The Metabolic Geography of The Red Squirrel (Tamiasciurus Hudsonicus)

The metabolic geography of the red squirrel (Tamiasciurus hudsonicus)
Elad Ben-Ezra
Department of Natural Resource Sciences
McGill University, Macdonald campus
Montreal, Quebec, Canada
October 2009
A thesis submitted to McGill University in partial fulfillment

of the requirements of the degree of Master of Science
© Elad Ben-Ezra
2009
Abstract
In coining the term “metabolic geography”, this thesis investigates geographic
variation in metabolic rate, body size, and population density of eight red squirrel
populations along a 3000 km latitudinal gradient in western Canada. There was a
positive trend between body mass and latitude along the gradient, consistent with
the prediction of Bergmann’s rule. In addition, abundance increased with mean
annual temperature along the gradient, and all else being equal, squirrels present
in high abundance were larger than squirrels present at low abundance. Resting
metabolic rate increased with latitude, but there was no relationship between
maximum metabolic rate and latitude. Overall, this suggests that the metabolic
geography of red squirrels is driven more by regional variation in the demands of
maintaining homeothermy rather than the supply of resources. In addition,
squirrels at high latitudes are operating much closer to their physiological limits
than squirrels at lower latitudes.
i
Resumé
Cette thèse étudie la géographie métabolique de huit populations d’écureuils roux
tout au long d’un gradient latitudinal de 3000 km dans l’ouest canadien. En
particulier, les variations géographiques du taux métabolique, de la taille
corporelle et de la densité de population seront examinées. La masse corporelle
avait tendance à augmenter tout au long du gradient, en accordance avec le
principe de Bergmann. La densité de la population augmentait avec la température
moyenne annuelle, et toutes choses étant égales par ailleurs, les écureuils des
populations denses étaient plus gros que les écureuils des populations moins
denses. Le taux métabolique au repos augmentait avec la latitude, mais il n’y avait
pas de relation entre le taux métabolique maximum et la latitude. Sur l’ensemble,
ces résultats suggèrent que les demandes énergétiques reliées au maintient de
l’homéothermie commandent les besoins énergétiques des écureuils roux et que le
taux métabolique au repos, par opposition au taux métabolique maximum, est un
trait physiologique plus pertinent à l’écologie les écureuils. De plus, les écureuils
des latitudes élevées vivent beaucoup plus proches de leurs limites physiologiques
que les écureuils des latitudes basses.
ii
Contribution of Authors
This thesis consists of two manuscripts intended for publication, both co-authored
by Murray Humphries. As my Master’s thesis supervisor, Murray Humphries
contributed the initial experimental design and methodology, and provided critical
guidance during all stages of fieldwork, analysis, and writing.
Acknowledgements
I would like to thank my supervisor, Murray Humphries, who provided me with
the essential framework, guidance, and freedom to embark on an almost year long
field season that would test my limits as a field biologist and provide me with the
experience of a lifetime. Subsequent discussions with Murray about both my
specific results and science in general helped me grow as a scientist, for which I
am extremely grateful. Thanks to my committee members, Jim Fyles and Lauren
Chapman, who provided much appreciated feedback on my project.
I would like to thank Jean-François Aublet, who as the field technician in
the Humphries lab accompanied me during the first half of my winter field season
and taught me how to drive the trailer. Jean-François and I endured many trials
and challenges in establishing the routine that I would continue to use in the latter
half of my winter field season. I would also like to thank my other field assistants
Connie O’Connor and Catherine Henry, who were with me during the summer
and winter, respectively. Quinn Fletcher introduced me to squirrel camp and the
delicate art of respirometry, and was an inspiration to me as a new graduate
student in the Humphries lab. Thanks to all my labmates in the Humphries lab
who helped improve both of my manuscripts with their very thorough and
iii
thoughtful comments. I would also like to thank Judy Buchanan-Mappin and the
staff at the University of Calgary Kananaskis Field Station, Darrell Regimbald
and the Canfor Peace Liard Woodlands, Troy Pretzlaw, Matthew Wheatley,
Chiara Feder, and the Kluane Red Squirrel Project for their help in finding
suitable study sites. Special thanks to the many Yukon First Nations who allowed
me to work on their traditional territory.
I would like to thank my family, who have always encouraged and
supported me in everything I do, and for instilling in me my values and
appreciation of the natural world.
Thanks to the various funding agencies. Specifically, the Canadian
Foundation for Innovation New Opportunities Fund and the NSERC Northern
Research Chair and Discovery Grant programs for providing funding to Murray
Humphries. And thanks to the NSERC CGS program and the Northern Scientific
Training Program for providing me with funding.
I would be remiss if I did not thank Gabriel Blouin-Demers, Gregory
Bulté, and Marie-Andrée Carrière. It was my two years as an undergraduate in
Gabriel’s lab at the University of Ottawa that inspired me to pursue my Master’s.
Greg and Marie-Andrée always treated me as an equal and I learned a great deal
about being a field biologist from each of them.
Finally, I would like to thank Ruby, our 2005 Chevy Silverado, for being a
trooper during the 32,000 km I put her through in just over 9 months. She endured
everything from flat tires to freezing temperatures to pulling a 40 foot trailer on
nothing but fumes. I became very attached to that truck. We did it Ruby!
iv
Table of Contents
Abstract .................................................................................................................... i
Resumé.................................................................................................................... ii
Contribution of Authors ......................................................................................... iii
Acknowledgements ................................................................................................ iii
Table of Contents .................................................................................................... v
General Introduction ............................................................................................... 1
Literature Review ............................................................................................... 1
Literature Cited ................................................................................................... 7
Tables and Figures ............................................................................................ 12
Chapter 1: Geographic variation in body size and abundance in the

North American red squirrel (Tamiasciurus hudsonicus)..................................... 13
Abstract ............................................................................................................. 13
Introduction ....................................................................................................... 14
Methods ............................................................................................................ 16
Results ............................................................................................................... 19
Discussion ......................................................................................................... 20
Literature Cited ................................................................................................. 25
Connecting Statement ........................................................................................... 38

Chapter 2: Geographic variation in resting and maximum metabolic rates of the
North American red squirrel (Tamiasciurus hudsonicus)..................................... 39
Abstract ............................................................................................................. 39
Introduction ....................................................................................................... 40
Methods ............................................................................................................ 44
v
Results ............................................................................................................... 49
Discussion ......................................................................................................... 51
General Conclusion ............................................................................................... 71

