Abstract
The observation of heterothermy in a single suborder (Strepsirrhini) only within the primates is puzzling. Given that the placental-mammal ancestor was likely a heterotherm, we explored the potential for heterothermy in a primate closely related to the Strepsirrhini. Based upon phylogeny, body size and habitat stability since the Late Eocene, we selected western tarsiers (Cephalopachus bancanus) from the island of Borneo. Being the sister clade to Strepsirrhini and basal in Haplorrhini (monkeys and apes), we hypothesized that C. bancanus might have retained the heterothermic capacity observed in several small strepsirrhines. We measured resting metabolic rate, subcutaneous temperature, evaporative water loss and the percentage of heat dissipated through evaporation, at ambient temperatures between 22 and 35°C in fresh-caught wild animals (126.1 ± 2.4 g). We also measured core body temperatures in free-ranging animals. The thermoneutral zone was 25–30°C and the basal metabolic rate was 3.52 ± 0.06 W.kg−1 (0.65 ± 0.01 ml O2.g−1.h−1). There was no evidence of adaptive heterothermy in either the laboratory data or the free-ranging data. Instead, animals appeared to be cold sensitive (Tb ~ 31°C) at the lowest temperatures. We discuss possible reasons for the apparent lack of heterothermy in tarsiers, and identify putative heterotherms within Platyrrhini. We also document our concern for the vulnerability of C. bancanus to future temperature increases associated with global warming.
Highlights
IntroductionThe capacity to become heterothermic conveys significant fitness benefits and promotes survivability (Geiser and Turbill, 2009; Geiser and Brigham, 2012; Lovegrove et al, 2014b; Nowack et al, 2015, 2016; Stawski et al, 2015; Lovegrove, 2017)
Mass-specific resting metabolic rate (RMR) displayed inflection points at Ta = 25.0 ± 1.3◦C (±95% confidence interval; CI) and Ta = 30.0 ± 2.5◦C (±95% CI), and displayed a significant and linear relationship with Tas < 25◦C [F(1, 7) = 9.44, p < 0.018, r2 = 0.57] and Tas > 30◦C [F(1, 13) = 9.99, p = 0.007, r2 = 0.43], but not with Tas between these values (Figure 1A, Table 1)
The accuracy of the thermal limits proposed by the piecewise regression analysis was confirmed by substituting basal metabolic rate (BMR) into the respective regression equation of each line, in order to calculate the Ta at which they intersected BMR
Summary
The capacity to become heterothermic conveys significant fitness benefits and promotes survivability (Geiser and Turbill, 2009; Geiser and Brigham, 2012; Lovegrove et al, 2014b; Nowack et al, 2015, 2016; Stawski et al, 2015; Lovegrove, 2017). The study confirmed earlier work (see Grigg and Beard, 2000; Grigg et al, 2004) and showed that contrary to a longstanding paradigm, strict homeothermy is, as argued by Augee and Gooden (1992), the more derived state This conclusion, in combination with recent work on brown antechinus (Antechinus stuartii; Stawski et al, 2015), sugar gliders (Petaurus breviceps; Nowack et al, 2015), and short-beaked echidnas (Tachyglossus aculeatus; Nowack et al, 2016), provided support for the argument that the ancestors of the three crown mammalian clades namely, the Monotremata, Marsupialia and Placentalia, likely survived the mass extinction event marking the Cretaceous-Paleogene (K-Pg) boundary because of their heterothermic capacity (Lovegrove et al, 2014b; Lovegrove, 2017)
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