PHYSIOLOGICAL ECOLOGY OF FOSSORIAL MAMMALS:
A COMPAPATIVE STUDY
By
LUIS C. CONTRERAS
<(
A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF THE
UNIVEPSITY OF FLOP IDA IN PARTIAL FULFkLM^NT OF THE REQUIREMENTS
FOR THE DEGREE OF DOCTOR Of PHILOSOPHY
UNIVERSITY OF FLORIDA
1983
ACKNOWLEDGMENTS
I would like to acknowledge the people and institutions that have
encouraged, assisted, and supported me during this study.
I would like to thank the members of my committee: Dr. Brian K.
McNab, Chairman, Dr. Charles A. Woods, Dr. John F. Anderson, and Dr.
David K. Beede. A great part of the work was done in the laboratories
of Dr. McNab and Dr. Mario Rosenmann, Departamento de Ciencias
Ecologlcas, Facultad de Ciencias Basicas y Farmaceuticas , Universidad
de Chile. Part of the research was done in the laboratory of Dr. Craig
Heller, Stanford University, California, who generously let me use his
equipment .
Field work was supported by Dr. McNab, Dr. Rosenmann, and Dr.
Woods from the Florida State Museum and the Department of Zoology,
University of Florida. Invaluable field assistance was provided by
Lie. Jose Yanez V. from the Museo Nacional de Hlstorla Natural de Chile
and Juan Carlos Torres, student of biology at the Universidad de Chile.
I would like to thank Dr. James Patton from the Museum of
Vertebrate Zoology, University of California, Berkeley, for his help
during my stay there and for letting me use some of his captured
Thomomys .
li
I am very grateful to the Department of Zoology, University of
Florida, the Department of Biology, Facultad de Cienclas Basicas y
Farmaceuticas , Unlversidad de Chile, the Fulbright Commission; and the
Organization of the American States for their support.
Drs. McNab and Anderson made it possible for this work to be
written in intelligible English.
Last, but not least, I would like to thank my parents Mr. Luis C.
Contreras and Mrs. Alicia Casanova, who generously provided me with
their spiritual and material support.
ill
TABLE OF CONTENTS
ACKNOWLEDGMENTS 11
ABSTRACT vl
CHAPTER ONE INTRODUCTION 1
CHAPTER TWO BIOENERGETICS OF THE FOSSORIAL SPALACOPUS CYANUS
(OCTODONTIDAE: RODENTIA) FROM TWO ALTITUDES 3
Introduction 3
Methods 5
Results 7
Discussion 19
CHAPTER THREE METABOLIC AND THERMAL RESPONSE OF FOSSORIAL
MAMMALS TO LOW TEMPERATE AND OXYGEN PRESSURE 30
Introduction 30
Methods 31
Results 32
Discussion 61
CHAPTER FOUR ENERGETICS OF FOSSORIAL MAMMALS AND ITS RELATION
TO BODY MASS AND DISTRIBUTION 67
Introduction 67
Methods 69
Results 71
Discussion .
95
CHAPTER FIVE CONCLUSIONS
111
LITERATURE CITED 113
BIOGRAPHICAL SKETCH 120
V
Abstract of Dissertation Presented to the Graduate Council of the
University of Florida in Partial Fulfillment of the Requirements
for the Degree of Doctor of Philosophy
PHYSIOLOGICAL ECOLOGY OF FOSSORIAL MAMMALS:
A COMPARATIVE STUDY
By
Luis C. Contreras
August 1983
Chairman: B.K. McNab
Major Department: Zoology
This study evaluates the significance of some physiological
characteristics and their interpretation as adaptations to fossorlal
living mammals.
An intraspecific study of the energetics in the South American
rodent Spalacopus cyanus from low altitude and high temperature and
from high altitude and low temperature indicates that the basal rate of
metabolism is low in animals from both populations, but it is lower in
the larger anim.als from high altitudes (74 vs 85% of the value expected
from the Kleiber relation). Minimal thermal conductance is low in both
populations (80 and 85%, respectively). Tolerance to high ambient
temperature is the same in both populations; however, it is attained by
a low rate of metabolism at high altitude and by a small body mass at
low altitude. These characteristics are Interpreted as adaptations to
reduce overheating, especially in the warmer burrows at low altitude.
vl
In studying the thermal and metabolic response to low temperature
and oxygen pressure, it was found that interspecif Ically the critical
oxygen pressure was lower in fossorial than in surface dwelling
mammals. Even though the basal rate of metabolism and body mass did
not set P(,, they may be of importance in reducing respiratory stress,
because the development of hypoxia and hypercapnia is directly
proportional to these factors.
Fossorial mammals scale basal rate of metabolism according to the
function /M^ = 9.752 This function yields lower
values than expected by the Kleiber relation at body masses larger than
74.5 g and higher values at small masses. The combination of this
relationship and minimal thermal conductance determines a temperature
differential between body temperature and the lower limit of
thermoneutrality independent of body mass. Species that do not fit
this pattern at small masses have low basal rates of metabolism, high
minimal thermal conductances, live in warm environments, and are poor
thermoregulators .
These characteristics are Interpreted mainly as adaptations to
reduce overheating. Although alternative hypotheses, e.g., that these
modifications are related to hypoxia and hypercapnia, low food
availability, and the high cost of burrowing, should also be
considered .
vll
CHAPTER ONE
INTRODUCTION
One of the difficulties in comparative studies is that organisms
living in nature are exposed to multiple uncontrolled variables and to
their Interactions. Fossorial mammals seem to offer a good opportunity
for these kinds of studies, because they live in relatively stable and
well characterized environments (Rosenmann 1959, Kennerly 1964, McNab
1966, Studier and Baca 1968, Studler and Proctor 1971, Arlell 1979).
Moreover, fossorlality has evolved in several different taxa; i.e.,
marsupials, edentates, Insectlvores , and rodents; thus, by studying
them we can distinguish the characteristics related to fossorlality
from those Independent of it. Several morphological characteristics in
these anim.als have been Indisputably attributed to this mode of life
(Eloff 1951, Dubost 1968, Hildebrand 1974, Topachevskii 1969/1976).
[^Several respiratory and energetic characteristics of these
animals, such as low critical oxygen pressure, low rate of metabolism,
and body size, have been proposed as adaptations to hypoxia and
hypercapnia (Baudinette 1972, Ariel! et al. 1977, Arlell and Ar 1981b),
to overheating (McNab 1966, 1979), to low food availability (Jarvis
1978), or to the high cost of burrowing (Vleck 1979, 1981). \ These
1
2
propositions have generated some controversy, because the same
characteristics have been attributed to different selective forces.
The aim of this study was to evaluate the significance of these
characteristics and proposed explanations in fossorlal mam.mals. First,
I compare the energetics of two populations of the South American
rodent Spalacopus cyanus. One of them lives at 70 m altitude in a warm
habitat near the Pacific Ocean, the other lives at 2500 m altitude in a
colder ambient in the Andean Mountains of central Chile. Second, 1
studied the metabolic and thermal response of this and other fossorlal
mammals to low temperature and oxygen pressure to see if these animals
show a greater tolerance to hypoxia than other mammals, and if they do,
whether this lower sensitivity is related to their rate of metabolism.
Third, I present new data on the energetic parameters of 11 fossorlal
rodents from South America, North America, and Africa, and I discuss
these data and others found in the literature in relation to body size
and distribution.
CHAPTER TWO
BIOENERGETICS OF THE FOSSORIAL SPALACOPUS CYANUS (OCTOCONTIDAE :
RODENTIA) FROM TWO ALTITUDES
Introduction
A fossorlal existence has developed independently in several
mammalian orders; e.g., marsupials, insectivores , rodents, and
edentates. Adaptations to fossoriality include several physiological
as well as morphological characteristics. (jThe microenvironment faced
by fossorial mammals is relatively stable, characterized by high
relative humidity, small temperature variation, low oxygen tension, and
high carbon dioxide tensionJ(Rosenmann 1959, McNab 1966, Studier and
Baca 1968, Studier and Proctor 1971, Ariell 1979, MacLean 1981).
Several respiratory characteristics of fossorial mammals have been
regarded as adaptations to the hypoxic and hypercapnic atmosphere of
their burrows (Detweiler and Sporri 1957, Bartels et al. 1969, Quillam
et al. 1971, Darden 1972, Chapman and Bennet 1975, Lechner 1976, Ar et
al. 1977, Ariel! and Ar 1979, 1981a, b). In general, all of these
studies indicate a high H^,-02 affinity, low 850* high O2
capacity, high buffering capacity of blood pH, reduced sensitivity to
CO2, low respiratory frequency, small respiratory dead space, low
tissue PO2, and low heart rate.
