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

Abstract

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.

Keywords: Cretaceous–Palaeogene boundary; Madagascar; Tenrec ecaudatus; hibernation; mammals.

Figure 1.

An illustration of predation of common tenrecs by snakes, one cause of high mortality at the Ankarafantsika site. (a) A captured Malagasy ground boa (Acrantophis madagascariensis) 2 days after swallowing an adult male tenrec. (b) The tenrec that was extracted from the live boa. (c) The body temperatures of the tenrec and the dead tenrec within the snake, captured by an iButton transmitter–logger package that was implanted into the tenrec. (Online version in colour.)

Figure 2.

Hibernation bouts of eight to nine months in three common tenrecs (Tenrec ecaudatus) measured in the dry deciduous forest of western Madagascar. Note the complete lack of IBAs. The measures of soil temperature in (a) were obtained less than 3 m from the hibernaculum, whereas those in (b,c) were measured about 200 m from the hibernaculum, accounting for the lack of precise fit of the soil temperatures to the corresponding T_bs in (b,c). The torpor bouts in (b,c) in the period following excavation were induced in the laboratory when the animals were exposed to an ambient temperature of 18°C. The data in (d) illustrate the daily rhythms of T_b in a normothermic adult male tenrec prior to entry into hibernation. (Online version in colour.)

Figure 3.

Frequency distributions of black body air temperatures (a), soil temperatures at a depth of 250 mm (b) and body temperatures (c) of an adult male tenrecs (data from figure 2a). Note that, throughout the austral winter, neither the soil nor the body temperature decreased below 22°C. (Online version in colour.)