vi
General Introduction
Macro-physiology is a relatively young field concerned with determining the
ecological implications of large-scale geographic variation in physiological traits.
While there has been considerable research conducted on geographic variation in
metabolism at the inter-specific level, very little is known about how energetic
traits vary within a species’ range. The objective of this thesis is to determine how
resting metabolic rate, maximum metabolic rate, body size, and population
density vary within a small mammal’s geographic distribution from near the core
of its range to near the edge of its range.
Literature Review
Metabolism, the biological process by which organisms consume, transform, and
expend energy (McNab 2002), is an important contributor to ecosystem function.
Indeed, metabolic rate is a fundamental trait that determines how much of an
individual organism’s energy can be allocated to maintenance, growth, and
reproduction. Brown et al. (2004) proposed in their “metabolic theory of ecology”
(MTE) that metabolic rate controls ecological processes at all levels of
organization. They also contended that inter- and intra-specific variation in
metabolic rate can largely be explained by two factors: body size and body
temperature. While MTE has generated considerable controversy, specifically in
the assertion of “universal” scaling factors (McNab 2008), it has also highlighted
the importance of understanding the ecological implications of metabolism.
Evaluating the ecological relevance of metabolism requires going beyond
the typical scaling with body mass to evaluate the considerable residual variation
1
present in allometric relationships. Several relevant biotic and environmental
factors such as diet (Bozinovic et al. 2007), activity level (Bryant 1997), climate
(Lovegrove 2003), season (Hayes 1989), and habitat (McNab 2009) have been
shown to affect metabolism. Latitude can serve as a reliable proxy for most, if not
all, of these variables, and has been shown to be a significant predictor of
metabolic rate at the inter-specific level in birds (Anderson & Jetz 2005) and
mammals (Lovegrove 2003; Rezende et al. 2004). However, there is a noticeable
paucity of intra-specific studies on the effect of latitude on metabolism.
Most of the studies on intra-specific metabolism and latitude have focused
on either a few populations or a small geographic scale. Bozinovic et al. (2009)
examined four populations of degus (Octodon degus) in Chili and found that basal
metabolic rate (BMR) increased with the net primary productivity of the
populations’ habitat. BMR, but not maximum metabolic rate (MMR), was found
to be higher in a population of Chroeomys olivaceus from a cold, rainy habitat in
southern Chili compared to a population from an arid, warm habitat in northern
Chile (Novoa et al. 2005). Aalto et al. (1993) performed the most intensive intra-
specific study to date, as they measured the metabolic rates of four populations of
bank voles (Myodes glareolus, formerly Clethrionomys glareolus) across a 25
degree latitudinal gradient in Europe, and found no effect of latitude on BMR.
Several other studies have examined geographic variation in intra-specific
metabolism using altitude (Hayes 1989), life-history traits (Wikelski et al. 2003)
or island occupancy (Mathias et al. 2004). Taken as a whole, however, these
intra-specific studies are rather inconclusive, and more thorough studies that
2
capture a significant range of the environmental conditions individuals experience
throughout a species’ geographic distribution are needed to properly evaluate the
effect of latitude on metabolism.
One of the most important factors in determining an animal’s overall
energy budget is body size. Any study on the energetics of multiple populations of
a species over a large geographic scale must consider the role that body size
variation may play. Specifically, when dealing with latitudinal gradients,
Bergmann’s rule (James 1970; Mayr 1956), a long-standing ecogeographic rule,
predicts that body size should increase with latitude. Bergmann’s rule has been
tested extensively, both inter- (Medina et al. 2007) and intra-specifically
(Wigginton & Dobson 1999), with most studies generally favouring the rule but
often with many exceptions. However, there is still much debate as to the possible
mechanisms that underlie Bergmann’s rule (Blackburn & Hawkins 2004).
Several hypotheses have been proposed to explain why a trend of
increasing body size with latitude may exist. The heat conservation hypothesis
suggests that larger animals, by reducing their surface area/volume ratio and
supporting thicker pelage, are better able to occupy higher latitudes and the
corresponding colder climates (Gaston & Blackburn 1999). A related idea was
proposed by James (1970), who suggested that animals in warm, moist
environments are limited by the demands of keeping cool, therefore making it
advantageous to be small bodied to speed the rate of heat loss. The dispersal
hypothesis argues that large-bodied animals are better represented at high
latitudes based on superior dispersal ability compared to small-bodied animals
3
(Blackburn & Hawkins 2004). Finally, the scarcity of resources hypothesis notes
that animals living at high latitudes must often deal with fewer and less
predictable food resources, and can mitigate this situation by increasing their
starvation time with a larger body mass (McNab 1999). However, despite the
many hypotheses and lack of clear mechanism, the extent and pattern of
geographic variation in body size throughout a species’ distribution has important
ecological implications, particularly in the impact it has on the physiology of
animals.
In terms of metabolic rate, there are two important energetic set-points for
all homeotherms – basal metabolic rate (BMR), which represents the lower limit
of energy needed to sustain basic physiological processes in a resting,
postabsorptive animal at a thermoneutral temperature, and maximum metabolic
rate (MMR), which represents the upper limit of energy an animal can expend
when its metabolic machinery (i.e. primarily locomotor muscles, but also brown
adipose tissue, visceral organs, etc.) is working at its sustainable maximum
(Weibel et al. 2004). The various metabolic traits and terms studied in this thesis
are listed in Table 1 for reference. The functional relationship between BMR and
MMR has been vigorously debated. The aerobic capacity model, for example,
suggests that natural selection acted primarily to increase maximal aerobic
capacity of endotherms, and that BMR is simply elevated as a correlated response
to MMR (Hayes & Garland 1995). A common explanation for this type of link
between BMR and MMR is that animals that have the metabolic machinery that
allow for high levels of energy processing and expenditure when active, in turn,
4
have a higher cost of maintaining that machinery when at rest, analogous to an
engine with high horse power having higher fuel requirements when idling.
Indeed, Rezende et al. (2004) found a strong positive correlation between BMR
and MMR in their inter-specific meta-analysis.
However, several authors have suggested that the selective forces acting
on BMR and MMR may differ (Rezende et al. 2004; Weibel et al. 2004). It has
been shown that animals of similar size and BMR can have substantially different
MMR, with “athletic species” having much greater metabolic scope – defined as
the ratio of MMR/BMR (Weibel et al. 1987). At the bio-physiological level,
BMR and MMR are quite distinct. When an animal is functioning at their BMR,
oxygen is consumed in all cells primarily for maintenance of cellular function and
blood flow is distributed evenly to all organs (Weibel et al. 2004). When
functioning at MMR, however, over 90% of oxygen is consumed in a single organ
system, the locomotor muscles, for ATP re-synthesis and consequently over 90%
of blood flow is directed to the locomotor muscles in response to the increased
energy demand (Weibel et al. 2004). These differences have supported the
contention that BMR and MMR are functionally distinct and serve different
purposes for animals operating in their environment.
In terms of their relationship to body size, MMR appears to scale more
steeply with mass than does BMR, possibly due to greater changes in muscle
temperature for larger mammals working at maximum capacity (Gillooly & Allen
2007 but see White et al. 2008). Nonetheless, one consequence of the differential
scaling relationship is that metabolic scope generally increases with body size.
5
In this thesis, I explore the relationship between metabolic rate (BMR and
MMR), body mass, and population density in eight populations of red squirrels
along a latitudinal gradient that spans over 3000 km in western Canada. Red
squirrels are non-hibernating diurnal tree squirrels that occur primarily in
coniferous-dominated habitat. They maintain year-round territories centered on a
midden of hoarded conifer cones (Steele 1998). Among various coniferous forest
types, red squirrels can be found throughout the western boreal region in white
spruce habitat – a mast-seeding tree that results in a large annual variation in food
supply (Steele 1998).
This study will be the first to examine, within one season, the metabolic
traits of multiple populations of a free-ranging small mammal in the field. By
documenting the relationship between metabolism and latitude within a species,
this study will add to a growing body of literature on ecophysiology, but also
provide new data and questions in the field of what we term “metabolic
geography”.
6
Literature Cited
Aalto, M., Gorecki, A., Meczeva, R., Wallgren, H., and Weiner, J. 1993
Metabolic Rates of the Bank Voles (Clethrionomys-Glareolus) in Europe
Along A Latitudinal Gradient from Lapland to Bulgaria. Annales
Zoologici Fennici 30, 233-238.
Anderson, K. J. and Jetz, W. 2005 The broad-scale ecology of energy expenditure
of endotherms. Ecology Letters 8, 310-318.
Blackburn, T. M. and Hawkins, B. A. 2004 Bergmann's rule and the mammal
fauna of northern North America. Ecography 27, 715-724.
Bozinovic, F., Munoz, J. L. P., and Cruz-Neto, A. P. 2007 Intraspecific variability
in the basal metabolic rate: Testing the food habits hypothesis.
Physiological and Biochemical Zoology 80, 452-460.
Bozinovic, F., Rojas, J. M., Broitman, B. R., and Vasquez, R. A. 2009 Basal
metabolism is correlated with habitat productivity among populations of
degus (Octodon degus). Comparative Biochemistry and Physiology A-
Molecular & Integrative Physiology 152, 560-564.
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B. 2004
Toward a metabolic theory of ecology. Ecology 85, 1771-1789.
Bryant, D. M. 1997 Energy expenditure in wild birds. Proceedings of the
Nutrition Society 56, 1025-1039.
7
Gaston, K. J. and Blackburn, T. M. 1999 A critique for macroecology. Oikos 84,
353-368.
Gillooly, J. F. and Allen, A. P. 2007 Changes in body temperature influence the
scaling of V-O2max and aerobic scope in mammals. Biology Letters 3, 99-
102.
Hayes, J. P. 1989 Altitudinal and Seasonal Effects on Aerobic Metabolism of
Deer Mice. Journal of Comparative Physiology B-Biochemical Systemic
and Environmental Physiology 159, 453-459.
Hayes, J. P. and Garland, T. 1995 The Evolution of Endothermy - Testing the
Aerobic Capacity Model. Evolution 49, 836-847.
James, F. C. 1970 Geographic Size Variation in Birds and Its Relationship to
Climate. Ecology 51, 365-390.
Lovegrove, B. G. 2003 The influence of climate on the basal metabolic rate of
small mammals: a slow-fast metabolic continuum. Journal of
Comparative Physiology B-Biochemical Systemic and Environmental
Physiology 173, 87-112.
Mathias, M. L., Nunes, A. C., Marques, C. C., Sousa, I., Ramalhinho, M. G.,
Auffray, J. C., Catalan, J., and Britton-Davidian, J. 2004 Adaptive
energetics in house mice, Mus musculus domesticus, from the island of
Porto Santo (Madeira archipelago, North Atlantic). Comparative
8
Biochemistry and Physiology A-Molecular & Integrative Physiology 137,
703-709.
Mayr, E. 1956 Geographical character gradients and climatic adaptations.
Evolution 10, 105-108.
McNab, B. K. 1999 On the comparative ecological and evolutionary significance
of total and mass-specific rates of metabolism. Physiological and
Biochemical Zoology 72, 642-644.
McNab, B.K. 2002 The Physiological Ecology of Vertebrates: A View from
Energetics. Cornell University Press, Ithica, NY, USA.
McNab, B. K. 2008 An analysis of the factors that influence the level and scaling
of mammalian BMR. Comparative Biochemistry and Physiology A-
McNab, B. K. 2009 Ecological factors affect the level and scaling of avian BMR.
Comparative Biochemistry and Physiology A-Molecular & Integrative
Medina, A., Marti, D. A., and Bidau, C. J. 2007 Subterranean rodents of the genus
Ctenomys (Caviomorpha, Ctenomyidae) follow the converse to
Bergmann's rule. Journal of Biogeography 34, 1439-1454.
Novoa, F. F., Rivera-Hutinel, A., Rosenmann, M., and Sabat, P. 2005
Intraspecific differences in metabolic rate of Chroeomys olivaceus
9
(Rodentia : Muridae): the effect of thermal acclimation in arid and mesic
habitats. Revista Chilena de Historia Natural 78, 207-214.
Rezende, E. L., Bozinovic, F., and Garland, T. 2004 Climatic adaptation and the
evolution of basal and maximum rates of metabolism in rodents. Evolution
58, 1361-1374.
Steele, M. A. 1998 Tamiasciurus hudsonicus. Mammalian Species 586, 1-9.
Weibel, E. R., Bacigalupe, L. D., Schmitt, B., and Hoppeler, H. 2004 Allometric
scaling of maximal metabolic rate in mammals: muscle aerobic capacity as
determinant factor. Respiratory Physiology & Neurobiology 140, 115-132.
Weibel, E. R., Taylor, C. R., Hoppeler, H., and Karas, R. H. 1987 Adaptive
Variation in the Mammalian Respiratory System in Relation to Energetic
Demand .1. Introduction to Problem and Strategy. Respiration Physiology
69, 1-6.
White, C. R., Terblanche, J. S., Kabat, A. P., Blackburn, T. M., Chown, S. L., and
Butler, P. J. 2008 Allometric scaling of maximum metabolic rate: the
influence of temperature. Functional Ecology 22, 616-623.
Wigginton, J. D. and Dobson, F. S. 1999 Environmental influences on geographic
variation in body size of western bobcats. Canadian Journal of Zoology-
Revue Canadienne de Zoologie 77, 802-813.
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Wikelski, M., Spinney, L., Schelsky, W., Scheuerlein, A., and Gwinner, E. 2003
Slow pace of life in tropical sedentary birds: a common-garden experiment
on four stonechat populations from different latitudes. Proceedings of the
Royal Society of London Series B-Biological Sciences 270, 2383-2388.
11
Tables and Figures
Table 1. Definitions of metabolic traits. Abb = abbreviation of terms, where
applicable.
Trait Abb. Definition