The energetics of fossorial mammals have been studied by several
authors; however, there has been no complete agreement on the data or
in their Interpretation. In the first comparative study on energy
3
4
expenditure of fossorial mammals, McNab (1966) included five species of
herbivorous rodents. Q.ow metabolic rate and high thermal conductance,
together with a small body size, especially when living in a constantly
warm environment, were interpreted as adaptations to reduce the
probability of overheating^ This interpretation has also been extended
by MacMlllen and Lee (1970) to burrowing mammals in general. However,
Gettinger (1975) and Vleck (1979) questioned McNab' s data and
interpretation. These comments have been answered by McNab in two
papers. The first one includes new data not only on fossorial
herbivorous rodents, but also on fossorial insectlvores , thus extending
the body mass (M^) and food habits range of the species examined
(McNab 1979). The second paper concerns the methods used to estimate
the minimal thermal conductance (McNab 1980) .
From this new set of data (McNab 1979), a more complex pattern
emerged. I^he basal rate of metabolism is lower than expected if M^,
is greater than 80 g, but it is higher if M], is lower than 60 g,
unless they inhabit an extremely constant and warm environment. This
pattern indicates that bloenergetlc adaptations to fossorlality include
(1) maintenance of a small temperature differential between body
temperature and the lower limit of thermoneutrality Independent of body
mass by matching the mass sensitivity of the basal rate to that of the
minimal thermal conductance; (2) reduced basal metabolic rate; (3)
standard to high thermal conductance; and (4) small body mass.^
In the present study the bloenergetlc characteristics of two
populations of the fossorial Spalacopus cyanus (Octodontidae) are
estimated to evaluate the significance of these parameters as
5
adaptations to fossorlality in different environments. One population
is from low altitude, ca. 70 m, close to the Pacific Ocean, the other
is from higher altitude, ca. 2500 m, in the Andean Mountains of central
Chile. Spalacopus cyanus is distributed from 30°S to 37°S along the
coast of Chile, and it is also found above 2000 m altitude in the Andes
between 33°S and 34°S (Osgood 1943, Mann 1978). The animals from the
mountains are larger than those from the coast but have the same
chromosomal characteristics (Feig et al. 1972).
Methods
Live animals were trapped during August with snare traps in
Con-Con, Valparaiso (32°56'S, 71°31'W; ca. 70 m) and from Farrellones,
Santiago (33°20'S, 70°11'W; ca. 2500 m). The animals were shipped by
air to Gainesville, Florida. They were kept in heterosexual pairs in
steel cages of about 60 x 80 cm filled with about 30 cm of humid dirt
where they could dig their burrows. Ambient temperature was between 20
and 23°C. The room, had windows and the photoperiod was not
controlled. They were fed mainly rabbit food, sweet potatoes, and
carrots a£ libitum.
Oxygen consumption measurements in eight individuals from low land
and nine from the mountains were made at different ambient
temperatureswith an open flow system, utilizing either a param.agnetic
Beckman G-2 or an Applied Electrochemistry oxygen analyzer. Carbon
dioxide and water vapor were absorbed from the gas stream after the
metabolic chamber and before the flow rate being measured. Ambient
temperature (T^) was controlled by submerging the ca. 3 liter
metabolic chamber in a thermoregulated water bath, and T^ was
6
measured vjith a mercury thermom.eter or a thermocouple located on the
interior top of the chamber. Room, air was pumped into the metabolic
chamber at a flow rate between 600 and 750 ml/min. Each run lasted at
least 2 h. All runs were m.ade during daytime between 0800 and 1800
hours. The animals were left without food between 2 and 12 h before
measurements, except for the 24 h continuous runs in which the animals
were provided with food within the chamber. Body temperature (Tj.)
and body mass (Mt) were measured at the beginning and end of each
run.
Oxygen consumption was calculated using the equation
Vq^(cts^ 02/g h) = 27.257 (APq^ Pb)/T
where APq is the fractional change in oxygen content, in the gas
stream between the entrance into and the exit from the metabolic
chamber, Fj. the flow rate (ml/mln), Pt the barometric pressure (mm
Hg), T the temperature of gas stream at the site of the flow rate
measurement (°K), and the body mass (g). The mean of the two
lowest periods lasting at least five minutes was considered to
represent the value for that run.
Mean basal rate of metabolism (V^o^) was estimated from.
measurements of minimal oxygen consumption within the zone of
thermoneutrality. The minimal thermal conductance was calculated from
the relationship Cjj, = Vq /(Tb “ Tg) for each measurement of
2
oxygen consumption below the limit of thermoneutrality. This method
solves the problem, of extrapolation to a higher Tb than actually is
measured, when the minimal thermal conductance is calculated by the
regression method (McNab 1980). The calculated thermal conductance
7
reflects the "wet" or total thermal conductance. The V^,q2 and
were compared to the expected values from the allometrlc equations of
Kleiber (1961) and McNah and Morrison (1963), respectively.
Burrow, ground surface, and air temperatures at both localities
were measured in summer and winter.
Statistical t-tests were performed to test for the differences
between the obtained values for and % from the expected
values based on body mass after angular transformation. Statistical
z-tests were used to test for differences in body size between
different sexes in each locality and within sexes in different
localities. Variation around means are expressed as + 1 standard error
(SE).
Results
The rate of oxygen consumption over a 24 h period shows the
absence of a circadian or photoperlodic effect in Individuals from both
populations (Fig. 2-1). Periods of rest are spaced by about 15 min to
1.5 h.
The bioenergetic characteristics of Spalacopus taken from the
coast and from the mountains are shown in Table 2-1. Anim.als from both
populations are good thermoregulators at Tg between 2 and 32°C. Body
temperature is not significantly different P > 0.05; Figs. 2-2, 2-3;
Table 2-1) between these populations. The V^,q2 is low in both
populations, but is significantly lower in individuals from the
mountains than in those from the coast (Table 2-1). The minimal
thermal conductance below 20°C is equally low in both populations
(Table 2-1, Figs. 2-4, 2-5).
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40
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19
Comparing the of animals trapped in the field (Table 2-2) we
can see, first, that there is significant sexual dimorphism in
individuals from the lowlands but not in those from high altitude; and,
second, that females and males from low altitude have a body size equal
to 71.3% and 83.9%, respectively, of the high altitude animals of the
same sex .
In Figures 2-6 and 2-7 the environmental temperatures measured at
both localities in winter are plotted. Average burrow temperatures in
winter are 4° and 11°C for the mountain and coastal populations,
respectively. Note that burrow temperature, as well as temperatures
measured at 10 cm deep in the ground, shows a greater dally fluctuation
at the coastal site. Average summer burrow temperatures are 15 and
26°C at the mountain and low altitude sites, respectively.
Discussion
Activity Pattern
The activity pattern of cyanus over 24 h lacks a circadian or
photoperiod effect (Fig. 2-1), as is characteristic of fossorlal forms
such as Geomys bursarius (Vaughan and Hansen 1961), Thomomys bottae
(Vleck 1979), jC. talpoides (Andresen and MacMahon 1981), Arvlcola
terrestris (Alroldi 1979), and Scalopus aquaticus (Arlton 1936). This
pattern is manifested in the activity observed in captive animals, as
well as in the field, except during the warmer hours of the summertime
when activity decreased, making trapping less successful.
Basal Metabolic Bate
Previous measurements on the bloenergetic characteristics of S.
cyanus have been done in two captive animals from the coastal region
20
Table 2-2. Body mass of Spalacopus cyanus from two altitudes.
Altitude (m)
Male
Female
2500
118.3 + 7.3
NS
112.5 + 7.7
0.04
0.01
70
99.3 + 2.2
0.001
80.2 + 3.2
Values represent m.ean + SE, (g).
T-test was used to test for differences.
Figure 2-6.
Environmental temperatures of the habitat of cyanus
at high altitude during winter.
TEMPERATURE
22
24
TIME OF DAY
h
25
Sample size was seven Individuals for each sex at each locality.
(McNab 1979). However, these animals had an extremely large never
found in nature, not even in the largest animals from high altitude.
Because of this, even though there are similarities in the values
(Table 2-1), the discussion will consider only the data from this
study.
The values of found in individuals of cyanus from both
populations are significantly lower than expected from the Kleiber
relation, and they are significantly lower in the individuals from high
altitude and cooler sites (Table 2-1). In general, these low values
are in accordance with those of other fossorial mammals. Looking at
this parameter alone, other things being equal, according to the
thermal stress hypothesis (McNab 1966, 1979), we should expect a lower
■»
^b02 altitude because burrow temperature is higher there.
