The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum

Abstract

The influence of climate (mean annual rainfall, rainfall variability, ambient temperature, T a) on the basal metabolic rate (BMR) of 267 small mammals (<1 kg) from six zoogeographical zones was investigated using conventional and phylogenetically independent data (linear contrasts). All climate variables varied between zones, as did BMR and body temperature (T b) , but not thermal conductance. Holarctic zones were more seasonal and colder, but rainfall was less variable, than non-Holarctic zones. In general, the BMR was most strongly influenced by body mass, followed by T a and the rainfall variables. However, there was significant variation in the strength of these relationships between zones. BMR and T b increased with latitude, and mass-independent BMR and T b were positively correlated. The latter relationship offers evidence of a slow-fast metabolic continuum in small mammals. The fast end of the continuum (high BMR) is associated with the highest latitudes where BMR is most strongly influenced by T a and mean annual rainfall (i.e. mean productivity). The slow end of the continuum (low BMR) is associated with the semi-tropics, low productivity zones, and climatically unpredictable zones, such as deserts. Here rainfall variability has the strongest influence on BMR after body size. The implications of a slow–fast metabolic continuum are discussed in terms of various models associated with the evolution of BMR, such as the aerobic capacity models and the "energetic definition of fitness" models.

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Fig. 1a–e.
Fig. 2a–e.
Fig. 3a–c.
Fig. 4a–c.
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Abbreviations

BMR:

basal metabolic rate

C :

thermal conductance

CV MAR :

coefficient of variation of mean annual rainfall

EDF :

energetic definition of fitness

ENSO :

El Niño Southern Oscillations

G :

growth

MAR :

mean annual rainfall

M b :

body size

MR :

metabolic rate

N :

net energy

P :

production energy

PI :

phylogenetically independent

RMR :

resting metabolic rate

T a :

ambient temperature

T b :

body temperature

T cold :

mean coldest month temperature over all years

T lc :

lower critical limit of thermoneutrality

T mean :

mean yearly month temperature over all years

T warm :

mean warmest month temperature over all years

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Acknowledgements

I am very grateful to Ted Garland for advice on PDAP, Steven Piper for statistical advice, and Scott Steppan for kindly providing unpublished data on Sciurid phylogeny. Useful suggestions from two anonymous referees allowed me to provide a more objective interpretation of my analyses. Thank you. A core-rolling NRF Grant and a University of Natal Research Grant financed this study.

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Appendices

Appendix A

Data for the BMR, T b and C of 267 mammals <1 kg were obtained from the literature as shown in Table 3

Table 3. Physiological and climate data for 267 small mammals (<1 kg). Taxonomic nomenclature of Species column follows Wilson and Reeder (1993); some species names therefore do not follow that of the publication source. The Weather station code is assigned by the National Climatic Data Center (NCDC) in Asheville, NC. "T"=temperature stations, "R"=rainfall stations. The zoogeographical zones (Zone column) follow Udvardy (1975); af=Afrotropical, au=Australasia, im=Indomalaya, na=Nearctic, nt=Neotropical, pa=Palaearctic. Minimum thermal conductance (C) was calculated as the slope of the regression of minimum oxygen consumption and ambient temperature below thermoneutrality. [E east (longitude), N north (latitude), S south (latitude), T mean mean yearly month temperature over all years, W west (longitude)]

Appendix B

Phylogeny of small mammals (<1 kg) from six zoogeographical zones (Figs. 7, 8, 9, 10). The branch lengths were calculated arbitrarily following Pagel (1992). Taxonomic nomenclature follows Wilson and Reeder (1993). For eutherian mammals I followed the inter-ordinal relationships of Murphy et al. (2001). I used Kirsch et al. (1997) for metatherian species relationships. Major within-order sources were: Carnivora (Beninda-Emonds et al. 1999), Insectivora (Ruedi 1998), Lagomorpha (Halanych and Robinson 1997, 1999; Halanych et al. 1999), Macroscelidea (Raman and Perrin 1997), and Primates (DelPero et al. 2000; Purvis 1995), Rodentia: For major relationships among rodent families I followed Catzeflis et al. (1995), Nedbal et al. (1994), Robinson et al. (1997), Huchon et al. (1999) and Michaux and Catzeflis (2000). Relationships among families of the Sciuridae were kindly provided by S.J. Steppan (personal communication). Species relationships of the Sciuridae were obtained from Nadler et al. (1982, 1984) and Levenson et al. (1985). Other rodent species sources were: Muridae (Qumsiyeh 1986; Modi 1987; Chaline and Graf 1988; Qumsiyeh et al. 1991; Rogers and Engstrom 1992; Smith and Patton 1993; Planz et al. 1996; Watts and Baverstock 1995a, 1995b, 1996; Steppan 1995, Bellinvia et al. 1999; Barome et al.2000; Conroy and Cook 2000; Martin et al. 2000; Tiemann-Boege et al. 2000; Bell et al. 2001), Heteromyidae (Rogers 1990; Riddle 1995)

Fig. 7.
figure7

Clade A: Marsupials, Manoscelidae, Carnivora, and Insectivora

Fig. 8.
figure8

Clade B: Scantentia, Primates, Lagomorpha, and some rodents

Fig. 9.
figure9

Clade C: Rodentia (Dipodidae, Petromyscinae, Mystromyinae, Dentromurinae, Gerbillinae, Murinae)

Fig. 10.
figure10

Clade D: Rodentia (Cricetinae, Arvocolinae, Sigmodontinae, Neotominae)

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Lovegrove, B.G. The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B 173, 87–112 (2003). https://doi.org/10.1007/s00360-002-0309-5

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Keywords

  • Basal metabolic rate
  • Mammals
  • Climate
  • Unpredictable environments
  • Metabolic continuum