Basal metabolic BMR The minimum amount of energy needed to
rate sustain basic physiological processes in a
resting, postabsorptive animal at a
thermoneutral temperature
Resting metabolic RMR Similar to BMR, but in a non-postabsorptive
rate animal
Maximum MMR The amount of energy an animal can expend
metabolic rate when its metabolically active tissues and
organs are working at their sustainable
maximum. Measured by cold-exposure,
intense activity, or a combination of the two.
Also knows as VO2 max or summit
metabolism
Field metabolic FMR Average energy expenditure of an animal
rate under natural conditions in its environment
Metabolic scope The ratio of MMR/BMR (or RMR). Provides
an estimate of an animal’s ability to raise its
metabolism in response to thermogenic or
locomotor demands
Aerobic reserve MMR – BMR (or RMR). Similar to scope,
provides an indicator for metabolic
constraints.
Mass-specific Any expression of metabolic rate that is
metabolism expressed on a per gram basis or otherwise
corrected for the mass of the animal
Whole-body Any expression of metabolic rate that is
metabolism expressed on the level of the entire animal
12
Chapter 1: Geographic variation in body size and abundance in the
North American red squirrel (Tamiasciurus hudsonicus)
Abstract
The factors that are traditionally hypothesized to drive body size variation
according to Bergmann’s rule are typically strongly correlated with latitude. One
notable but rarely studied factor that may also contribute to intra-specific body
size variation is the local abundance of a population. We document the body size
and abundance of multiple wild populations of red squirrels (Tamiasciurus
hudsonicus) across a 3000 km latitudinal gradient. As predicted by Bergmann’s
rule, mean body mass increased with latitude and decreased with temperature and
precipitation, although the relationships were only marginally significant.
However, local abundance was also a significant predictor of body mass, with
squirrels from high-abundance sites having a larger body mass than expected
based on their latitude or climatic conditions. We suggest that a shared influence
of habitat and climatic suitability on abundance and body size may conceal or
even reverse underlying associations between climate and body size, which may
help to explain the extensive variation in the degree to which different taxa
conform to or contradict Bergmann’s rule.
13
Introduction
Body size is one of the most important life-history traits of an organism. Variation
in body size can affect the behaviour (Labonne et al. 2009) and physiology
(Lovegrove 2003) of animals. Inter- and intra-specific geographic variation in
body size has long been studied in the context of Bergmann’s rule. Originally
formulated from the observation that large-bodied animals tend to occur at high
latitudes, Bergmann’s rule (James 1970; Mayr 1956) predicts a negative
relationship between body size and latitude within endotherms. Numerous studies
have documented empirical patterns in support of (Ashton et al. 2000; Blackburn
& Hawkins 2004; Blois et al. 2008) or in contradiction (Medina et al. 2007; Yom-
Tov & Yom-Tov 2005) to Bergmann’s rule. However, while many hypotheses
attempting to explain Bergmann’s rule have been proposed (summarized in
Blackburn and Hawkins 2004), for the most part they remain controversial (see
McNab 1999) and no consensus on mechanism has emerged. This lack of
mechanism has led biologists to consider other ecologically relevant factors that
may help drive variation in body size, such as food availability (Meiri et al.
2007), species richness (Olson et al. 2009), and population dynamics (Yom-Tov
et al. 2007).
One notable, but rarely studied factor that has the potential to affect body
size variation is the local abundance of a population. Local abundance, or
population density, has been shown to affect many life-history traits in mammals
(LeBlanc et al. 2001; Pettorelli et al. 2001), birds (Bretagnolle et al. 2008; Wilkin
et al. 2006), and fish (Martinson et al. 2008). However, the vast majority of such
14
studies have examined temporal variation in abundance of a single population,
rather than geographic variation among multiple populations. Here we explore
how body size and local abundance vary between multiple populations of a wide-
spread mammal.
Although there have been many studies on intra-specific geographic
variation in body size (Ashton et al. 2000), few have been able to incorporate a
large proportion of the latitudinal range of the species in question. In addition,
many confounding factors, such as differences in abundance, inter-specific
competition, and habitat type further complicate determining why individuals
vary in body size throughout a species’ range. To address this issue, we selected
the North American red squirrel (Tamiasciurus hudsonicus) as a study species, as
it is suitable for disentangling many of the confounding factors in previous
studies. Red squirrels are common throughout Canada’s boreal region. Within one
season, we sampled squirrels from eight populations along a 3000 km latitudinal
gradient from northern Yukon (latitude 67oN) to southern Alberta (latitude 51oN),
spanning nearly the entire north-south range of the boreal forest in western
Canada (Fig. 1). This gradient thus allowed us to capture a significant portion of
the extent of variation in environmental conditions experienced by T. hudsonicus
throughout its western boreal range. Red squirrels occur primarily in coniferous-
dominated habitat, with conifer seeds as their main food source (Steele 1998),
which allowed us to control for the effect of habitat- and food-type by selecting
only white spruce (Picea glauca) stands as study sites. At our sites, T. hudsonicus
does not occur with any other Sciuridae species or other mammal species that
15
specialize on conifer seeds, vastly reducing the potential for confounding effects
on body size due to inter-specific competition for resources. We also estimated
the local abundance of squirrels at each site, which allowed us to determine if
abundance affected body size, a population-level factor that has been largely
ignored in studies on intra-specific geographic variation.
This study thus took advantage of the capacity to measure within one
season both the body size and local abundance of multiple, free-ranging
populations of a mammal across a large geographic scale. Our first objective was
to check for the presence of the “traditional” Bergmann pattern in body size
variation across the latitudinal gradient, and determine whether the pattern can be
best explained by latitude alone, or a combination of other environmental factors.
A second objective was to determine how local abundance varies across the
latitudinal gradient. Our final objective was to determine if abundance can help
predict geographic variation in body size.
Methods
We sampled red squirrels from 8 populations occurring in white spruce habitat
along a 3000 km latitudinal gradient from northern Yukon to southern Alberta,
Canada (Fig. 1). Sites were selected based on appropriate white spruce habitat
(i.e. avoiding mixed forest habitat) and road access, while trying to maintain an
even spatial distribution along the latitudinal gradient. Sampling was conducted
during the winter of 2007/2008, between late-October and early-March. To reduce
any potential seasonal bias on our results, we staggered the order of our sampling
sites as much as possible (Table 1).
16
Squirrels were live-captured using tomahawk traps baited with peanut
butter and placed on central territories at each site. Mass was recorded (± 0.1 g)
on a digital scale (Mettler PG12001 SDR), squirrels were ear-tagged for later
identification, and released back onto their territories. In addition to body mass,
we measured the left hind tarsus for all squirrels at 7 of the 8 sites as another
proxy for body size. All protocols followed the guidelines established by the
American Society of Mammalogists (Gannon & Sikes 2007) and were approved
by the Faculty of Agricultural and Environmental Sciences animal care committee
at McGill University (Animal Care Protocol #4728).
Local abundance was measured through a modified capture-
release/territory survey method. Red squirrels actively defend exclusive central
territories (middens). We thoroughly searched a given area of forest (ca. 500 m x
200 m grid) at each site to determine the number of middens, and their locations
were marked with a handheld GPS (Global Positioning System) unit (Garmin,
Olathe, Kansas, United States) and flagging tape. In winter, active middens can
easily be detected by the presence of white spruce cones and bracts above the
snowline. Red squirrels are diurnal, vocal, and vigilantly patrol their territories,
leaving noticeable snow tracks in winter (Steele 1998). We captured and marked
squirrels with ear-tags, and noted the presence of middens, snow tracks, and
territorial calls to estimate the number of squirrels present at each site. All snow
tracks were followed to a central midden. If we were unsuccessful at trapping at a
midden, we surveyed the immediate area for signs of squirrel activity. If a
territorial call was noted or a squirrel was sighted we used binoculars to record if
17
the squirrels was marked. Our estimate of squirrel abundance at each site thus
includes the total number of squirrels trapped and ear-tagged plus any additional
squirrels that were visually observed but not trapped, during an average of 110
person-hours of search effort per site. While it is possible that we did not detect
all squirrels within our study grids, we are confident that our estimate provides a
reliable index of relative abundance, particularly given the wide range of
environments and squirrel abundance within our latitudinal gradient.
Variables
Latitude and elevation were determined from GPS locations of middens at each
site. Thirty-year averages (1961-90) of temperature and precipitation (spatial
resolution of 2 km2) were determined for each site in ArcMap (ESRI, Redlands,
California, United States) using data acquired from Climate Source Inc.
(Corvallis, Oregon, United States). White spruce stand density was measured at
each site using a point sampling method with an optical prism to determine
average basal area (Kulow 1966). Data for environmental variables at each site
are presented in Table 1. We used body mass as an index of body size in this
study, but note that mean tarsus length was correlated with mean body mass for
males and females across the seven sites where both were measured (F2,11 = 5.38,
R2 = 0.49, p = 0.02). We determined local abundance by calculating the number
of squirrels per km2 at each site. GPS locations of middens were imported into
ArcMap and the Hawth’s Analysis Tools extension package was used to calculate
minimum convex polygons around middens at each site. We did not include
longitude of the sites as an explanatory variable in any statistical analyses. Given
18
that all sites were from continental, boreal forest habitat, as opposed to coastal
habitat, we had no a priori reason to suspect that variation in longitude will affect
any response variables.
Statistical Analyses
A parametric t test was used to examine if body size differed between sexes
across the gradient. Local abundance (number of detected squirrels per km2)
values were log-transformed to satisfy the assumption of normality. We used
general linear modeling and stepwise analysis to determine what factors best
predict variation in body size and abundance. All statistical analyses were
performed with JMP version 8.0 (SAS Institute, Cary, North Carolina, United
States). We defined statistical significance as p < 0.05. For the stepwise analysis,
the p-value thresholds for variables to enter and exit the model were 0.15 and 0.1,
respectively.
Results
Body size
Across the gradient, male squirrels were significantly larger than females (t =
2.88, df = 112, p = 0.005). General linear models with latitude (F1,7 = 4.10, R2 =
0.41, p = 0.089), temperature (F1,7 = 4.15, R2 = 0.41, p = 0.088), and precipitation
(F1,7 = 5.27, R2 = 0.47, p = 0.0615) as single, independent predictors of body mass
were all marginally significant. Squirrel body mass increased with latitude and
decreased with mean annual temperature and precipitation (Fig. 2). We then
included all variables (temperature, precipitation, latitude, elevation, and spruce
19
density) in a stepwise analysis to determine which variable(s) predicted body
mass. Precipitation was the only variable included in the best explanatory model.
Abundance
The general linear models of local abundance showed that abundance increased
with temperature (F1,6 = 6.96, R2 = 0.54, p = 0.039 – Fig. 3A), but did not vary
significantly with latitude (F1,6 = 3.44, R2 = 0.36 , p = 0.11 – Fig. 3B) or
precipitation (F1,6 = 1.15, R2 = 0.16, p = 0.32). Temperature was also the only
variable retained in the stepwise analysis.
Local abundance was then included with all other environmental and
biotic variables in a stepwise analysis of significant predictors of squirrel body
size variation. A model including temperature and abundance as independent
variables was deemed to be the best explanatory model (F2,7 = 5.62, R2 = 0.69, p =
0.053), and was on the cusp of statistical significance. To determine the effect of
each variable on body mass, we plotted the partial residuals of both temperature
and abundance against their respective partial residuals of mass. The partial
residuals of annual temperature decreased with the partial residuals of squirrel
body size (F1,7 = 13.3, R2 = 0.69, p = 0.011 – Fig. 4A) while the partial residuals
of abundance increased with body size (F1,7 = 5.53, R2 = 0.48, p = 0.057 – Fig
4B).
Discussion
Body size
Although all single-variable models were only marginally significant, there was a
trend for squirrel body mass to increase with latitude along the gradient, as
20
predicted by Bergmann’s rule. There was a trend for colder and drier sites to have
larger squirrels than warmer and wetter sites (Fig. 2). The high co-linearity
between latitude, temperature, and precipitation across our study sites (Table 2)
limits our ability to disentangle the best predictors of red squirrel body size.
Nonetheless, according to our stepwise analysis, precipitation was the sole
variable that was retained in the best explanatory model. Several recent intra-
specific studies of geographic variation in body size (Blois et al. 2008; Yom-Tov
& Geffen 2006) have suggested that precipitation is a main driver of body size
variation.
Abundance
Unlike our analysis of body size, only one variable, temperature, was strongly
correlated with abundance, explaining 53.7% of the observed variation (Fig. 3A).
Along the gradient, warmer sites had more squirrels per unit area than colder
sites. Temperature was also the only factor retained in the best explanatory model
of abundance in our stepwise analysis.
Had we not included abundance in our analysis of latitudinal variation in
red squirrel body size, our results would have been rather typical, namely that two
latitude-correlated climate variables, precipitation and temperature, are the best
predictors of body size variation. However, when abundance was included as a
potential explanatory variable, a much higher proportion of body mass variation
can be accounted for (71.3% vs. 52.9%) and both climate and abundance emerge
as independent predictors of body mass. All else being equal, red squirrels
occupying cold climates are larger than squirrels occupying warm climates and
21
squirrels present in high abundance are larger than squirrels present at low
abundance (Fig. 4).
It is perhaps unsurprising that variation in body size of the North
American red squirrel is correlated with environmental temperature. Because of
their small size for non-hibernating mammals in the boreal ecosystem, it is
possible that the increase in body size with decreasing ambient temperature is a
thermoregulatory adaptation to increase total heat output in the face of the high
energetic demands of endothermy in extreme cold environments (Humphries et
al. 2005). In addition to the thermoregulatory advantage, another benefit to larger
body size in colder environments with high seasonality and, presumably, lower
food availability, is an increase in fasting endurance or starvation time (Blackburn
& Hawkins 2004). While we did not measure food availability directly, the
density of spruce trees at each site decreased significantly with latitude (p =
0.019, R2 = 0.63), suggesting a declining gradient of food availability with
latitude. Both the thermoregulatory advantage and increase in starvation time are
possibilities that would favour a body size increase for squirrels in colder,
northern populations.
The local abundance of a population is an aspect that has been largely
ignored in studies of geographic variation in body size. More generally, although
spatial variation in abundance across species ranges has been treated as a general
rule of biogeography, the patterns and determinants of large scale variation in
local abundance is a critically understudied aspect of mammal ecology and
biogeography (Caughley et al. 1988; James 1970; Jarema et al. 2009; Sagarin &
22
Gaines 2002). Thus, it is unsurprising that most mammal studies that have
associated body size to population abundance involve time series approaches that
use year-to-year variation in body size as an indicator or mechanism of density
dependence. Most of these studies find a negative association between body size
and abundance over time, presumably because more individuals occupying the
same habitat means fewer resources per individual (in the absence of allee effects
– LeBlanc et al. 2001; Mysterud et al. 2001; Yom-Tov et al. 2007; Zedrosser et
al. 2006). In contrast, in the context of spatial variation in abundance across large
spatial scales, high abundance is generally assumed to reflect favorable climatic
and habitat conditions (Brown 1984; Sagarin & Gaines 2002). Contributions of
these same favorable climatic and habitat conditions to large body size could
explain why we found a positive relationship between abundance and body size.
In other words, abundance and body size might co-vary with habitat and climatic
suitability. Red squirrel abundance increased slightly from our southern-most site
to the mid-range of the gradient, then declined sharply at higher latitudes (Fig.
3B). This mid-point roughly corresponds to the center of the boreal forest region
in western Canada, which could represent the highest quality white spruce habitat
for squirrels across our gradient, assuming that habitat quality declines toward the
periphery of the boreal forest range (Curnutt et al. 1996). Alternatively, there may
be a causal relationship between abundance and body size, such that large
squirrels are able to attain higher abundance or abundant populations are able to
grow larger, but we find it difficult to identify plausible mechanisms that might
drive either form of causality.
23
The potential for body size and abundance to be positively related to both
habitat quality and climatic suitability introduces the potential for an intriguing
biogeographical contradiction. In situations where abundance declines from the
core to the edge of a species range (Brown 1984; Brown et al. 1995), but see
Sagarin and Gaines 2002), Bergmann’s rule would predict that, moving poleward
from the range center, body size would increase as average abundance declines.
Thus, in general, populations near the poleward edge of the range should have
large body size and low abundance, whereas populations in the core of the range
should have smaller body size and higher abundance, creating a negative
relationship between body size and abundance. At a coarse level, we observed the
same pattern in red squirrels; our two most northern populations had larger body
size and lower abundance than our smaller sized, more abundant southerly
populations. Yet, by sampling abundance and body size across multiple sites, it
becomes clear that at sites where body size is larger than predicted by latitude,
abundance is high, and at sites where body size is smaller than predicted,
abundance is low. This potential for correlations between abundance and body
size to mask or reverse underlying associations between climate and body size
may help to explain the extensive variation in the degree to which different taxa
conform to or contradict Bergmann’s rule (Ashton et al. 2000; Olson et al. 2009;
Yom-Tov & Yom-Tov 2005; Zedrosser et al. 2006). Better evaluation of this
possibility requires more large scale studies examining in what species and in
what ecological situations patterns of spatial variation in abundance and body size
do or do not co-vary.
24
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29
Tables and Figures
Table 1. Environmental variables for each site along the latitudinal gradient. YT =
Yukon Territory, Canada; BC = British Columbia, Canada; AB = Alberta,
Canada. Temp = mean annual temperature, Precip = annual precipitation,
Elevation = mean elevation above sea level, Spruce density = mean basal area of
white spruce stand.
Site Dates sampled Latitude Temp Precip Elevation Spruce