However, other things are seldom, if ever, equal, especially in the
field. McNab (1979) proposed that fossorial mammals scale Vj^q to
2
body mass to a function different from the Kleiber relation (Vo2/Mt,
= 3.42 M^|“'25) with an exponent between -0.50 to -0.40,
intercepting the Kleiber relation at about 80 g. Thus, we should
expect a greater difference between the observed and expected values
from the Kleiber relation as body mass increases above 80 g, which is
the case for cyanus studied here.
Minimal Thermal Conductances
Minimal thermal conductance in fossorial mammals living in cool
burrows (< 20°C) are generally equal to the standard values (McNab
1979). The lower minimal thermal conductances of S. cyanus found in
26
this study probably can be related to a seasonal change similar to the
one described for Geomys plnetls (Ross 1980). If so, higher values
should be expected during the summer, especially at low altitude.
The correlation of thermal conductance with ambient temperature
(Figs. 2-4, 2-5) Is probably related to postural changes In the shape
of the animal. At low Tg the animals frequently adopted a more
spherical shape, reducing the surface to volume ratio. At high Tg
the animals usually adopted a position maximizing the exposed surface.
Blood circulation to the tall and feet, denoted by the color of the
skin, also Increased with Increasing Tg. The same behavior has been
observed In the genera Thomomys and Ctenomys (personal observation).
Evaporative cooling Is of no significance to heat dissipation In
Geomys, Spalax, Heterocephalus (McNab 1966), or Thomomys (Gettlnger
1975). Spalacopus was never seen to spread saliva on the fur.
Spreading of saliva on the entire body has been observed to occur and
to be of Importance In Tachyoryctes and Hellophoblous (McNab 1966).
There Is a question whether this avenue of heat loss Is Important In
nature, given the high relative humidity In burrows.
The Temperature Differential
The combination of , Cjj,, and determdnes the
temperature differential between T^ and Tg at the lower limit of
thermoneutrallty (T^) by the equation
ATi = 3.42 F Mb +0.25
(McNab 1974), where F Is equal to the ratio between the Vb02 and C
expressed as percentage of the expected values based on Mb.
Nevertheless, animals from these two populations have a similar ^T^
27
(10.0 and 10.7°C). However, these values are obtained by different
means. The individuals from high altitude have a small F value,
produced mainly by a low V^,q^ . Individuals of the population on the
coast have a small My, and an F ratio close to unity (Table 2-1).
Because a small ATj is related to high temperature tolerance (McNab
1979), individuals from the two populations should show a similar
tolerance to high Tg; this is actually the case (Figs. 2-2, 2-3).
According to the thermal stress hypothesis of McNab (1966, 1979),
we should expect the individuals from the lower and warmer place to
show a greater tolerance to high Tg. However, two factors should be
considered regarding this disagreement. First, the animals from low
altitude do not face a constant and warm, environment. Thus, if they
could reduce the F ratio or to a greater extent, they could become
poor thermoregulators at the low Tg found during winter. A second
factor may be that the lower V]j02°f individuals from high altitudes
and lower burrow temperature may be thought of as an adaptation to a
lower oxygen partial pressure given by the combination of fossorlal
habits and high altitude. Even though the lower V^,q^ of the high
altitude cyanus is possibly related to a lower oxygen tension, it
cannot explain the larger body size of those animals because the total
requirements for oxygen increase with body mass. If the level of the
rate of metabolism is actually an adaptation to low oxygen tension, we
should expect a positive correlation between this level and the
critical oxygen pressure, not only intraspeciflcally , but also
int er specif Ically .
28
Vleck (1979, 1981) interpreted the low metabolic rate and small
body size in fossorlal mammals in warmer environments as adaptations to
the high cost of obtaining food by burrowing, the cost being higher
when soil friability and food availability are low. Undoubtedly, the
cost of burrowing is high; however, fossorlal mammals do not get all
their food from underground. Thomomys bottae and Spalacopus cyanus
feed on the surface vegetation around the opening of their burrows.
Several points suggest that the thermal stress hypothesis (McNab
1966, 1979) Is more likely than the cost of burrowing hypothesis (Vleck
1979) to explain the observed characteristics in S^. cyanus. According
to the cost-of-burrowing model, we should expect a larger In more
friable soils than in hard soils. This is not the case for S. cyanus.
Individuals with smaller are found mainly In friable sandy soils
along the coast and, to a much lesser extent. In hard clay soils in the
ravines around the Central Valley (Contreras, personal data). Larger
Individuals are found only In the Andean Mountains above 2000 m
altitude and always in hard clay soils. An alternative explanation
would be a much larger plant productivity in the hard soils or a very
small plant productivity in the sandy soils. The high population
densities at both sites indicate that food availability is unlikely to
be low in either environment.
A similar pattern of body size differences and soil type was found
along an altitudinal transect of 758 m in the Beartooth Mountains,
Wyoming, for Thomomys talpoides (Tyron and Cunningham 1968). In this
case the larger M^ was claimed to relate to higher protein content in
the stomachs of the individuals. However, the relation was not a
29
strict one, food availability was essentially the same along the
transect, and the study did not consider seasonal fluctuation or food
storage .
The opposite trend was found for bottae (Davis 1938). In this
case Mb decreased with altitude and was claimed to relate to food
availability; however, sample sizes per locality were very small, and
there were no actual measurements of food availability.
Another indication making the thermal stress hypothesis more
likely IS that S. cyanus individuals show sexual dimorphism of Mb
only at low altitude, the warmer sites. During pregnancy and lactation
females would have an Increase in heat production due to an Increment
in Mb, as well as by hormonal stimulation (Kleiber 1961). This
Increase in heat production would more likely represent overheating
problems at low altitude because of higher burrow temperature, and
smaller females would thrive better than larger ones at low altitudes.
Clearly, a long term ecological study of S. cyanus living in
contrasting habitats is highly necessary to describe tbe actual
characteristics and relationships of the individuals to the environment
in which they live. A study of this type has been done in Thomomys
— (Andresen and MacMahon 1981). However, they considered only
different successlonal stages within a given local area, thus thermal
factors were more or less the same in the different stages. In that
case, the animals responded to differences in food availability by a
change in population density.
CHAPTER THREE
METABOLIC AND THERMAL RESPONSE OF FOSSORIAL MAMMALS
TO LOW TEMPERATURE AND OXYGEN PRESSURE
Introduction
Fossorlal manimals spend most of their life underground in
microenvironments characterized by darkness, high relative humidity,
small temperature fluctuations, and hypoxic and hypercapnic atmospheres
(Rosenmann 1959; Kennerly 1964; McNab 1966; Studier and Baca 1968;
Studier and Proctor 1971; Baudinette 1974; Ariell 1979; MacLean 1981).
Adapatations to these conditions are found in diverse taxa, e.g.,
marsupials, Insectlvores , edentates, and rodents.
Proposed adaptations include low basal rates of metabolism (Vt^q
2
and standard to high minimal thermal conductances (C^,) (McNab 1966;
1979; Goreckl and Chrlstov 1969; Bradley et al. 1974; Nevo and Shkolnik
1974; Bradley and Yousef 1975). The low rates of metabolism are
considered adaptations to the hypoxic and hypercapnic conditions of
their burrows (Baudinette 1972; Ariel! et al. 1977; Ariell and Ar
1981_b) in attenuating respiratory anoxia or acidosis. McNab (1966)
argued that this interpretation is unlikely because burrow oxygen
tensions (PO2) usually above values where rates of m.etabollsm are
affected and also because fossorlal mammals are insensitive to hypoxia
and hypercapnia. The only m.easured critical oxygen pressure (P^) for
30
31
a fossorlal mammal (Spalax ehrenbergl ) indicates that these animals
have lower P^, than non-f ossorlal mammals, and their rates of
metabolism did not differ from expected values based on body mass
(M^,) (Ariel! et al . 1977).
The aim of this study was to determine whether fossorial mam.mals
have a lower sensitivity to low Pg than surface dwellers; and if
2
they do, whether this characteristic is related to the level of the
rate of metabolism.
Methods
Animals . Three adult male eastern moles, Scalopus aquaticus
(Talpidae), were caught near Gainesville, Florida. They were kept in
glass aquaria with moist soil and were fed canned dog food, worms, and
crickets .
Five and six adult cururos Spalacopus cyanus (Octodontidae) from
70 and 2500 m. altitude, respectively, were used in my experiments.
Localities and conditions of captivity were indicated in Chapter Two.
One mole-m.ouse, Notiomys macronyx (Cricetidae ) , was collected at
700 m altitude, 18 km SE of Barlloche, Prov. Rio Negro, Argentina, by
O.P. Pearson. The animal was fed canned dog food, worms, apples,
mushrooms, grapes, oatmeal, and sweet potatoes ad libitum. It was kept
in a large aquarium with moist soil within which it established
tunnels .
