Patterns, mechanisms and evolution of avian facultative hypothermic responses : a southern African perspective.
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Date
2001
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Abstract
Recent evidence suggests that avian facultative hypothermic responses are more common than
previously thought. Traditionally, several categories of avian hypothermic responses have
been recognized, and are frequently differentiated on the basis of minimum body temperature
(T[b]) The available data suggest that the capacity for shallow hypothermia (rest-phase
hypothermia) occurs throughout the avian phylogeny, but that the capacity for pronounced
hypothermia (torpor) is restricted to certain taxa. However, there are currently too few data to
test hypotheses concerning the evolution of avian hypothermic responses. Facultative
hypothermia occurs over most of the avian body mass (M[b]) range, but is most common in
small species. Minimum body temperature during hypothermia (T[min]) is continuously
distributed from 4.3 °C to ca. 38°C. The continuous T[min] distribution, as well as recent
evidence that the T[b] ranges of different avian physiological states may overlap, question the
biological reality of specific T[b] limits. Pattens 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.
I investigated normothermic thermoregulation and hypothermic responses to restricted
food in the speckled mousebird Colius striatus in the context of the distinction between
normothermia, rest-phase hypothermia, and torpor. The lowest T[b] recorded in a bird which
was able to arouse spontaneously was 18.2°C. However, I was unable to clearly discern
between normothermic, hypothermic and torpor T[b] ranges. Furthermore, hypothermic
responses did not accord with the patterns typically observed in birds and mammals.
Metabolic suppression normally associated with entry into torpor and the defence of a torpor
T[b] setpoint was largely absent. Laboratory data for C. striatus, as well as published data for Colius colius suggest that
clustering behavior plays an important thermoregulatory role in mousebirds. Hence, I
investigated thermoregulation under semi-natural conditions in C. striatus. In particular, I was
interested in the interaction between clustering behavior and hypothermic responses during
energy stress (restricted feeding). In contrast to clustering birds, rest-phase thermoregulation
in single birds was characterised by linear decreases in T[b] and the birds did not appear to
defend a specific T[b] setpoint. During restricted feeding, both clustering and single birds
exhibited significant decreases in rest-phase T[b]. The extent of these facultative hypothermic
responses was greater in single birds than in clustering birds, supporting the prediction that
clustering behavior moderates the use of facultative hypothermia.
I also tested the prediction that in free-ranging C. colius, the use of heterothermy
should be rare, even at the coldest time of the year. I recorded mid-winter rest-phase body
temperatures (T[b]) in a flock of free-ranging C. colius in an arid habitat in the Karoo, South
Africa. The mousebirds' rest-phase T[b] was fairly labile, but was maintained above 33°C,
despite T[a]s as low as -3.4 °C. The mousebirds showed no evidence of torpor under natural
conditions; a facultative hypothermic response, during which T[b] was reduced to 29 - 33°C,
was only observed on one occasion. The observed patterns of thermoregulation supported my
predictions, and suggest that thermoregulation in clustering C. colius in the wild is
significantly different to that of single birds under laboratory conditions. My results also
suggest that the pronounced capacity for heterothermy usually associated with mousebirds is
not necessarily representative of their patterns of thermoregulation under natural conditions.
The capacity for avian torpor appears to be dependent on phylogeny. To investigate
phylogenetic constraints on the capacity for torpor, I measured metabolic responses to food
deprivation in a small, arid-zone passerine, the red-headed finch (Amadina erythrocephala). I observed significant reductions in rest-phase energy expenditure and body temperature (T[b]) in
response to restricted feeding. The maximum extent of T[b] suppression (ca. 5°C) and energy
savings (ca. 10%) were consistent with those reported for a number of other passerines. The
lowest T[b] I observed in a bird able to arouse spontaneously was 34.8°C. My data support the
hypothesis that the capacity for heterothermy in passerines is phylogenetically constrained,
and that the majority cannot employ torpor in response to energetic stress.
Selection for the capacity for torpor is presumably similar to the selection pressures
acting on other avian energetic traits, such as basal metabolic rate (BMR). I tested the
generality of a recent model linking the slow-fast mammalian metabolic continuum to global
patterns of climatic predictability using BMR data for 219 non-migratory bird species. Avian
BMR varied significantly between zoogeographical zones, with Afrotropical, Indomalayan
and Australasian species generally exhibiting lower BMR than Holarctic species. In addition,
the magnitude of differences between arid and mesic species varied between zones. In the
Nearctic, these differences were pronounced, whereas no significant differences were evident
for Afrotropical or Australasian species. A slow-fast metabolic continuum similar to that
described in mammals appears to exist for birds, with higher BMR associated with
predictable, seasonal environments and lower BMR with less predictable environments, in
particular those affected by the El Niño Southern Oscillation.
I constructed a generalised, conceptual model which attempts to predict the occurrence
of torpor using phylogeny, M[b] constraints, a trade-off between energetic benefits and potential
ecological costs, and specific ecological factors. A recent hypothesis suggests that endotherm
heterothermy is monophyletic, and predicts that torpor should be more widespread in
phylogenetically older taxa. Once phylogeny is considered, the most important determinant of
avian torpor is M[b]. I used an existing model of endotherm torpor to predict the relationship between M[b] and minimum T[b] during torpor. The available data show that the lower limit of
torpor T[b] is determined by the M[b]-dependent costs of rewarming following a torpor bout.
Finally, I constructed a model based on the assumption that torpor is adaptive if the energetic
benefits exceed the potential ecological costs. The model predicted that torpor should be more
prevalent in species near the extremes of the avian metabolic continuum. The available data
provide tentative support for this prediction. In addition to generalised factors such as
phylogeny and M[b], specific aspects of a particular species' ecology need to be considered
when predicting the occurrence of avian torpor.
Description
Thesis (Ph.D.)-University of Natal, Pietermaritzburg, 2001.
Keywords
Birds--Physiology., Colius spp., Body temperature--Regulation., Birds, Effect of temperature on., Hypothermia., Cold--Physiological effect., Theses--Zoology.