Torpor in songbirds and the evolution of avian heterothermy

Abstract

Heterothermy is an energy saving physiological mechanism that allows small endothermic homeotherms to overcome conditions of reduced energy availability. Seasonal variations in environmental temperature and food availability pose different energetic constraints for many bird species, compelling some to rely on behavioural or physiological responses to offset the costs of normothermic thermoregulation. Heterothermy is most pronounced in phylogenetically older orders such that few data provide evidence of heterothermy in the most recently derived avian order comprising of ~55% of global avian biodiversity – Passeriformes. Sunbirds and swallows in particular, have traits similar to those of phylogenetically primitive taxa that use torpor (pronounced hypothermia; hypometabolism) which are the small body size and seasonal/unpredictable variations in food availability. In addition, sunbirds are convergently similar to hummingbirds which both rely predominantly on a nectivorous diet. Swallows on the other hand are diurnal aerial hunters of insects but share a similar diet to many Caprimulgiformes which rely on nocturnal aerial hunting of insects. In this study, I measured gaseous exchange using flow-through respirometry and body temperature (Tb) at air temperatures at 5, 10, 15, 20 and 25℃ in five southern African songbird species under a food deprivation treatment. White-bellied sunbirds (Cinnyris talatala) and southern double-collared sunbirds (Cinnyris chalybeus) displayed substantial reductions in Tb (~10℃ below normothermic levels) whilst maintaining relatively high resting metabolic rate or RMR from here on (defined as the metabolic rate measured in resting birds during their rest-phase, for the purposes of this study), to suggest they were not in torpor. Additionally, they responded to external stimuli even at the the lowest Tair to which they were exposed. In contrast, even though birds in torpor display substantial reductions in Tb, they also maintain relatively low RMR and become lethargic. RMR ranged from 0.038W at ~20℃ to 0.268W at ~10℃ in C. talatala, and 0.092W at ~25℃ to 0.271W at ~10℃ in Ch. amethystina. Amethyst sunbirds (Chalcomitra amethystina) maintained normothermy and one individual showed deep reductions in Tb whilst maintaining shallow reductions in RMR. Since Chalcomitra amethystina is a slightly larger species from a different genus, occurring in a different habitat, especially from C. chalybeus, this response may be common in more sunbird species than previously reported. South African cliff swallows (Petrochelidon spilodera) and red-billed queleas (Quelea quelea) maintained normothermy with only two individuals of each species reducing their Tbs to levels that could be considered heterothermic. These findings illustrate that, whereas sunbirds may frequently use a pronounced form of rest-phase hypothermia, swallows and queleas may occasionally use shallow rest-phase hypothermia in extreme conditions. These species likely experienced selection pressures for heterothermic responses due to their specialists’ diets and high metabolic demands.