Barry G. Lovegrove

AVIAN FACULTATIVE HYPOTHERMIC RESPONSES: A REVIEW

Abstract Recent evidence suggests that avian facultative hypothermic responses are more common, and occur in a wider variety of ecological contexts, than previously thought. The capacity for shallow hypothermia (rest-phase hypothermia) occurs throughout the avian phylogeny, but the capacity for pronounced hypothermia (torpor) appears to be restricted to certain taxa. Families in which torpor has been reported include the Todidae, Coliidae, Trochilidae, Apodidae, Caprimulgidae, and Columbidae. Facultative hypothermia occurs in species ranging in body mass (Mb) from <3 g to ca. 6500 g. Minimum body temperature (Tb) during hypothermia is continuously distributed from 4.3°C to ca. 38°C. The physiological distinction between torpor and rest-phase hypothermia is unclear. Whereas these two responses have traditionally been distinguished on the basis of Tb, we find little support for the biological reality of specific Tb limits. Instead, we argue that emphasis should be placed on understanding the relationship between metabolic and Tb reduction and the capacity to respond to external stimuli. Patterns of thermoregulation during avian hypothermic responses are relatively variable, and do not necessarily follow the entry–maintenance–arousal patterns that characterize mammalian responses. Avian hypothermic responses are determined by a suite of ecological and physiological determinants including food availability, ambient temperature, hormone levels, and breeding cycle. Respuestas Facultativas de la Hipotermia en Aves: Una Revisión Resumen. Evidencias recientes sugieren que las respuestas facultativas de la hipotermia aviar son más comunes y ocurren en una gran cantidad de contextos ecológicos, a diferencia de lo que anteriormente se pensaba. La capacidad de una hipotermia ligera (hipotermia de descanso) ocurre en toda la filogenia de las aves, pero la capacidad de mantener una hipotermia pronunciada (torpor) aparece sólo en ciertos taxones. El torpor ha sido reportado en las familias Todidae, Coliidae, Trochilidae, Apodidae, Caprimulgidae y Columbidae. La hipotermia facultativa ocurre en especies con un peso corporal (Mb) de <3 g hasta 6.5 kg. Durante la hipotermia, la temperatura mínima corporal (Tb) está distribuída contínuamente entre 4.3°C y 38°C. La diferencia fisiológica entre el torpor y la hipotermia de descanso no es clara. Tradicionalmente se ha reconocido que las dos respuestas se basan en la Tb. Sin embargo, nosotros encontramos pocas evidencias biológicas sobre límites específicos de la Tb. Por el contrario, nosotros argumentamos que el énfasis debe enfocarse en la relación entre la reducción metabólica y de Tb y la capacidad de responder a estímulos externos. Los patrones de termoregulación de las respuestas hipotérmicas de las aves son relativamente variables y no necesariamente siguen los patrones de entrada-mantenimiento-elevación que caracterizan estas respuestas en los mamíferos. Las respuestas de la hipotermia en aves están determinadas por la interacción entre factores ecológicos y fisiológicos como disponibilidad de alimentos, temperatura ambiental, niveles hormonales y ciclo reproductivo.

The evolution of endothermy in Cenozoic mammals: a plesiomorphic‐apomorphic continuum

The evolution of endothermy in birds and mammals was one of the most important events in the evolution of the vertebrates. Past tests of hypotheses on the evolution of endothermy in mammals have relied largely on analyses of the relationship between basal and maximum metabolic rate, and artificial selection experiments. I argue that components of existing hypotheses, as well as new hypotheses, can be tested using an alternative macrophysiological modeling approach by examining the development of endothermy during the Cenozoic. Recent mammals display a 10°C range in body temperature which is sufficiently large to identify the selective forces that have driven the development of endothermy from a plesiomorphic (ancestral) Cretaceous or Jurassic condition. A model is presented (the Plesiomorphic‐Apomorphic Endothermy Model, PAE Model) which proposes that heterothermy, i.e. bouts of normothermy (constant body temperature) interspersed with adaptive heterothermy (e.g. daily torpor and/or hibernation), was the ancestral condition from which apomorphic (derived), rigid homeothermy evolved. All terrestrial mammal lineages are examined for existing data to test the model, as well as for missing data that could be used to test the model.

Phenotypic flexibility in the basal metabolic rate of laughing doves: responses to short-term thermal acclimation.