Two common mole-rats Cryptomys hottentotus (Bathyergldae) were
trapped in Pietermaritzburg, South Africa by G. Hickman. They were
maintained in rat laboratory cages with sawdust. They were fed sweet
32
potatoes, carrots, and rabbit food pellets. They did not eat worms or
dog food even when available.
Experiments . Basal rate of metabolism and minimal thermal
conductance were estimated by measuring rates of oxygen consumption at
different ambient temperatures using techniques described in Chapter
2. Body temperatures and body masses were measured at beginning and
end of each run.
Subsequently, rates of metabolism and body temperatures were
measured at 12, 10, 8, and 6% oxygen at 30, 20, and 10°C. In these
cases oxygen-nitrogen mixtures, rather than atmospheric air, were
pumped through the metabolic chamber. These experiments lasted 1
hour. The measurements allowed estimates of the critical oxygen
tensions where or Tu fell below values found at normoxic
2
conditions (Rosenmann and Morrison 1974).
Results
Standard conditions
The parameters of energetics of the species studied as well as
those obtained from the literature are given in Table 3-1. Notiomys
macronyx maintains T], about 36.8°C at temperatures below 31oc.
At higher T^s, body temperature Increases slightly (Fig. 3-1). Basal
rate of metabolism in this species is 113.4% of the expected based on
body m.ass (Kleiber 1932, 1961) and has a thermal conductance as
expected for its size (McNab and Morrison 1963).
Cryptomys hottentotus maintains a relatively low body temperature
(35.70c) for a mammal while inactive at ambient temperatures up to
33-340C (Fig. 3-2). Body temperature does not increase exponentially
Table 3-1. Bioenergetlc parameters In some fossorial mammals.
33
Mean standard deviation, other values are mean _f standard error
Figure 3-1. Resting rate of oxygen consumption and body temperature of
Notiomys macronyx as a function of ambient temperature.
Thermal conductance is the average of each measurement
below 20°C. Basal rate is the average value of
measurements between 29 and 32.5®C.
1
RATE OF METABOLISM ccOg/g-h
35
LU
QC
D
>- f-
Q <
O cr
CQ LU
a.
LU
o
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AMBIENT TEMPERATURE °C
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37
•
1
I — I — I — I — I — I — \ —
(7) m ro
ro ro rO
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3dniVd3dkN31
AQOa
M-s/^ooo i^snoavi3N do 3ivd
AMBIENT TEMPERATURE
38
at temperatures above the thermoneutral zone as in most other mammals;
It remains constant at about 37.5°C, During activity, however, body
temperature greatly increases and the animals became hyperthermic (Fig.
3-2). A high rate of evaporative water loss coupled with a low basal
rate of heat production and high thermal conductance may be important
in the ability of £. hottentotus to maintain a low at high ambient
temperatures .
Response to low oxygen tensions
Critical oxygen pressures were determined by calculating linear
equations relating and V]302 to Pq2 below (Fig. 3-3, 3-4,
3-5, 3-6, 3-7, 3-8, 3-9, 3-10, 3-11, and 3-12). These equations are
* •
given in Table 2. Note that the equation = b(v_ ) Pqo +
2 ^2 ^
intercept could not be calculated for aquaticus or M. mac r onyx,
because neither species showed a reduction in the rate of metabolism
below normoxlc values at any combination of Pq2 ^nd Tg used (Fig.
3-4 and 3-6). Consequently, Pc02 could not be calculated by
extrapolating the equation to normoxlc Vq . Both species did show a
reduction in T^ when exposed to very low P02 and low Tg, thus
allowing the calculaton of ^cT^ (Fig. 3-3, 3-5; Table 3-2 and 3-3).
Critical oxygen pressure for body temperature generally is higher
than for resting oxygen consumption. Maximal rates of oxygen
consumption are, however, more sensitive to a low P02 Than T^;
these relationships are shown in Figures 3-3, 3-4, 3-5, and 3-6 for S.
aquaticus and macronyx.
Table 3-3 shows the P^. for body temperature and resting V02
for fossorial mammals. The values for aquaticus and M.
OT
C
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O
CM
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ro
Lo
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o
LU
GC
3
<
CC
LU
CL
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LU
H
U
CD
<
Figure 3-4. Resting rate of oxygen consumption (mean + SE) in
Scalopus aquaticus versus Pq at different Tg. Upper
curve is the highest rate of metabolism measured at
10°C.
42
D)
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44
AMBIENT TEMPERATURE
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33
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60
48
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AMBIENT TEMPERATURE
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52
Oo ^IV
AMBIENT TEMPERATURE
(U
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I
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RATE OF METABOLISM cc02/g h
54
mmHg
U2
cfl
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to
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60
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56
O
111
cc
3
H
<
GC
UJ
Q-
LU
I-
m
m
Oo
Figure 3-12. Resting rate of oxygen consumption (mean - SE) in Spalacopus cyanus from high
altitude versus Pq2 at different T^. Equations for lines below are given
in Table 3-2.
58
^•G/^ooo lAisnoaviBN do diva
o
mmmHg
59
Table 3-2. Linear regression equations of and Vq versus Pq
below values of normoxla in fossorial ma^als. ^
Species t
3
1.
2.
"b ■ »(T,1
’'°2 ■
X Pq^ - intercp.
X Pq^ - intercp.
n
r2
P <
Scalopus aauaticus 10
1.
0.2489
16.38
5
0.998
.01
20
1.
0.1085
11.25
8
0.920
.01
Notiomvs macronvx 10
1.
0.1960
12.75
6
0.937
.01
20
1.
0.0822
5.33
5
0.912
.01
Crvptomvs hottentotus 10
1.
0.1585
16.38
7
0.974
.01
2.
0.0321
0.21
4
0.992
.01
20
1.
0.1085
11.25
8
0.920
.01
2.
0.0272
0.56
6
0.910
.01
Soalacjoous cvanus 70 m 10
1.
0.2332
22.84
11
0.945
.01
2.
0.0377
1.06
11
0.800
.01
20
1.
0.1544
15.05
11
0.876
.01
2.
0.0271
0.91
7
0.766
.01
2500 m 10
1.
0.1728
16.37
15
0.922
.01
2.
0.3984
1.28
8
0.823
.01
20
1.
0. 0757
7.48
8
0.507
.05
2.
0.0230
0.62
8
0.895
.01
Soalax ehrenbsrqi^ 10
1.
0.2332
16.62
2.
0.0362
0.21
20
1.
0.0995
7.24
2.
0.0115
0.77
1. From Ariel! et al. 1977
60
Table 3-3, Critical oxygen pressures for resting rates of metabolism
and body temperature for fossorial mammals.
Species
Mb (g)
N
P
^CTb
^c02
Reference
ScaloDus aquaticus
45.5
3
10
68.8
65.9 ^
This study
20
67.2
Notiomvs macronvx
62.0
1
10
65.1
62.0 ^
This study
20
64.9
Cryotomvs hottentotus
71.4
2
10
103.3
104.1
This study
20
103.6
100.1
Spalaoopus cyanus
70 m
95.9
5
10
97.9
91.9
This study
20
97.5
89.1
2500 m
137.8
6
10
94.7
80.7
This study
20
94.5
79.4
Soalax ehrenberoi
186.0
13 ^
10
71.3
65.0
Arieli et al. 1977
20
72.8
82.0
^ Values calculated by
the equation ? -
co<>
= 1.
PoTb
- 7.2900
(n = 6, r = .854, ?
<.01) for - 10°c.
2
Total number of animals captured, actual number of animals used in the experiments
not given.
P/.TL = Critical oxygen pressure below which body temperature falls below normal
c ib
value, mm Hg
N = Number of animals used in the experiments.
= Ambient temperature, °C.
^c02 ~ Critical oxygen pressure below which metabolic rate falls below normal value,
mm Hg.
61
macronyx were estimated by using the equation
Pe02= 1*0561 PcT^- 7.29
(r^ = 0.729, p < .01, n = 6) at Tg = 10°C derived from the data
given in Table 3-3.
Discussion
The relation of rate of metabolism and body temperature to
in fossorial mammals is similar to that of other mammals (Segrem and
Hart 1967; Rosenmann and Morrison 1974, 1975; Ariel! et al. 1977).
4
Mammals can tolerate large reductions in P02 with no reduction in
their rates of oxygen consumption or body temperatures. The critical
oxygen pressure, below which there is a progressive reduction in Vq^
and T^j, is proportional to the rate of metabolism (Segrem and Hart
1967; Rosenmann and Morrison 1975, 1976; Ariel! et al. 1977).
Consequently P^ is generally higher at a lower Tg. Surprisingly,
Ariell et al. (1977) reported that Pc02 Spalax ehrenbergi is 17
mm Hg lower at 10°C than at 20°C (Table 3-3). It is difficult to
explain this observation.