(d/m/y) (oN) (oC) (mm) (m.a.s.l) density (m2)
Rock River, YT 25/10/07 – 4/11/07 66.91 -6.7 398 471 25.1
Stewart Crossing, 8/11/07 – 19/11/07 63.36 -3.8 379 520 34.8
YT
Montague, YT 16/2/08 – 24/2/08 61.82 -3.2 281 615 31.9
Kluane, YT 2/3/08 – 10/3/08 60.95 -2.3 400 917 34.0
Prophet River, 24/11/07 – 2/12/07 58.32 -0.1 564 617 23.8
BC
Hinton, AB 7/12/07 – 18/12/07 53.47 1.6 639 1330 44.6
Nordegg, AB 1/2/08 – 10/2/08 52.46 1.0 595 1458 54.0
Kananaskis, AB 15/1/08 – 29/1/08 51.04 1.4 695 1517 44.5
30
Table 2. Linear least-square correlations between environmental variables for the
eight sites along the latitudinal gradient.
Temperature Precipitation Spruce Elevation Latitude

density
Latitude -0.9655 -0.8708 -0.7915 -0.9329 1
Elevation 0.8381 0.8041 0.8902 1
Spruce density 0.6799 0.5723 1
Precipitation 0.8379 1
Temperature 1
31
Figure 1. Map of study sites (triangles) across western Canada.
32
A
280
260
240
Body mass (g)
220
200
180
160
50 52 54 56 58 60 62 64 66 68
Latitude
280
260
240
Body mass (g)
220
200
180
160
-8 -6 -4 -2 0 2 4
o
Temperature ( C)
33
C
280
260
240
Body mass (g)
220
200
180
160
200 300 400 500 600 700 800
Precipitation (mm)
Figure 2. Mean body mass (± SE) of squirrels increased with (A) latitude and
decreased with (B) mean annual temperature and (C) annual precipitation.
34
A
2.8
Abundance (log individuals/km2)

2.6
2.4
2.2
2.0
1.8
-8 -6 -4 -2 0 2 4
o
Mean annual temperature ( C)
B
2.8
Abundance (log individuals/km )
2
2.6
2.4
2.2
2.0
1.8
50 52 54 56 58 60 62 64 66 68
Latitude
Figure 3. Abundance of squirrels declined with (A) mean annual temperature and
did not vary significantly with (B) latitude.
35
A
2
Parital residual of temperature
-1
-2
-3
-4
-5
180 200 220 240 260
Partial residual of mass
2
Parital residual of temperature
-1
-2
-3
-4
-5
180 200 220 240 260
Partial residual of mass
Figure 4. Partial residuals of (A) mean annual temperature and (B) abundance
against the partial residuals of squirrel body mass from the