SUMMARY Many birds exhibit considerable phenotypic flexibility in maintenance energy requirements, and up- or downregulate basal metabolic rate (BMR) over time scales of days to weeks during thermal acclimation. However, the extent to which individual birds can reverse the direction of BMR adjustments over short time scales remains unknown. In this study, we examined metabolic responses to short-term thermal acclimation in laughing doves Streptopelia senegalensis. In 30 wild-caught doves (mean body mass=92.6 g) divided into three experimental groups of 10 birds each, initial BMR averaged 0.760±0.036 W. Thereafter, each group was acclimated to one of three acclimation air temperatures (Tacc=10, 22 or 35°C) for 21 days, during which time the doves were housed in individual cages. Following the first acclimation period (acclimation I), BMR (W) was significantly lower and was negatively and linearly related to Tacc [BMR=0.714-0.005Tacc]. Acclimation I BMR varied from 0.546±0.039 W in doves acclimated to Tacc=35°C to 0.665±0.058 W at Tacc=10°C. A second acclimation period of a further 21 days (acclimation II) revealed that the direction of BMR adjustments could be reversed within individuals, with acclimation II BMR again negatively and linearly related to Tacc. The slope of the relationship between BMR and Tacc following acclimation II was not significantly different to that following acclimation I. BMR exhibited consistent inter-individual variation, with a low but significant repeatability of 0.113. The within-individual BMR variation of up to 26% that we observed in laughing doves reveals that BMR is a highly flexible trait in this species, and reiterates the need to take phenotypic plasticity into account in comparative analyses of avian energetic parameters.

Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius).

Thermoregulation and the energetic significance of clustering behavior were assessed in the white‐backed mousebird Colius colius. Basal metabolic rate was 40% below the predicted allometric values. Rest‐phase body temperature (Tb) was highly labile and as low as 26°C. Rest‐phase Tb was not regulated with respect to a constant set point temperature, as occurs typically in endotherms. Rather, we observed periods of linear decreases in rest‐phase Tb at a rate dependent on ambient temperature (Ta) and the number of individuals in a cluster. The apparent inability of individual mousebirds to maintain rest‐phase homeothermy suggests that clustering behavior is obligatory in the defense of a rest‐phase set point Tb. The low rest‐phase body temperatures exhibited by single C. colius hence appear to represent a normothermic state rather than typical avian facultative hypothermia. The birds were able to make significant energy savings by means of clustering behavior. These energy savings were dependent on Ta and the number of birds in the cluster. At a Ta of 15°C, the mean energy expenditure of each bird in a cluster of six was 50% of that of a single bird. The metabolic traits of C. colius are likely be adaptive in the arid habitats that this species inhabits.

Daily Torpor in Free‐Ranging Rock Elephant Shrews, Elephantulus myurus: A Year‐Long Study

Under laboratory conditions, rock elephant shrews, Elephantulus myurus, use daily torpor under both short and long photoperiod acclimation. However, use of heterothermy often differs under field and laboratory conditions. We investigated the use of torpor in free‐ranging elephant shrews from May 2001 to May 2002. The elephant shrews were capable of daily torpor throughout the year, with torpor most prevalent during winter. We recorded two torpor bouts during early summer (November). We recorded a total of 467 torpor bouts during the year. The mean torpor minimum body temperature (Tbmin) for the whole year was 15.3° ± 4.4°C, and the mean bout length was 8.6 ± 3.5 h. These values were in the range expected for daily heterotherms. However, there was some marginal overlap with hibernation characteristics; a few torpor bouts were longer than 24 h in duration, and Tbmin decreased below 10°C. Torpor was highly correlated with low ambient temperature and photoperiod. Torpor was also correlated with invertebrate abundance after controlling for photoperiod effects. During the year in which this study was conducted, the rainfall was 14% below long‐term average. Historical rainfall records show that summer rainfall during strong El Niño years is up to 40% below the long‐term average. During these drought years, the frequency of summer torpor may be higher, highlighting the need for long‐term physiological data in free‐ranging animals.

Daily Heterothermy in Mammals: Coping with Unpredictable Environments

Zoogeographical patterns of daily heterothermy in mammals show that the Afrotropical and Australasian zones have the highest number of species, genera and orders exhibiting daily torpor. The Palaearctic has the lowest incidence of daily torpor. The Australasian and the Afrotropical zones also showed the highest incidences of summer torpor and torpor in desert species. These patterns suggest an association of daily torpor with unpredictable environments (low inclement energetic gains), versus an association of hibernation with predictably cold seasons (high inclement energetic costs).