I found that the critical oxygen pressure for T^ is higher than
for resting V02 in fossorial mammals (Table 3-3); a similar
conclusion can be derived from data given for Spalax ehrenbergi at
10°C (Ariell et al . 1977). The reduction in T^ indicates an
increment in thermal conductance, probably due to locomotor activity to
avoid hypoxic conditions. In the tundra vole (Microtus oeconomus),
body temperature decreases at a faster rate, if the animal is active
under hypoxic conditions (Rosenmann and Morrison 1974). Body
02
tem.perature is generally more sensitive than V,
to extreme
62
conditions. In mammals exposed to high Tg, body temperature
Increases above normal values before the rate of oxygen consumption.
Critical Pq for six highland and 15 lowland small mammal
species has been reported by Rosenmann and Morrison (1975). They
arbitrarily adjusted P^. values to 3.8 times standard rate of
metabolism (3.8 cm^02/g h). For comparison I adjusted
the data from this study to 3.8 times the basal rate of metabolism
(Table 3-4). Tbe comparison showed that fossorlal mammals had a Pg
significantly lower than that found in both lowland mammals (t = 5.10,
n = 21, P < .001) and highland mammals (t = 2.63, n = 10, P< .05).
Undoubtedly this greater tolerance to low Pq Is Important to
fossorlal mammals, especially when active in closed burrows at low
ambient temperatures and high altitudes.
The data on fossorlal mammals at 10°C (Table 3-3) show
independence of Pq with respect to body mass:
log Pc02 = -0.0392 log + 82.177
(r2 = 0.015, P > 0.5, n = 6). Despite a proposed correlation of the
ability to extract oxygen at low tensions with body mass (Hall 1966).
Similar results to this study were found for 21 species ranging from 8
to 481 g by Rosenmann and Morrison (1975); however, it is possible that
in their study the influence on body size on Pq has been obscured by
tbe standardization to 3.8 times basal rate of metabolism. Since
larger species require a lower ambient temperature to reach a 3.8 times
basal rate of metabolism than smaller species. Low rates of metabolism
in fossorlal mammals have been considered as an adaptation to low Pq^
(Baudinette 1972, Ariel! et al. 1977, Ariel! and Ar 1981b). Although
63
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e c
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64
there Is a correspondence between the rate of metabolism and Pc at
the intraspecific level, no correlation is found interspecif ically
among fossorial mammals between the rate of metabolism and Pc,
irrespective of whether rate of metabolism is expressed per unit body
mass :
P^O = -39.75 (Vto ) + 120.8 (r2 = .362, P >0.10, n = 6)
2 2
or on total body size:
P_0 = -0.1603 (Vbo Mfc) + 93.9 (r2 = .1737, P > 0.20, n = 6)
CU2 2
A larger number of species was considered from Rosenmann and
Morrison (1975) (Table 3-5) to determine whether the lack of
correlation was peculiar to fossorial mammals or due to small sample
sizes. These data also indicate that no correlation exists between
Pc and the rate of metabolism at the interspecific level when
expressed per unit body mass:
P„0 = -1.500 (3.8Vbo ) + 130.7 (r2 = 0.142, P>.20, n = 14)
2 2
or on total body size:
Pco^ = 0.0086 (3.8Vb02 ^b) + H8-2 (r2 = 0.079, P>.20, n = 14)
I conclude that fossorial mammals do show a greater tolerance to
low Po . however this greater tolerance is related neither to body
2
mass nor to the rate of metabolism at the interspecific level. The
critical Pn as measured here is the response of the whole individual
2
to low Po . Specific values are the result of a combination of
2
several physiological characteristics, such as small respiratory dead
space (Darden 1972), high blood oxygen-affinity (Hall 1965, 1966;
Bartels et al. 1969; Baudinette 1974; Ar et al. 1977; Quilllam et al.
1971; Lachner 1976), low heart rate (Ariell and Ar 1981^), short tissue
65
Table 3-5, Basal rate of metabolism (V^j02) » critical oxygen pressure
(Pj,) for metabolism for some of the species studied by
Rosenmann and Morrison (1975),
Species
''bOj
«b
Pc
Reference
Octodon dequs
0.811
181
139
12, personal data
Acomys cahlrinus
1,10
49
131
16
Spermophilus parryii
0.68
472
131 '
2, 4, 15
Glauconys volans
1.217
67
128
9, 10
Baiomys taylori
1.95
8
127
6
Microtus oeconorous
2.50
36
123
2
Meriones unguiculatus
1.412
48
123
3, 7, 11, 17
Dicrostonyx rubrlcatus
1.83
52
123
2, 15
Clethr ionomys rutilus
3.00
33
122
14
Cavia porcellus
0. 581
481
117
Personal data
Mus musculus (feral)
1.80
19
116
13
Mus musculus (white)
1.76
35
116
13
Peromyscus maniculatus
1,908
21
109
5, 8
Microtus pennsylyanicus
1.93
29
97
1
1, Bradley 1976; 2, Casey et al. 1979; 3, Contreras 1984a; 4, Erikson
1956; 5, Ha3ward 1965; 6, Hudson 1965; 7, Luebert et al. 1979; 8,
McNab and Morrison 1963; 9, Muul 1968; 10, Neumann 1967; 11, Robinson
1959; 12, Rosenmann 1977; 13, Rosenmann and Morrison 1974; 14,
Rosenmann et al. 1975; 15, Scholander et al, 1950; 16, Shkolnik and
Borut 1969; Weiner and Gorecki 1981.
Body mass (M|j) and P^, from Rosenmann and Morrison (1975) .
a Average from estimated values.
66
diffusion distance (Ariel! and Ar 1981^), and high myoglobin
concentration in skeletal muscles (Ar et al. 1977; Lachner 1976), each
of which permits these animals to tolerate hypoxic conditions.
Low Pj. values of fossorial mammals permit them to tolerate lower
Pq environments than surface dwelling mammals. Even though low
2
rates of metabolism are not important in setting P^., they may reduce
respiratory stress from low O2 and high CO2 tension because the
development of hypoxic and hypercapnic conditions in burrows is
directly proportional to rate of metabolism (Withers 1978^, MacLean
1981). The combination of low P^, and low V02 may have special
relevance to colonial species with large body mass that live in clay
humid soils at high altitude, since these conditions enhance hypoxia
and hypercapnia in burrow microenvironments (Withers 1978^; Wilson and
Kilgore 1978; Ariel! 1977; MacLean 1981).
CHAPTER FOUR
ENERGETICS OF FOSSORIAL MAMMALS AND ITS RELATION
TO BODY MASS AND DISTRIBUTION
Introduction
Mammals usually avoid environmental fluctuations in their
environment by adjusting their activity pattern and/or by living in
comparatively constant microenvironments. Fossorial mammals of many
taxa, e.g., marsupials, Insectivores , edentates and rodents,
spend most of their life in burrows. Their food. Invertebrates, roots
and tubers, is contained in the soil and they excavate tunnels to
obtain it. They are seldomly, if ever, seen above ground, except in
some species during breeding, dispersal, or flooding of their burrows.
Burrov/ microenvironments are characterized by darkness, high
relative humidity, small temperature fluctuations, and hypoxic and
hypercapnic atmospheres (Rosenmann 1939, Kennerly 1964, McNab 1966,
Studier and Baca 1968, Studler and Proctor 1971, Baudinette 1974,
Ariel! 1979, McLean 1981).
Several physiological as well as morphological (Dubost 1968)
characteristics of these animals have been proposed as adaptations to
this way of life. Other studies have analyzed the respiratory
adaptations to hypoxia and hypercapnia (Darden 1972, Hall 1965, Bartels
et al. 1969, Baudinette 1974, Ar et al. 1977, Qullliam et al. 1971,
Lechner 1976, Ariell and Ar 1981a, b) . Early studies on the energetics
67
68
of fossorial mammals indicated that they are characterized by a low
basal rate of metabolism and a standard to high thermal conductance
(McNab 1966, Gorecki and Christov 1969, Bradley et al. 1974, Bradley
and Yousef 1975, Nevo and Sholnik 1974).
Low basal rate of metabolism has been interpreted as an adaptation
to hypoxic and hypercapnic conditions of their burrows (Baudinette,
1972, Ariell et al. 1977, Ariel! and Ar 1981b). Fossorial mammals
Indeed have a lower critical oxygen pressure than surface-dwelling
mammals, however this critical oxygen pressure bears no relation to the
rate of metabolism at the interspecific level.