36
temperature/abundance linear model. The partial residuals of temperature
decreased with the partial residuals of squirrel body size, while the partial
residuals of abundance increased with body size.
37
Connecting Statement
In Chapter 1, it was shown that there is a trend of increasing body mass with
latitude among the eight red squirrel populations sampled along the latitudinal
gradient. Body mass variation has important consequences in terms of its impact
on physiology and energetic traits. Chapter 2 examines how two key energetic
traits, resting and maximum metabolic rate, vary along the gradient and the results
are evaluated and discussed in light of the body mass variation documented in
Chapter 1.
38
Chapter 2: Geographic variation in resting and maximum metabolic rates of
the North American red squirrel (Tamiasciurus hudsonicus)
Abstract
While metabolic rate is known to scale with mass, there is a significant amount of
residual inter- and intra-specific variation that can be partially explained by
differences in climate, temperature, and habitat. This study is the first to examine
large-scale intra-specific variation in the metabolic rate of a small mammal. We
examined variation in resting and maximum metabolic rate (RMR and MMR,
respectively) of the North American red squirrel (Tamiasciurus hudsonicus) by
sampling individuals from eight populations along a latitudinal gradient from near
the core to near the edge of the species’ range. We found that RMR increased
with latitude, suggesting that the demands of maintaining homeothermy are
driving red squirrel energetics. However, MMR did not vary with latitude, which
taken with our RMR results, show that red squirrels at high latitudes operate
closer to their physiological limits than squirrels at lower latitudes.
39
Introduction
Metabolic rate is known to scale across all taxonomic groups according to well-
known relationships that are dictated primarily by body mass (Brown et al. 2004;
McNab 2008). However, there remains a significant amount of residual variation
that can be partially explained by a suite of biotic and environmental factors such
as diet (Bozinovic et al. 2007), activity level (Bryant 1997), latitude (Anderson &
Jetz 2005), climate (Lovegrove 2003), season (Hayes 1989a), and habitat (McNab
2009). Latitudinal gradients simultaneously capture a significant portion of the
variation in most, if not all, of these factors. It is therefore unsurprising that
latitude has often been used as a proxy to examine underlying variation in
metabolic rate.
Most of our understanding of how metabolic rate varies with latitude is at
the inter-specific level, summarized in several meta-analyses published in recent
years. Lovegrove (2003) and Rezende et al. (2004) showed that the basal
metabolic rate (BMR) of small-mammals increased with latitude in both the
northern and southern hemispheres. Similarly, Anderson & Jetz (2005)
demonstrated that the field metabolic rate (FMR) of 248 avian and mammalian
populations increased with latitude. However, despite numerous inter-specific
studies on the effect of latitude on metabolic rate, there have been very few
examinations of this question at the intra-specific level. This paucity is likely due
to the methodological challenges of efficiently capturing and measuring
metabolism of animals in multiple, geographically separate populations.
40
Despite the logistic challenges, several authors have attempted to address
the question of geographic variation and intra-specific metabolism. A summary of
intra-specific studies on geographic variation in metabolic rate is presented in
Table 1. In terms of geographic scale and number of populations studied, Aalto et
al. (1993) is the most thorough examination of intra-specific metabolism to date.
They measured the metabolic rate of four populations of bank voles (Myodes
glareolus, formerly Clethrionomys glareolus) across a 25 degree latitudinal
gradient in Europe, and found no effect of latitude on BMR. However, their site
selections (i.e. a mountainous southern site compared to low-lying northern sites)
offset many of the expected environmental correlates that are common across
latitudinal gradients. Taken as a whole, intra-specific studies on the effect of
latitude and metabolism are rather inconclusive (Table 1), primarily because no
studies to date have captured a significant range of the environmental conditions
individuals experience throughout a species’ geographic distribution.
When considering how metabolic rate may be expected to vary across the
latitudinal range of a homeotherm’s geographic distribution, particularly towards
the poleward range limit, two important factors must be considered: the energy
demands of maintaining homeothermy and the energy supply provided by food
resources. The demand of maintaining homeothermy in cold, thermally
challenging environments has often been suggested to favour selection of high
BMR to increase heat production and therefore thermoregulatory capacity. This
hypothesis is mainly based on the assumption that BMR and maximum metabolic
rate (MMR) are functionally linked, with the latter also assumed to be the true
41
measure of thermoregulatory capacity or cold-tolerance (Rezende et al. 2004).
From the low latitude perspective, a companion theory is that higher
environmental temperatures could favour a low BMR in response to overheating
and water conservation (Krol et al. 2003; Shkolnik & Schmidtnielsen 1976). In
terms of the supply of energetic resources, it is important to remember that a high
BMR is energetically costly, and populations at the periphery of a species’ range
tend to be limited in terms of resources (Curnutt et al. 1996; White 2008).
Selection may therefore favour a lower BMR at extreme high latitudes in response
to decreasing or less predictable resources (McNab 1999). In summary, if the
demand of homeothermy is driving a species’ energetics, then we would expect
metabolic rate to increase with latitude across its distribution, while if the supply
of energetic resources is the driving force, we would expect metabolic rate to
decrease at high latitudes, especially approaching the species’ range limit.
The objective of this study is to determine how the metabolism of a wide-
ranging small mammal varies across a large-scale latitudinal gradient. More
specifically, we seek to determine the direction of the relationship between
metabolism and latitude. As a secondary objective, we will determine if latitude
or a combination of other environmental factors can best predict variation in
metabolism. We consider two important energetic traits, RMR and MMR. RMR is
similar to BMR, in that it represents the lower limit of energy needed to sustain
basic physiological processes in a resting animal at a thermoneutral temperature,
with the caveat that the animal does not have to be in a postabsorptive state (i.e. it
can be digesting food). RMR is preferable to BMR for our study as a non-
42
postabsorptive state is an important criterion to maintain normal behaviour in
small mammals (Speakman et al. 2004). MMR represents the upper limit of
energy an animal can expend when its metabolically active tissues and organs
(primarily locomotor muscles) are working at their sustainable maximum (Weibel
et al. 2004).
We chose the North American red squirrel (Tamiasciurus hudsonicus) as a
model species as it has an extensive geographic range which encompasses the
entire north-south range of the boreal region in western Canada. Red squirrels are
a very interesting species from a energetics perspective, as they do not hibernate
and are among the smallest boreal mammals active above the snow throughout the
winter (Pruitt & Lucier 1958), thus exposing them to harsh winter conditions.
Their small size makes them well suited to this type of study, as it has been
suggested that small mammals should show greater metabolic adaptations in
response to cold climates, due both to a higher surface area/volume ratio and
structural restrictions in their ability to reduce heat loss via increases in pelage
thickness (Steudel et al. 1994). Red squirrels cache conifer cones in the fall to
serve as their main winter food source (Steele 1998). By selecting only white
spruce (Picea glauca) stands as study sites, we were able to minimize spatial
variation in habitat- and food-type. Within one season, we sampled squirrels from
eight populations along a latitudinal gradient that spanned over 3000 km from
southern Alberta (latitude 51oN) to northern Yukon (latitude 67oN), approaching
the northern limit of the species’ distribution and covering nearly the entire north-
south range of the boreal forest in western Canada (Chapter 1, Fig. 1).
43
In any comparative study of whole-body RMR, both inter- and intra-
specifically, one important issue to consider is mass differences between groups
(Hayes 2001). In this case it is especially important as we have previously
documented a Bergmann’s rule trend of increasing body mass with latitude
among our red squirrel populations (Chapter 1). With prior knowledge that mass
increased with latitude, we might expect whole-body RMR and MMR to increase
with latitude as well. However, if selection favours a decrease in RMR with
latitude, possibly due to resource limitations, the mass-RMR relationship might be
superseded by selection for reduced “whole-body” and/or “mass-specific” RMR
at high latitudes. Thus, we seek to examine whether whole-body and/or mass-
specific rates of resting and maximum metabolism increase with latitude, as might
be expected if thermoregulatory demands drive metabolic variation, or decrease
with latitude, as might be expected if resource supply drive metabolic variation.
Methods
Study sites
Environmental variables for all eight study sites are presented in Table 1 of
Chapter 1. All sites were characterized by a dominance (> 80% of trees with a
diameter at breast height > 5 cm) of white spruce trees. Our study was conducted
during the winter of 2007/2008, between late-October and early-March. We
specifically chose winter months because they are an energetically stable time of
year for red squirrels, with no additional energetic demands such as mating,
lactation, or cone hoarding (Humphries et al. 2005; Steele 1998). Ideally, all
squirrels would have been sampled during roughly the same period in winter.
44
However, since the logistics of our study necessarily involved sampling over
months instead of days, we staggered the order of our sampling sites as much as
possible, to reduce any potential seasonal bias on our results (Chapter 1, Table 1).
Metabolic measurements – resting metabolic rate
This study took advantage of a mobile energetics laboratory, a 11-m cargo trailer
that contains all the equipment necessary to perform respirometry and can be
towed with a truck from site to site. Upon arriving at a site, a given area of forest
would be surveyed, and red squirrels were live-captured using tomahawk traps
baited with peanut butter that were placed on the squirrels’ central territories
(middens). Squirrels were trapped in the afternoon (between 13h00 and 19h00)
and immediately taken to the mobile laboratory where they were provided with ad
libitum peanut butter for food and apple slices for moisture. Body mass was
measured using a ± 0.1 g scale (Mettler PG12001 SDR) prior to metabolic
measurements. Because red squirrels are diurnal, metabolic trials were started at
minimum two hours following sunset to increase the likelihood that individuals
would rest.
Resting metabolic rate was measured using a positive pressure, flow-
through respirometry system. Squirrels were maintained in four liter plexiglass
metabolic chambers (Qubit, Kingston, Ontario, Canada) that were placed in
environmental chambers (Espec North America Inc., Hudsonville, Michigan,
USA) set to a constant temperature (24° C), which is within the thermoneutral
zone of red squirrels (Pauls 1981). The metabolic chamber rested on a motion
activity detector (MAD-1, Sable Systems International Ltd, Nevada, USA) that
45
provided an index of the squirrel’s activity throughout the trial. Fresh outdoor air
that had been scrubbed of CO2 and water via soda lime and Drierite©,
respectably, was pumped through each chamber at a constant rate of 700 ml/min.
Ex-current air from each chamber was sub-sampled at 200 ml/min, scrubbed of
CO2 and moisture, and sent to an oxygen analyzer (Oxzilla-II, Sable Systems
International Ltd, Nevada, U.S.A.). A computerized data acquisition system
(Sable Systems, RM8 Intelligent Multiplexer) was used to baseline the oxygen
analyzer with fresh scrubbed air at 12 minute intervals throughout the trial.
Oxygen consumption values were stored and analyzed using Expedata 1.0.18 data
management software by Sable Systems. Trial runs were corrected for equipment
drift and RMR was calculated by determining the lowest level of oxygen
consumption recorded for a minimum of 180 consecutive seconds during the ca.
2-3 hour trial. Squirrels were then ear-tagged, and released back onto their
territories after their metabolic traits were measured.
Metabolic measurements - maximum metabolic rate
For a subset of squirrels in six of the eight populations sampled, we recorded
maximum metabolic rate (MMR) following their RMR trial. MMR was recorded
in all populations except Hinton, AB and Kluane, YT. MMR is typically
measured as the highest rate of oxygen consumption in response to cold-exposure,
forced exercise, or a combination of the two (Rezende et al. 2004). MMR trials
commenced once the temperature of the environmental chamber was brought
down to 0oC, at which point the incurrent outdoor air was replaced with a mixture
of ca. 79% helium and 21% oxygen (helox). Helox is commonly used to induce
46
cold-exposure MMR as it increases thermal conductance compared to regular air
(Rosenmann & Morrison 1974). Using heated models, (Thomas et al. 1998) found
that under a helox atmosphere, heat flux increased 1.8 – 2.5 times that of regular
air depending on whether thermal conductance or convection was the dominant
form of heat loss. In addition to helox exposure, we lowered the temperature of
the environmental chamber to approximately -25oC at the maximum rate possible
(ca. 10oC/hour). Due to the risk of hypothermia, the squirrels’ oxygen
consumption values were constantly monitored throughout the trial, with manual
baseline measurements only being taken at the beginning and end of the MMR
trial. Typically, oxygen consumption would steadily increase until a rapid drop
occurred, at which point the squirrel could no longer increase its metabolic rate to
maintain homeothermy (Rosenmann & Morrison 1974). The highest oxygen
consumption for 300 consecutive seconds was taken as MMR. We chose to
slightly increase this time period for MMR compared to RMR as MMR values for
some squirrels occasionally “spiked” dramatically for short, unsustainable periods
of time (i.e. 10 – 30 seconds).
Activity
During the MMR trials, squirrels would typically respond to cold-exposure in two
ways – by being highly active or by being highly inactive. We quantified their
activity by calculating an activity index from the motion activity detector. The
output of the motion activity detector is an oscillating line that deviates from its
mean in both the positive and negative direction when it detects movement. Our
index of activity was calculated by multiplying the coefficient of variation (cv) of
47
the output of the motion activity detector by a factor of 104. A high cv therefore
corresponds to high activity while low cv corresponds to low activity. During one