Torpor patterns in the pouched mouse (Saccostomus campestris ; Rodentia): a model animal for unpredictable environments

Abstract Patterns of spontaneous and induced daily torpor were measured in the Afrotropical pouched mouse (77–115 g), Saccostomus campestris, in response to photoperiod, temperature, and food deprivation, using temperature telemetry. Photoperiod had no influence on the incidence, depth, or duration of daily torpor in either males and females. Although the testis size index decreased in response to food deprivation and photoperiod by a maximum of 24%, full testis regression did not occur. Torpor bout duration was, on average, 5.3 h, independent of photoperiod and ambient temperature. Males did not enter torpor in response to food deprivation but did in response to low ambient temperature, though significantly less frequently than females. At normothermia, the body temperatures (daily minimum, mean, maximum) of males were significantly lower than those of females. Minimum body temperatures of both males and females during torpor did not fall below 20 °C at an ambient temperature of 15 °C. The patterns of torpor measured here differ from those observed in species from strongly seasonal environments. They suggest adaptation to an environment rendered unpredictable by the El Niño Southern Oscillations. As an aseasonal, opportunistic breeder capable of year-round adaptive hypothermia, the pouched mouse represents an excellent model animal for research on physiological and behavioral adaptations to unpredictable environments.

THE EVOLUTION OF BODY ARMOR IN MAMMALS: PLANTIGRADE CONSTRAINTS OF LARGE BODY SIZE

Abstract.— Predictions associated with opposing selection generating minimum variance in basal metabolic rate (BMR) in mammals at a constrained body mass (CBM; 358 g) were tested. The CBM is presumed to be associated with energetic constraints linked to predation and variable resources at intermediate sizes on a logarithmic mass scale. Opposing selection is thought to occur in response to energetic constraints associated with predation and unpredictable resources. As body size approaches and exceeds the CBM, mammals face increasing risks of predation and daily energy requirements. Fast running speeds may require high BMRs, but unpredictable and low resources may select for low BMRs, which also reduce foraging time and distances and thus predation risks. If these two selection forces oppose each other persistently, minimum BMR variance may result. However, extreme BMR outliers at and close to the CBM should be indicative of unbalanced selection and predator avoidance alternatives (escapers vs. defenders), and may therefore provide indirect support for opposing selection. It was confirmed that body armor in defenders evolves at and above the CBM, and armored mammals had significantly lower BMRs than their nonarmored counterparts. However, analyses comparing the BMR of escapers–the fastest nonarmored runners (Lagomorpha)—with similar‐sized counterparts were inconclusive and were confounded by limb morphology associated with speed optimization. These analyses suggest that the risks and costs of predation and the speed limitations of the plantigrade foot may constrain the evolution of large body sizes in plantigrade mammals.

Heterothermy in elephant shrews, Elephantulus spp. (Macroscelidea): daily torpor or hibernation?

Abstract The physiological parameters of heterothermy (e.g. minimum body temperature and oxygen consumption, percentage metabolic reduction, and bout length) were measured in two species of Elephantulus elephant shrews (Elephantulus myurus and Elephantulus rozeti; Macroscelidea) as a function of ambient temperature. Both species displayed deep torpor whereby the body temperatures of ca. 5 °C and oxygen consumption as low as 2% of basal metabolic rate were attained. Torpor bout length (n=57 bouts) never exceeded 24 h. These data are characteristic of both hibernation (minimum body temperature and metabolism) and daily torpor (bout length), and argue that these two physiological responses may not necessarily have separate evolutionary origins.

Circadian activity rhythms in the solitary Cape molerat (Georychus capensis: Bathyergidae) with some evidence of splitting

Circadian activity patterns were measured in the solitary, subterranean Cape molerat, Georychus capensis, under fixed 12:12 LD, constant dark DD, and constant light LL photoperiods for 250 consecutive days using passive infra-red activity sensors. The molerats displayed significant nocturnal activity rhythms under 12:12 LD and free-running rhythms (23.5 h < tau > 25.8 h) under constant conditions. In one individual evidence was found of splitting of the activity rhythm under constant dark; the split rhythms free-ran with short- and long-periods of 23.6 h and 24.7 h, respectively. These data show that, despite degenerate retinae, G. capensis (i) are capable of perceiving light at the level of the circadian pacemaker; (ii) can entrain endogenous activity oscillators to fixed photoperiods; and (iii) display evidence of a free-running activity oscillator.