The interaction of low basal rate of metabolism, high minimal
thermal conductance and small body size has been interpreted as a to
reduce overheating (McNab 1966, MacMillen and Lee 1970, Ross, 1980)
when digging, especially in warm burrows. However, the low basal rate
of metabolism and low body temperature of the golden-mole Chrysochlorls
aslatica have been interpreted as a consequence of a primitive
physiology (Withers 1978). A final interpretation of the low basal
rate of metabolism and small body size of this animal relates them to
the high energy expenditure involved in food searching by digging
(Vleck 1979, 1981, Andersen 1982). Even though all these hypotheses
intend to explain low rates of metabolism and small body size, it has
been found lately that fossorial mammals at body mass less than 80 g
tend to have higher rates of metabolism than expected (McNab 1979).
Here I present and analyze new data on the energetics of fossorial
mammals, together with the data available in the literature, in
relation to body size, food habits, and distribution.
69
Methods
Animals. Three Scapanus latlmanus were caught In mole live traps
(Yates and Schmidly 1975) along a small stream on the Stanford
University campus, Santa Clara Co,, California in June, 1982.
Two ^naemys fuscus were trapped alive using leg traps Oneida
Victor No. 0, with the edges cushioned by Tygon tubing. They were
trapped 3 km east of Laguna Malleco, Parque Nacional Tolhuaca, IX
Region, Chile, in November, 1982. For description of the habitat see
Greer (1966).
Four £t_enomys sp. (Gallardo 1979) were caught in the same way as
A. fuscus in Longulm.ay and Llucura, Prov, Malleco, IX Region, Chile
(30 27'S, 71° 17'W and 38° 30'S, 71° lO'W) in November, 1982. For
description of the habitat refer to Greer (1966).
Six Ctenomys maulinus bruneus were caught in Cordillera de Las
Raices, Prov. Malleco IX Region, Chile (38° 26'S, 71° 27'W) at 1650 m
altitude in December, 1980, These animals were caught in open volcanic
sands as well as in Nothofagus~Araucaria forest.
Six Ct_enomys fulvus were trapped in the vicinities of San Pedro de
Atacama, II Region, Chile (22° 25'S, 68° 15’S) at 2436 m during
September 1982. Two other individuals tentatively assigned to Ctenomys
fulvus were collected in La Ola, III Region, Chile (26° 30'S, 69° 05'W)
by the side of a stream at 4,000 m during September, 1982, The climate
in this locality, as in San Pedro de Atacama, is a high altitude desert
(Castri and Hajek 1976).
Four individuals of Thomomys bottae melanotus were trapped near
Bishop, Owen's Valley, Inyo Co., California (37° 25'N, 118° 25'W) in
April, 1982.
70
Four T. bottae bottae were trapped on the Stanford University
Campus (37° 30'N, 122° 12’W) in May, 1982.
Two T. townsendli beckmani were collected in Valmy, Humbolt Co.,
Nevada (40° 50'W, 117° 15'W) during May- June, 1982.
All rodents were maintained in individual cages provided with
sawdust or moist dirt. The rodents were fed sweet potatoes, carrots,
green grass, and rabbit food pellets ad libitum. The moles were fed
earthworms and canned dog food. Ambient temperature was about 20° with
no control of the photoperiod.
Ambient temperatures were recorded in the field in most of the
cases .
Experiments . — Rates of oxygen consumption were measured at
different ambient temperatures. Oxygen consumption of the animals from
Chile was measured in a closed system. The animals were placed in a
stainless steel chamber with CO2 and water absorbents. The chamber
was submerged in a therm.oregulated water bath, connected to an
automatic manometric respirometer and this in turn to a recorder
(Morrison 1951). Each animal measurement lasted for at least 3 hours
and the lowest value of about 8 to 13 min was considered.
Measurements on Scapanus and Thomomys were made in an open system,
using an Applied Electrochemistry Oxygen Analyzer. Each run lasted at
least two hours, and the average of the lowest two values lasting at
least five min was considered. All values were corrected for STDP and
a respiratory quotient equal to 0.8 was assumed in the calculations.
Body m.ass and body temperature were recorded at the beginning and at
the end of each run.
71
In the case of Ctenomys maullnus and fulvus measurements were
also made with an open system as described in Chapter Two.
Minimal thermal conductance was calculated as the average of each
individual measurement of oxygen consumption, usually below 20° C
ambient temperature (McNab 1980) . When minimal thermal conductance
reported in the literature was calculated by linear regression and did
not extrapolate to body temperature at V02 equal to zero, it was
recalculated according to McNab (1980).
Results
A summary of the data on the energetics of the species studied
here, as well as that found in the literature, is presented in Table
4-1. A species by species interpretation is given in this section.
Scapanus latimanus Isa good thermoregulator, the average body
temperature (T^,) equals 37.1° C at ambient temperatures (T3)
between 6 and 30° C. At higher T^s body temperature Increased to
37.6 at 34° C Tg , when the animal was at rest. However, when the
animal was active, it became hyperthermic (Fig. 4-1). This species has
a basal rate of metabolism (V^jQ^) as expected from body mass (100.3%)
(Kleiber 1932, 1961). Minimal thermal conductance (C^,) was lower
than expected from body mass (87.4%) (McNab and Morrison 1963). These
values are similar to those reported for Scalopus aquaticus (McNab
1979). Neither of these two species clearly distinguishes between
physical and chemical thermoregulation, as is shown by the high Vq^
values near the lower limit of thermoneutrality (Fig 4-1).
Table 4-1. Parameters of energetics in fossorial mammals.
72
Hellophoblus argentoclnerus 88 O.85+O.0A3 8/ 76.0 0.139+0.0050 20/ 130.0 0.58 35.1 30.0 5.1 McNabl966
73
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74
Ctenomys peruanus 490 0.45 2/ 62.0 0.056 2/ 124.0 0.50 35.2 27.2 8.0 Morrison and
75
Number of measurements/ number of animals.
Minimal thermal conductance as a percentage of 1.00 (McNab and Morrison 1963)
Figure 4-1. Rate of metabolism and body temperature versus ambient
temperature in Scapanus latimanus . Different symbols
represent different animals (3) . The open circle at
33.2°C ambient temperature represent an active animal.
Mean V]^02 calculated between 30 and 34°C. Minimal
thermal conductance is indicated by the slope of the line
below thermoneutrality. The numerical value of slope is
indicated in the graph.
RATE OF METABOLISM ccOg/g h
77
LU
78
A temperature range of 19.5-26° C was found in the superficial
burrows of latimanus (ca. 4-6 cm deep) in which these animals were
captured. At the same time the temperature range was 12-29° C in the
air, 15-36° C at the ground surface, and 20.5-22.2° C at 25 cm deep in
the ground. The ground was very humid.
Aconaemys fuscus had an average = 37.3° C at air temperatures
between 6 and 32° C; T^, increased slightly with Tg (Fig. 4-2).
They have a and Cjj, close to expected (103.5 and 94.6%,
respectively). Frequent rainfall and snowfall are common in the range
of A. fuscus . The temperature range in the air was -3 to 18° C; at 20
cm deep in the ground it was 13.5 to 14° C.
Ctenomys sp. maintains an average T^, = 36.4° C up to 32° C (Fig.
4-3). This species presented a low Vt02 (78-72%) and low minimal
thermal conductance (81%). The temperature at 18 cm in the ground was
13° C.
Ctenomys maulinus bruneus maintains an average T], equal to 36.7°
C below 26° C ambient temperature (Fig. 4.4). Body temperature
Increased sharply at higher Tg. This species has the highest
of any Ctenomys (94.7%), and the lowest lower limit of
thermoneutrality. Ctenomys m. bruneus also shows the least tolerance
of high ambient temperature (Fig. 4.4). Minimal conductance is low
(82%). Tem.peratures of 10.7 and 14.5° C were recorded in burrows at 25
and 21 cm deep. The following temperature profile of the ground was
also found at 17:30 h on 11 December 1980: Air, 15.2° C; surface, 18°
C; 10 cm, 16 C; 20 cm, 14.5° C; 30 cm, 13; and at 50 and 70 cm deep.
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84
AMBIENT TEMPERATURE
85
11° C. Burrow cores were found on the surface of the ground after snow
had melted indicating snow-ground interface activity by these animals.
The ground at Cordillera de Las Raices is usually covered by snovj 6-7
months a year and upon occasion for as much as 10 months.
Ctenomys fulvus , in contrast to C^. maulinus , inhabits the
extremely arid Atacama Desert. This species maintains a slightly lower
T^ up to 25° C Tg; body temperature Increases at Tg higher than
30° C (Fig 4-5 and 4-6). Basal rate of metabolism is 77% of expected.
Minimal thermal conductance is also low. Ambient temperatures in the
C. fulvus habitat are shown in Table 4-2. Burrow temperatures ranged
between 9 and 16.5° C. During February they range between 19 and 25° C
(Rosenmann 1959) .