of the MMR trials, the MAD detector was not functioning. We were therefore
able to classify 46 of the 47 squirrels sampled for MMR.
Environmental variables across latitudinal gradient
Latitude and elevation were determined from GPS locations of middens at each
site. Thirty-year averages (1961-90) of temperature and precipitation (spatial
resolution of 2 km2) were determined for each site in ArcMap (ESRI, Redlands,
California, United States) using data acquired from Climate Source Inc.
(Corvallis, Oregon, United States). White spruce stand density was measured at
each site using a point sampling method with an optical prism to determine
average basal area (Kulow 1966).
Statistical Analyses
We used general linear modeling and stepwise analysis to determine what factors
best predict variation in RMR and MMR along the latitudinal gradient. All
statistical analyses were performed with JMP version 8.0 (SAS Institute, Cary,
North Carolina, United States). We defined statistical significance as p < 0.05. For
the stepwise analysis, the p-value thresholds for variables to enter and exit the
model were 0.15 and 0.1, respectively.
Animal care
All protocols followed the guidelines established by the American Society of
Mammalogists (Gannon & Sikes 2007) and were approved by the Faculty of
48
Agricultural and Environmental Sciences animal care committee at McGill
University (Animal Care Protocol #4728).
Results
RMR and latitude
Latitude was the best predictor of RMR, and was the only variable retained in the
stepwise analysis. RMR significantly increased with latitude (R2 = 0.836, p =
0.0015, F1,6 = 30.7, n = 8 – Fig. 1). RMR also increased with mass for all 105
squirrels sampled across the gradient (R2 = 0.186, p < 0.0001, F1,103 = 23.5). As
reported in Chapter 1, there was a trend for the mean population mass to increase
with latitude (R2 = 0.402, p = 0.091, F1,6 = 4.03, n = 8). However, on a “mass-
specific” level, the mean population residuals from the mass-RMR relationship
increased with latitude as well, although the relationship was only marginally
significant (R2 = 0.417, p = 0.084, F1,6 = 4.29, n = 8 – Fig. 2).
MMR and activity
The squirrels were able to withstand extreme cold temperatures for an
unexpectedly long time. Active squirrels took an average time of 79 minutes
under a helox atmosphere to elicit MMR, while inactive squirrels took an average
of 114 minutes to elicit MMR, with prevailing air temperatures less than -20oC
(made colder yet by the 1.8-2.5 fold increase in heat loss at a given temperature
induced by helox exposure).
MMR was significantly and positively related to RMR among the 45
squirrels on which we measured both traits (R2 = 0.090, p = 0.046, F1,43 = 4.24, n
= 45 – Fig. 3A). However, both the frequency plot and kernel density plot of the
49
activity index of squirrels during the MMR trials was bimodal indicating two
distinct groups corresponding to high activity and low activity squirrels (Fig. 4A
and 4B). Therefore, to determine if activity affected MMR, squirrels were
classified into one of the two activity categories. The MMR calculated from
inactive squirrels (activity index < 35) represents “cold-induced MMR” while that
from active squirrels (activity index > 25) represents “cold-and-activity-induced
MMR” (Rezende et al. 2004). One squirrel had an intermediate activity index
between 25 and 35, and therefore was not categorized as either active or inactive
to ensure a distinct gap in activity between the two groups. Including activity in
the general linear model with RMR explained significantly more variation in
MMR (R2 = 0.46, p < 0.0001, F2,40 = 17.3, n = 43 –3b; model F-test p < 0.001 –
Fig. 3B).
Similar to RMR, MMR increased significantly with body mass (R2 = 0.22,
p = 0.0008, F1,45 = 12.9, n = 47 – Fig. 5A). And once again, adding activity to the
general linear model with body mass explained significantly more variation in
MMR (R2 = 0.52, p < 0.0001, F1,43 = 14.9, n = 45 – Fig. 5B; model F-test p <
0.001). There was also a significant interaction between mass and activity
category. Cold-and-exercise-induced MMR increased more rapidly with body
mass than cold-induced MMR (Fig. 5B).
While we chose to classify activity into two discrete categories, our results
are robust to treating the activity index as a continuous variable. MMR increased
in a similar fashion both with RMR and activity (R2 = 0.47, p < 0.0001, F2,41 =
50
18.0, n = 44), and with body mass and activity (R2 = 0.43, p < 0.0001, F2,43 =
16.2, n = 46).
MMR and latitude
MMR, unlike RMR, did not vary with latitude, nor any other
environmental variable. While the overall model of MMR including latitude and
activity category was significant (R2 = 0.53, p = 0.049, F2,8 = 4.5, n = 8 – Fig.
6A), latitude was not a significant factor (F1,8 = 0.97, p = 0.35). In addition to
there being no trend with whole-body MMR, there was no relationship between
mass-MMR residuals and latitude (F2,8 = 0.13, p = 0.88). There was a trend,
however, for metabolic scope (MMR/RMR) to decrease with latitude (F1,8 = 3.9, p
= 0.084 – Fig. 6B).
Discussion
Resting metabolic rate and latitude
Resting metabolic rate was very highly correlated with latitude across the gradient
(Fig. 1), remarkably explaining over 87% of the observed variation among the
eight populations of red squirrels. Moreover, RMR clearly increased along the
gradient, peaking at the northern-most site. We predicted that if thermoregulatory
demands of maintaining homeothermy are the driving force behind red squirrel
RMR, metabolic rate should increase with latitude. On the other hand, if the
supply of energy resources is the driving factor, we predicted that metabolic rate
should decrease with latitude. Our results clearly show that RMR increased along
the gradient, peaking at the northern-most site, suggesting that the demands of
maintaining homeothermy are driving red squirrel RMR. Furthermore, while we
51
were unable to directly measure food availability at each site, the density of
spruce trees significantly declined with latitude (Chapter 1, Table 2). We also
found that the population density of red squirrels declined sharply at the two
northern-most sites (Chapter 2, Figure 3A and 3B). Both of these results suggest
that energy resources were likely less available at the highest latitude sites, where
red squirrel RMR was highest, further strengthening our argument that the
demands of maintaining homeothermy drive red squirrel RMR along the gradient.
Latitude was a better predictor of RMR compared to any other
combination of temperature, precipitation, elevation, and white spruce density. It
is not entirely surprising that latitude is better at predicting RMR than any other
environmental or biotic variables, considering that it is such a holistic and
integrative variable itself. It has been suggested that latitude may be a better
predictor of long-term climate trends that operate closer to an evolutionary time
scale (i.e. thousands of years) than weather data that has been collected for shorter
periods of time (i.e. decades) (Rezende et al. 2004). In addition, many other
factors such as food availability, habitat suitability, seasonality, and
environmental unpredictability may vary with latitude, and often in a non-linear
fashion (Lovegrove 2003). Among our environmental variables, there were strong
linear correlations between latitude and temperature (R2 = 0.93), elevation (R2 =
0.87), precipitation (R2 = 0.76), and white spruce density (R2 = 0.63).
A pertinent question to ask regarding our RMR results is whether the
increase in whole-body RMR with latitude is driven by the trend of increasing
body mass we documented in Chapter 1. In order to test for this, we used the
52
residuals of the overall mass-RMR relationship to obtain a mean “mass-specific”
RMR for each population. There was a trend of increasing mass-RMR residuals
with latitude (Fig. 2), indicating that populations at high latitudes have higher
resting metabolic rates than predicted from mass alone. However, this is not to
over-shadow the primary importance of the whole-body RMR-latitude
relationship. It has repeatedly been noted in ecological studies that animals live at
the whole-body, and not mass-specific, level (McNab 1999), and we ignore
whole-body relationships at our own peril. Regarding our populations of red
squirrels, it is entirely plausible that the increase in body size is a metabolic
adaptation to increase whole-body RMR for the purpose of heat production and
conservation. One of the simplest ways selection can act on overall energy
budgets is through changes in body size (McNab 2002). Thus, the overall increase
in RMR with latitude, combined with the trend of increasing mass-RMR
residuals, support the hypothesis that the demands of maintaining homeothermy
in thermally challenging environments is driving latitudinal variation in red
squirrel metabolism.
Maximum metabolic rate and resting metabolic rate
Across the gradient we originally found a significant, but weak, positive
correlation between MMR and RMR, with RMR explaining only 9% of the
observed variation in MMR (Fig. 3A). However, the bimodal nature of the
frequency plot and kernel density plot of the activity index (Fig. 4A and 4B)
supports our original observation that squirrels exhibited two distinct behavioural
responses to the helox-induced cold exposure – high activity and low activity.
53
Indeed, adding activity as a categorical variable to the general linear model with
RMR explained significantly more variation in MMR, greatly increasing the
explanatory power from 9% to 46% (Fig. 3B). This result is important considering
that despite the functional relationship between MMR and RMR (or BMR) not
being fully known, several major theories regarding the evolution of endothermy
and BMR make assumptions or predictions regarding these two metabolic traits
being linked (Hayes & Garland 1995). While significant correlations between
BMR and MMR have been reported at the inter-specific level in birds
(Dutenhoffer & Swanson 1996) and rodents (Rezende et al. 2004), it has rarely
been documented in comparative studies at the intra-specific level (but see Hayes
1989b).
Maximum metabolic rate and latitude
Despite RMR increasing with latitude, and its correlation with MMR, there was
no relationship between MMR and latitude (Fig. 6A). This result is rather
surprising given that MMR, more so than RMR, is considered a standard measure
of a homeotherm’s ability to withstand low environmental temperatures. Given
that all active animals must, by definition, operate within their environment at
levels of energy expenditure greater than their RMR, a homeotherm’s ability to
tolerate cold ambient temperatures is often estimated by metabolic scope
(MMR/BMR or RMR) (McNab 2002) or aerobic reserve (MMR – FMR)
(Ochocinska & Taylor 2005). Indeed, inter-specific comparative work has found
that species from cold climates have higher MMRs (Bozinovic & Rosenmann
1989; Sparti 1992). It is assumed that a higher MMR, and accompanying greater
54
metabolic scope or aerobic reserve, would confer on animals a higher “metabolic
ceiling”, which would aid in thermoregulating in cold climates, particularly for
small mammal with high surface area/volume ratios. The reasoning is sound – a
lower metabolic scope or aerobic reserve, in theory, means that the animal has a
smaller capacity to raise its metabolic rate in the face of increased energy
demands. However, because RMR increased with latitude in our populations of
red squirrels while MMR did not, we actually found a trend of decreasing
metabolic scope with latitude (Fig. 6B). This result is even more surprising
considering that metabolic scope generally increases with body size (McNab
2002). While it may seem counter-intuitive, perhaps RMR is a more ecologically
relevant trait than MMR for red squirrels exposed to thermally challenging winter
environments. While at a broad scale, energy expenditure in endotherms is
negatively related to temperature (Anderson & Jetz 2005), this relationship may
not hold for small mammals in cold environments. Previous work on one of the
population sampled from the Yukon (Kluane) revealed that FMR of squirrels
actually decreased with colder ambient temperatures in the winter (Humphries et
al. 2005). Essentially, red squirrels are able to take advantage of their thermally
buffered micro-environments (well-insulated nests) and secure winter food source
(cone cache) to be more active on warmer winter days and spend less energy at
colder temperatures. By increasing the amount of time being inactive in their
nests on colder days, red squirrels can spend a greater portion of their time living
at energy levels closer to RMR than MMR; RMR may thus be the more
ecologically relevant metabolic trait, and selection may have favoured an elevated
55
RMR rather than MMR. Our results suggest that despite the energetic costs, red
squirrels at high latitudes operate closer to their physiological limits than squirrels
at lower latitudes.
Substitutive vs. additive thermogenic costs during MMR
Due to the nature of our MMR and activity data – with “cold-induced” MMR and
“cold-and-exercise-induced” MMR – there is a question regarding metabolic
scope that, while we initially did not design the study to answer, we have the
potential to address. One long-standing issue regarding endotherm energetics is
whether heat derived from locomotor activity can substitute for thermoregulatory
heat production. More specifically, if the costs of thermogenesis and exercise are
substitutive, then metabolic scope should be fixed and MMR during cold-
exposure should be the same as MMR during exercise and cold-exposure. This
situation would likely arise if there is an intrinsic constraint to the production of
heat by brown adipose tissue (BAT – thermogenesis) and skeletal muscles (both
thermogenesis and exercise), likely from nutrient limitation from the central
supply system. However, if the costs are additive, meaning that BAT and skeletal
muscles act independently of each other and that the central supply system can
handle both demands simultaneously, then metabolic scope should increase
during combined exercise and cold-stress compared to either demand alone. Our
results suggest that the costs of thermogenesis and maximal exercise are additive
in red squirrels, as they have the capacity to raise their MMR, and therefore
metabolic scope, in response to “exercise” during cold-exposure. Squirrels that
were highly active during MMR trials had significantly higher MMRs than
56
squirrels that were highly inactive (Fig. 5B). To our knowledge there has been
only one other study to date that has compared cold-induced MMR and cold-and-
exercise-induced MMR in small mammals. And in contrast to our results,
Chappell and Hammond (2004) found that deer mice had a fixed metabolic scope;
cold-and-exercise induced MMR was the same as cold-induced MMR. However,
it should be noted that we did not specifically design our study to test for the
effect of cold-and-exercise-induced MMR, which is usually elicited from forced
exercise via a running wheel or treadmill.
57
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63
Tables and Figures
Table 1. Summary of intra-specific studies on geographic variation in
metabolic traits. Direction of metabolic traits with main environmental
variable(s) indicated by + (positive effect), - (negative effect), or 0 (no
effect). BMR = basal metabolic rate; RMR = resting metabolic rate; MMR
= maximum metabolic rate; FMR = field metabolic rate.
Study Species No. of Main Trait, effect

