Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Bioenergetics of cross‐ice movements by Microtus pennsylvanicus, Peromyscus leucopus and Blarina brevicauda

Bioenergetics of cross‐ice movements by Microtus pennsylvanicus, Peromyscus leucopus and Blarina... Lomolino. M, V. 1989. Bioenergetics of cross-ice movements by Microtus pennsylvanicus. Peromyscus leucopus and Blarina hrevicauda. Holarct, Ecol. 12: 213-218. Laboratory and field experiments were conducted to investigate bioenergetics of winter dispersal and to compare winter (cross-ice) dispersal abilities of three small mammals: Microtus pennsylvanicus. Peromyscus leucopus and Blarina brevicauda. Total metabolic rates increased with running activity and decreased as ambient temperatures increased for all species. Thermal conductance was significantly higher for running than for resting Microtus and Peromyscus, but decreased significantly with activity for Blarina. Winter dispersal abilities, calculated from treadmill experiments, increased with ambient temperature and with body size of the species. The superior dispersal ability of Microlus in comparison with Peromyscus results from the former's ability to utilize more energy reserves during running. The comparatively low winter dispersal ability of Blarina, which was less than a third of the two rodent species, resulted from its high weight specific cost of transport at winter temperatures and its relatively low energy stores and/or energy utilization during running, M. V. Lomolino, Dept of Ecology and Evolutionary Biology, Univ. of Arizona, Tucson, AZ 85721. USA. Introduction Studies of the tnatnmalian fautia iti the Thousand Island Regioti of the St, Lawrence River. New York. USA. indicated that cross-ice movements during winter play an important role in determining insular community structure of terrestrial mammals (Lomolino 1983. 1984 and 1988). Seasonally inactive speeies. which have little opportunity to utilize the winter's ice eover, are disproportionately infrequent members of insular commutiities. The paucity of winter inactive species has been reported for other insular communities in temperate regions and appears to be a general phenomenon where ice cover provides a seasonally available mode of immigration {Jackson 1919. Hatt et al, 1948. Pruitt l^.^l. Beer et al. 1954. Banfield I9M, Cameron 1958. Denman 1965), Despite the potential importance of winter immigration abilities in determining insular community structure, there is little information available on absolute or even relative, cross-ice dispersal abilities (distances) of Accepted 10 November 1988 v(j) HOLARCTIC ECOLOGY HOLARCTIC ECOLOGY 12:3 (1989) terrestrial mammals. Existing models on bioenergetics of locomotion in mammals, however, enable a first approximation of cross-iee immigration abilities (Taylor et al, 1970. Wunder 1975, see also Linstedt and Boyce 1985, Aitehison 1987a. 1987b, Calder 1987). Maximum distance a mammal can travel across ice (void of food) may be calculated as energy stores divided by energy used per km traveled. The total rate of energy use during dispersal is equal to the sum of rates of energy use for basal metabolism (Eh), thermoregulation {E|), and locomotion (E,), Each of these rates and, therefore, the total rate of energy expenditure during dispersal is a less-than-linear function of body mass (Eh a M"". E, a M"^" and E, a M""; see Wunder 1975 and references therein). In contrast, energy stores in mammals are at least a linear function of body mass (Morrison 196{), Linstedt and Calder 1981, Linstedt and Boyee 1985), Therefore, maximum winter cross-ice dispersal distances of mammals should increase with body mass. In addition, because thermoregulatory expenditures decrease as ambient temperatures increase, winter 80 -- 0123- KEY RMR AMR, 1,4 km/hr AMR, 2,0 km/hr AMR, 2.6 km/hr 60 -- UJ Fig. I, Resting and active metabolic rates (RMR and AMR) of Microlus pennsylvanicus as a function of ambient temperature and running velocity (see Tab, 1), Metabolic rates are expressed as ml O; g""^ h ' so that the slope of the line relating metabolic rate lo temperature is equal to thermal conductance (in mi O^-oih-'X-'isee methods). I< Q: 40-- _i o m < tiJ 20-- -10 0 AMBIENT +10 TEMPERATURE (C) dispersal abilities should increase