Thomomys bottae melanotus from Owens Valley, Cal. had an average
T^, equal to 37.3° C at air temperatures below 30° C (Fig. 4-7).
Basal rate of metabolism and Cj„ are slightly lower than expected
(93.6 and 93.3%, respectively).
Small bottae from Stanford University campus have a lower
and it is even lower in the larger individuals from the same
locality (96.3 and 72.4%, Table 4-1, Fig. 4-8). The opposite is true
for Cgj: it is lower in the smaller animals (88.4% and 94%, Table
4-1, Fig. 4-8). Vleck (1979) reported m.easurements on T. bottae from
southern California that are similar to the values reported here on T.
bottae with the same body size (Table 4-1). Burrow temperatures for
T^. bottae ranged between 22.8 and 25.5° C. At 20 cm deep, soil
temperature was 22.3-25.6° C. Surface temperature varied between 14.4
to 45.0° C.
0) <u
c
(TS -H
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87
AMBIENT TEMPERATURE
tn
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89
AMBIENT TEMPERATURE
90
Table 4-2. Ambient temperatures in Ctenomy fulvus habitat between
San Pedro de Atacama and Solor, II Region, Chile, 20
September, 1982.
Time
T° air
Surface
Burrow
30 cm
deep
10:25
8.9
16.1
13.5
11:30
11.2
16.0
13.5
12:15
21.0
50.6
11.6
16.1
14.0
13:00
23.9
51.0
16.2
14.5
13:48
12.9
14:19
25.0
48.7
16.2
15.5
15:46
24.3
13.8
16.5
16.7
16:57
30.0
13.4
16.3
17.5
17:26
21.0
22:00
11.1
6.1
16.2
17.5
£
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92
AMBIENT TEMPERATURE
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94
AMBIENT TEMPERATURE
95
T_. townsendil backmanii maintains an average T]^ equal to 37.5° C
at air temperatures below 30° C, above which Tj, sharply Increases.
Basal rate of metabolism is 88.5% and is 91.4% (Fig. 4-9).
Environmental temperatures taken on 26th June, 1982 at 09:30 h at
Valmy, Nevada were as follows: air, 23.6° C; surface, 39° C; at 5.5 cm
deep, 22.4° C; and at 9 cm, 19° C.
Discussion
The basal rate of metabolism. McNab (1979) found that his
previous conclusion (McNab 1966) that fossorial mammals have a low
basal rate of metabolism only holds for animals with a body mass
greater than 100 g. The difference between measured values and those
expected from the Kleiber relationship Increases as body mass
Increases. When fossorial mammals have a body mass smaller than 80 g,
basal rate of metabolism is higher than expected by the Kleiber
relation, unless they live in warm environments (Tg 25° C). McNab
(1979) proposed that these animals scale basal rate of metabolism in a
manner that is different from the Kleiber relation, the exponent
falling between -0.50 and -0.40. Linear regression of the data in
Table 1 (except glaber , C^. asiatica , and A. hottentotus , see later)
shows that this is actually the case:
logic Vbo2/Mbl=-0.493 logic Mb+0.981 n=45 r2=0.840 (4-1)
or
Vbo2/Mb=9.752 Mb"0.^93 (4_2)
This pattern is Independent of phylogeny. At small mass, both the
Insectlvore Blarina and the rodent Pitimys , or the mole Scalopus and
the cricetld mole mouse Notiomys , have similarly high basal rates of
t3 ^ T3
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AMBIENT TEMPERATURE
98
metabolism. On the other hand, both the South American caviomorphs
Scalacopus and Ctenomys, and the North American Thomomys have lower
basal rates of metabolism with increasing body mass (Fig. 4-10).
Exceptions to this pattern are found among fossorial mammals with
body mass lower than 80 g inhabiting warm burrows. The extreme case is
represented by the naked mole-rat Heterocephalus glaber (Fig. 4-10).
As will be shown, poor thermoregulation is produced by combining a
small body size and a low basal rate of metabolism in these animals.
McNab (1983) proposed mean and minimal boundary curves for
endothermy relating basal rate of metabolism and body mass (Fig.
4-10). These equations Vb02 /^b “ 21 . 53M^,“0. 67 g^d Vb02
/M^, = 15.56Mb“*^'^^, respectively, intercept the Kleiber relation
at 80 and 37.7 g. Thus, at a small body mass a mammal should have a
basal rate of metabolism higher than predicted by the Kleiber relation
to be a good thermoregulator. Mammalian species whose basal rate of
metabolism falls below this minimal boundary curve are poor
thermoregulators and may enter into daily torpor. Among fossorial
mammals this is the case for H. glaber , C^, asiatica and A. hottentotus
(Fig. 4-10).
Even though burrow temperatures show much less daily fluctuation
than above ground ambient temperatures, some fossorial species
experience considerable fluctuations throughout the year (Ross 1980).
It has been widely noticed that fossorial mammals become less active
during the warmer seasons (Wilks 1963, Genelly 1965, 1980, Ariel! 1979,
Nevo et al. 1982, Contreras 1984a). In addition to this behavioral
change, fossorial mammals also show a physiological adaptation to high
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100 500 1000
BODY MASS g
101
Tg by reducing the rate of metabolism. Geomys pinetis in northern
central Florida has a basal rate of metabolism equal to about 97% of
expected from mass during winter, decreasing to about 71% during the
summer (Ross 1980).
The minimal thermal conductance . Fossorial mammals that live in
burrows with temperatures below 20° C have a minimal thermal
conductance close to the expected value based on body mass. However,
it is high when they live in warm environments (Tg > 25° C). This is
the case for Heterocephalus glaber (Burrow T° = 30-31° C) (McNab 1966,
Jarvis 1978), Hellophobius argentocinerus (T° = 26° C) (McNab 1966),
and Geomys pinetis (T° = 27° C) (Ross 1980) (Fig. 4-11).
Minimal thermal conductance, as with the basal rate of metabolism
may be adjusted with season, especially in those species with large
yearly fluctuations in burrow temperature and especially in species
that face high summer burrow temperatures. In Geomys pinetis minimal
thermal conductance increases from 127% in winter to 159% in the summer
(Ross 1980).
The temperature differential and the effectiveness of
thermoregulation. — Fossorial mammals, when at rest, usually can
maintain normal body temperature at ambient temperatures up to about
30° C. However, when active these animals store heat, even at ambient
temperatures as low as 5° C (Ross 1980), and body temperature may reach
lethal levels as ambient temperatures higher than 28° G (Fig. 4-1, 4-4,
and 4-6). The thermoregulatory ability of a mammal at any ambient
temperature will depend upon the balance established between the rate
of heat production and rate of heat loss. Basal rate of metabolism and
w
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103
n
O
O
100 500 100 0
BODY MASS (g)
104
minimal thermal conductance are both functions of body mass and in
conjunction they will determine the temperature differential between
body temperature and the temperature at the lower limit of the
thermoneutral zone (McNab 1974), assuming that a species conforms to
both scaling functions:
Vbo 3.42 Mfe-0.25
ATi = £ =
All =3.42 Mb+0-25
If a mammal shows deviations from the expected values in the
observed basal rate of metabolism or in minimal thermal conductance,
the observed AT]^ will also deviate from values expected according
to equation 4-3. To account for these deviations a factor can be
Incorporated in equation 4-3, such that is equal to the fractional
expression of the percentage observed values of the basal rate of
metabolism and minimal thermal conductance (F = %V^jQ2
AT^ = 3.42 F
In fossorial mammals the combination of low rates of metabolism,
high thermal conductances and/or small body masses, should lead to
small AT]^. The significance of AT^ for fossorial mammals rests on
its relationship to the temperature differential that a mammal
maintains between body temperature at high ambient tem.peratures (McNab
1979). Thus, animals with small ATj^ are able to tolerate higher
ambient temperatures because they maintain a lower Tg at high ambient
temperatures .
As was previously shown, fossorial mammals scale the basal rate of
metabolism according to equation 4-2, rather than to the Kleiber
relation. In this case:
105
9.752
All =
1.00
ATj^ = 9.752
From equation 4-5 it can be seen that in fossorial mammals ATi is
essentially independent of body mass (Fig. 4-12).
'The temperature differential at the lower limit of
thermoneutrality (AXi) is directly related to the effectiveness of
thermoregulation, and even though a small AT^ permits a mammal to
tolerate high ambient temperatures in burrows, it leads to poor
thermoregulation at low ambient temperatures. Because fossorial
mammals scale basal rate of metabolism according to equation 4-2, and
AXi is Independent of body mass (equation 4-5), AXi does not
decrease at small body mass, and generally does not fall below the
values predicted from the minimal boundary curve. As a consequence
small fossorial mammals are good thermoregulators and able
cold environments. Species that do not fit this pattern have a small
Axi, are poor thermoregulators and are restricted to warm
environments. Among fossorial mammals this is the case for
Heterocephalus glaber (McNab 1966, Jarvis 1978), Chysochlor^ aslatlca
(Withers 1978), Heliophoblus argentoclnerus (McNab 1966) and Geomys
bursflrius (Bradlsy and Yousef 1975).