populations environmental
variable
Bozinovic et al. Octodon 4 Primary BMR (+)
(2009) degus productivity
Broggi et al. Parus 2 Latitude BMR (+)
(2007) major
Novoa et al. Chroeomys 2 Precipitation, BMR (+, -)
(2005) olivaceus Temperature MMR (0, 0)
Mathias et al. Mus 2 Island BMR (-)
(2004) musculus occupancy
domesticus
Wikelski et al. Saxicola 4 Migratory RMR (+)
(2003) torquata ability
Aalto et al. Myodes 4 Latitude BMR (0)
(1993) glareolus
Hayes Peromyscus 2 Altitude BMR (+)
(1989a) maniculatus FMR (0)
MMR (0)
64
Figure 1. Whole body metabolic rate (VO2 ml/hr) ± SE vs. latitude for the eight
populations of red squirrels sampled along the latitudinal gradient.
65
Figure 2. Mass-RMR residuals ± SE vs. latitude for the eight populations of red
squirrels sampled along the latitudinal gradient.
66
A
Figure 3. (A) MMR (VO2 ml/hr) vs. RMR (VO2 ml/hr) for the 45 squirrels across
the gradient that had both metabolic traits measured. (B) MMR vs. RMR for
active compared to inactive squirrels (n = 43). Filled circles = active, open circles
= inactive.
67
A
Figure 4. (A) Frequency plot of squirrel activity index from MMR trials (n = 44).
Bin size = 10, with upper value as label. (B) Kernel density plot of activity index
from MMR trials.
68
A
Figure 5. (A) MMR (VO2 ml/hr) vs. body mass (g) for 47 squirrels across the
latitudinal gradient. (B) MMR vs. body mass for active compared to inactive
squirrels (n = 45). Filled circles = active, open circles = inactive
69
A
Figure 6. (A) MMR (VO2 ml/hr) ± SE vs. latitude for six populations along the
latitudinal gradient, for active compared to inactive squirrels. (B) Metabolic scope
(MMR/RMR) ± SE vs. latitude for the same populations along the gradient. Filled
circles = active, open circles = inactive
70
General Conclusion
This thesis documented how metabolic rate, body size, and population density of
red squirrels varied along a 3000 km latitudinal gradient in western Canada. This
study is the first to document these traits in multiple free-ranging populations of a
mammalian species over such a large geographic scale.
In the first chapter I showed that there was a trend of increasing body
mass along the gradient, consistent with the prediction of Bergmann’s rule. Red
squirrels at high latitudes are larger than conspecifics at lower latitudes. In
addition, I showed that local abundance increased with mean annual temperature
across the gradient. However, a particularly notable but initially counter-intuitive
result was that all else being equal, squirrels present in high abundance were
larger than squirrels present at low abundance. I suggest that the possibility exists
that abundance and body size co-vary with habitat suitability. If this were the
case, the positive association between body size and abundance in populations
near the northern limits of species’ distributions may potentially mask or dampen
the Bergmann trend of increasing body size with latitude.
In the second chapter I documented how RMR and MMR varied among
the eight populations along the gradient. Both whole-body and mass-specific
RMR increased with latitude, though the later was only marginally significant,
suggesting that it is the demands of maintaining homeothermy, rather than the
supply of energy resources that drive red squirrel metabolic rate along the
latitudinal gradient. However, there was no relationship between MMR and
latitude. The combination of these two relationships led to an unexpected result,
71
namely that there was a trend where metabolic scope decreased with latitude. It
has been shown that red squirrels can take advantage of their thermally buffered
micro-environments and secure winter food source to minimize the amount of
time spent outside of their nests on cold winter days (Humphries et al. 2005). If
red squirrels spend the majority of their time in winter living at energy levels
closer to their RMR rather than their MMR, and in light of my results, I suggest
that RMR may be a more ecologically relevant metabolic trait than MMR, and
selection may have favoured an elevated RMR rather than MMR in red squirrels.
By documenting how energetic traits vary for eight populations of red
squirrels along a latitudinal gradient in western Canada, this study can be
considered a first step in a field we termed “metabolic geography”. Indeed, there
is very little data available on the patterns of spatial variation in metabolism for
different populations or closely related species. There are therefore many
questions this field can answer and directions this field can take. Do the
differences in RMR among red squirrel populations reflect different levels of
energy expenditure in the field? Does the lack of differences in MMR reflect a
common “metabolic ceiling” that is shared among populations of red squirrels
regardless of climate? And are there fitness benefits of an elevated RMR for
squirrels in northern populations? By providing interesting results and at the same
time creating many more new questions, hopefully this study can serve as the
impetus to use geographic variation in metabolic traits to answer questions of
interest to both physiologists and ecologists.
72
Literature Cited
Letters 8, 1326-1333.
73

