed during gestation and lactation confirms that homeothermy is essential for reproduction in this species and probably for basoendothermic mammals in general. The relatively low costs of maintaining homeothermy in a sub-tropical environment might help shed light on how homeothermy could have evolved incrementally from an ancestral heterothermic condition.