In this context, the low basal rate of metabolism and poor
thermoregulation of the golden mole Chysochloris aslatjxa may be an
adjustment to burrowing in warm environments and not as a consequence
of a primitive physiology (Withers 1978). Note that the naked mole rat
also has a poor capacity for temperature regulation, and it is related
to warm burrows, and not to phylogeny. If this interpretation is
0)
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107
q
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in
fvi
£i
2
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CVJ
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m
m
100 500 1000
BODY MASS g
108
correct we should expect even poorer thermoregulation in the Grant's
desert golden mole Eremltalpa grant! , because it is smaller and
probably inhabits warmer burrows than C^. aslatica (Walker et al.
1964). However, better thermoregulatory capacity should be expected in
the large golden mole Chrysospalax, unless they have an extremely low
basal rate of metabolism (< 50% at 200 g), which is unlikely because
they live in forested areas (Walker et al. 1964), presumably with
cooler burrow temperatures.
I^The temperature differential is also adjusted in animals with
large body mas^ however in this case AT]^ values tend to be lower
than predicted by the curve reducing heat storage (Fig.
4-12), i.e. there is an adjustment at both small and large body masses.
Other alternatives have been proposed to explain changes in body
size and for low rates of metabolism in fossorial mammals. The large
body size in Thomomys talpoides on a 758 m altitudinal transect in the
Beartooth Mountains, Wyoming, was claimed to relate to higher protein
content in the stomachs of the individuals (Tyron and Cunningham
1968). However, the relation was not a strict one, food availability
was the same along the transect, and no seasonal fluctuations were
considered. In that case body mass was larger in shallower soils in
contraposition to the claim that small body size is related to shallow
soils (Davis 1938, Kennerly 1959).
^Food limitation has been Indicated to explain not only small body
size and low rate of metabolism but also colonialit^in Heterocephalus
glaber (Jarvis 1978). ^hese characteristics have also been considered
adaptations to optimize energy gain given the high cost of burrowing^
109
(Vleck 1979, 1981, Andersen 1982). In general, available data are in
agreement both with the thermal-stress hypothesis and the
cost-of-burrowing hypothesis, because plant primary productivity
usually decreases as ambient temperature increases. Vleck (1979),
although realizing that the hypotheses are not mutually exclusive,
thinks that small body size and low rates of metabolism may be favored
in less productive habitats by the economics of foraging rather than by
the thermal-stress hypothesis. He claims (Vleck 1979, 1981) in
opposition to the thermal-stress hypothesis that body size in Geomys
bursarius , compared to £. personatus (Kennerly 1959), and in Thomomys
quadratus , compared to T^. bottae (Davis 1938), is correlated to habitat
productivity rather than to soil temperature. However, £. personatus
is actually larger than £. bursarius and lives in more xeric
environments (Kennerly 1959) with presumably lower food availability.
In the case of T. quadratus and T. bottae, differences in body size
were claimed to relate to food availability (Davis 1938); however, the
number of Individuals caught per locality was few, there were no
measurements of food availability, and the altitude difference was
small (Davis 1938).
Even though, as Vleck (1982) points out, the largest members of
the family Geomyidae are found at low latitudes in Central America,
this observation does not necessarily contradict the thermal-stress
hypothesis. To evaluate this apparent contradiction, it is necessary
to know the energetic characteristics of these animals and the actual
burrow temperatures that they face. Among these Central American
gophers the largest individuals are found in at higher altitudes with
110
lower ambient temperatures, like the Mexican high Central Plateau.
Body size decreases at lower altitudes where the ambient is humid and
warmer. Moreover, thermal conductance is expected to be very high at
lower altitudes and warmer environments, because they have sparce and
coarse pelage on the dorsum and are almost naked on the ventral side
(Mendez 1970, and personal observation of the specimens from Guatemala
at the Florida State Museum). If Vleck is correct that these gophers
face high burrow temperatures and high plant productivity, this
combination would be an exception to his general suggestion that high
plant primary productivity occurs at lower temperatures.
Many organisms in nature respond to a given problem with different
solutions in different environments. When explaining interspecific
differences we principally rely on correlations and associations. In
this case, it is very likely that not only the thermal stress (McNab
1979), the cost of burrowing (Vleck 1981), or the hypoxia and
hypercapnia (Contreras 1984b), but also the historical factors (Smith
and Patton 1980) must be considered for us to have a global
understanding of the observed patterns in fossorial mammals.
CHAPTER FIVE
CONCLUSIONS
In Spalacopus cyanus the basal rate of metabolism is lower than
expected both in individuals from warm burrows at low altitude
(85%) and from cool burrows at high altitude (79%). However,
basal rates are lower in the larger animals from high altitude.
Minimal thermal conductance is 80% of the value expected from mass
at high altitude and 85% of expectations at low altitude.
The combination of the basal rate of metabolism, minimal thermal
conductance, and body size in Spalacopus determine a similar
temperature differential between body temperature and the lower
limit of thermoneutrality (10.0 and 10.7°C). Similar temperature
differentials, and consequently similar tolerances to high ambient
temperature, are attained by a low metabolic rate at high
altitudes, and by a smaller body size at lower altitudes.
Fossorial mammals have a lower critical oxygen pressure than
surface dwelling mammals.
Interspecifically the setting of the critical oxygen pressure is
not related to rate of metabolism or to body size in either
fossorial or surface dwelling mammals at masses between 8 and
481 g.
Ill
112
6. - Low rates of metabolism and small body size, although not setting
the critical oxygen pressure, may reduce respiratory stress by
hypoxia or hypercapnia.
7. - Basal rate of metabolism in fossorial mammals scales to body mass
according to the function V^q /^b ” 9.752 0.493^ This
equation intercepts the Kleiber relation at 74.5 g; thus, at
larger sizes the basal rate is lower than expected by the Kleiber
relation and is higher at smaller body masses.
8. - Minimal thermal conductance is high in those animals living in
warm environments ( 25°C).
9. - The combination of the basal rate of metabolism, minimal thermal
conductance, and body mass determine the temperature differential
maintained by an endotherm with the environment; this differential
is independent of body mass in fossorial mammals.
10. - Fossorial mammals that fall below the temperature differential
curve derived from the minimal boundary curve (McNab 1983) are
poor endotherms and are restricted to warm environments.
11. - This energetic pattern of fossorial mammals is interpreted as a
result of adaptations to reduce overheating and to maintain
endothermy at small masses when living in cool environments.
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BIOGRAPHICAL SKETCH
Luis Carlos Contreras Casanova was born In Santiago, Chile, on 23
October 1953. He completed secondary education at Liceo de Aplicacaion
No. 3 de Hompres, Santiago, in 1970. He spent the first half of 1970
in Michigan, U.S.A., as a Youth for Understanding exchange student.
In June 1977 he obtained the degree of Licenciatura en Biologia,
at the Facultad de Ciencias, Universidad de Chile. His thesis was on
the "Annual Reproductive Cycle in the Male Octodon degus Molina."
Since November 1977 he has been working at the Universidad de
Chile. In September 1979 he commenced graduate studies at the
University of Florida. After completion of his Ph.D. degree he will
continue work at the Departmento de Ciencias Ecologicas, Facultad de
Ciencias Basicas y Farmaceuticas , Universidad de Chile.
120
I certify that I have read this study and that in my opinion it
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adequate, in scope and quality, as a dissertation for the degree of
Doctor of philosophy.
B.K. McNab, Chairman
Professor of Zoology
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conforms to acceptable standards of scholarly presentation and is fully
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Associate Professor of
Zoology
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conforms to acceptable standards of scholffsly PResentati\on /fSW is fully
adequate, in scope and quality, as a dis
Doctor of philosophy.
C.A. Woods
Professor of Zoology
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It Professor of
Dairy Sci'ence
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and conservation
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adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
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Professor of Zoology
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conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Associate Professor of
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conforms to acceptable standards of schol^ly presentation anji, is fully
adequate, in scope and quality, as a dis/e
Doctor of Philosophy. I
C.A. Woods /
Professor of Zoology
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conforms to acceptable standards of
adequate, in scope and quality, as a
Doctor of Philosophy.
study and that in my opinion it
scholarly presentation and is fully
dissertation for the degree of
I certify that I have read this study and that in my opinion it
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adequate, in scope and quality, as a dissertation for the degree of
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