The Metabolic Geography of The Red Squirrel (Tamiasciurus Hudsonicus)

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The Metabolic Geography of The Red Squirrel (Tamiasciurus Hudsonicus)

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The metabolic geography of the red squirrel (Tamiasciurus hudsonicus)

Department of Natural Resource Sciences

McGill University, Macdonald campus

Montreal, Quebec, Canada

A thesis submitted to McGill University in partial fulfillment

In coining the term “metabolic geography”, this thesis investigates geographic

populations along a 3000 km latitudinal gradient in western Canada. There was a

the prediction of Bergmann’s rule. In addition, abundance increased with mean

geography of red squirrels is driven more by regional variation in the demands of

maintaining homeothermy rather than the supply of resources. In addition,

than squirrels at lower latitudes.

Cette thèse étudie la géographie métabolique de huit populations d’écureuils roux

tout au long d’un gradient latitudinal de 3000 km dans l’ouest canadien. En

particulier, les variations géographiques du taux métabolique, de la taille

corporelle et de la densité de population seront examinées. La masse corporelle

avait tendance à augmenter tout au long du gradient, en accordance avec le

principe de Bergmann. La densité de la population augmentait avec la température

pas de relation entre le taux métabolique maximum et la latitude. Sur l’ensemble,

ces résultats suggèrent que les demandes énergétiques reliées au maintient de

l’homéothermie commandent les besoins énergétiques des écureuils roux et que le

taux métabolique au repos, par opposition au taux métabolique maximum, est un

que les écureuils des latitudes basses.

by Murray Humphries. As my Master’s thesis supervisor, Murray Humphries

guidance during all stages of fieldwork, analysis, and writing.

I would like to thank my supervisor, Murray Humphries, who provided me with

experience of a lifetime. Subsequent discussions with Murray about both my

am extremely grateful. Thanks to my committee members, Jim Fyles and Lauren

Chapman, who provided much appreciated feedback on my project.

I would like to thank Jean-François Aublet, who as the field technician in

delicate art of respirometry, and was an inspiration to me as a new graduate

staff at the University of Calgary Kananaskis Field Station, Darrell Regimbald

me to work on their traditional territory.

I would like to thank my family, who have always encouraged and

supported me in everything I do, and for instilling in me my values and

appreciation of the natural world.

Thanks to the various funding agencies. Specifically, the Canadian

Training Program for providing me with funding.

I would be remiss if I did not thank Gabriel Blouin-Demers, Gregory

Bulté, and Marie-Andrée Carrière. It was my two years as an undergraduate in

Gabriel’s lab at the University of Ottawa that inspired me to pursue my Master’s.

about being a field biologist from each of them.

everything from flat tires to freezing temperatures to pulling a 40 foot trailer on

Literature Cited ................................................................................................... 7

Tables and Figures ............................................................................................ 12

Chapter 1: Geographic variation in body size and abundance in the

Literature Cited ................................................................................................. 25

Tables and Figures ............................................................................................ 30

Connecting Statement ........................................................................................... 38

Literature Cited ................................................................................................. 58

Tables and Figures ............................................................................................ 64

General Conclusion ............................................................................................... 71

Macro-physiology is a relatively young field concerned with determining the

ecological implications of large-scale geographic variation in physiological traits.

While there has been considerable research conducted on geographic variation in

of its range to near the edge of its range.

Metabolism, the biological process by which organisms consume, transform, and

expend energy (McNab 2002), is an important contributor to ecosystem function.

Indeed, metabolic rate is a fundamental trait that determines how much of an

individual organism’s energy can be allocated to maintenance, growth, and

reproduction. Brown et al. (2004) proposed in their “metabolic theory of ecology”

(MTE) that metabolic rate controls ecological processes at all levels of

organization. They also contended that inter- and intra-specific variation in

temperature. While MTE has generated considerable controversy, specifically in