with ambient temperatures. Here I test the above predictions and compare dispersal abilities of three species of small mammals at winter temperatures. seeds, peanut butter and laboratory mouse chow, whereas Blarina was fed freshly-killed lab mice iMus musculus) in addition to the above foods. All cages were kept in an environmental chamber under a natural photoperiod at \5''C. Metabolism studies were conducted using a 4-1 plexiglass chamber equipped with a treadmill. Metabolic rates were measured using an open-flow system (flow rate = 6.6 I min"') with an ADC (Model 225) infra-red Materials and methods gas analyzer to monitor CO, evolution. Oxygen conBoth laboratory and field experiments were used to sumption was calculated assuming a respiratory quoinvestigate and compare winter dispersal abilities of tient (RQ) of 0,80 (see Buckner 1964, Randolph 1980a three species of small mammals: Microtus pennsylvan- and 198(lb), icus, Peromyscus leucopus, and Blarina brevicada. Food was removed from cages 3 h prior to the start of the metabolism experiments with Microlus and Peromyscus, and 1 h prior to the start of experiments with Blarina. Metabolism runs for each species were conLaboratory experimenls ducted during each species" major activity period (i.e. The mammals used in this study were captured in New IIKM) to 16(K) h EST (Eastern Standard Time) for MicroYork State, USA. during March and April 1982, Micro- tus and Blarina and 19(K) to 23()() h for Peromyscus). Prior to each run, individuals were weighed to the lus and Peromyscus were trapped along the St. Lawrence River in Jefferson County, and Blarina was cap- nearest 0.1 g. then placed in the metabolism chamber tured in Broome County where metabolism studies for a 5 min adjustment period. Metabolic rates of Microtus were measured for resting and active individuals were conducted. All individuals were kept in scperate cages with wood (velocity = 0 to 3 km h"') at ambient temperatures shavings and soil, and food and water were supplied ad between —15 and +25°C, with the metabolism chamber libitum. Microlus and Peromvscus were fed sunflower placed in a top-loading freezer (ambient temperature < HOLARCnC ECOLOGY 12:1 Tab. I. Effects of running activity and subfreezing temperatures on thermal conductance (TCinml O^g'^^h"' "C ')for Microtm pennsylvanieus, Peromyscus leucopus and Blarina brevicauda. Values presented are means with standard deviations in parentheSpeeies Velocity (kmh"') -14 to +2(fC N TC N 0 to +25 TC N -14 to +6°C TC Microius - at rest - running all speeds L4 2.0 2.6 0.0 2.3 0.0 ].3 0.% 1.22 1.24 1.27 1.16 (0.167) (0.104)(0.178) (0.162) (0.178) _ - (0.166) (0.170) (0.253) (0.387) (0.276) 1.71 1.79 1.97 1.76 1,76 (0.189) (0.194) (0.377) (0.367) (0.325) Peromyscus liUirina 1.00 (0.160) 1.97 (0.295) 1.23 (0.148) 0.93 (0.107) " Conductances over the two temperature ranges. 0 to 25°C and -14 to +6X differed for all velocities (p <^ 0,01; t-test). " This value for resting metabolic rate in M. pennsylvanieus did not differ (t = 0.41, P > 0.50) from that reported by Bradley (1976) for this species in central New York State, USA (conductance = 0.98 (0.045), N - 53). ' Vertical bars indicate those values that did not differ from each other (P > 0.05); otherwise P < 0.01. Values for thermal conductance of Peromyscus and Blarina at rest were taken from Deavers (1976). -5°C) or walk-in environmental chamber. Almost all metabolism rates of Peromyscus and Blarina, which were recorded during maximum dispersal distance experiments, were measured for active individuals (velocity ^ 2 to 3 ktn h"') at ambient temperatures between 0 and I5°C. Maximum distances these species can travel across ice were estimated by running animals at relatively warm winter temperatures (~5°C) to minimize thermoregulatory costs (ice-melt above this temperature would preclude cross-ice movements). Running speeds were maintained at those which seemed optimal for each individual. Runs were terminated when individuals were apparently exhausted and were unable to run again after a 5 min rest period. Individuals were then removed from the chamber and weighed, and total distance traveled was recorded. Total oxygen consumption (total CO, evolution for RQ of O.SII) was recorded to estimate the cost of transport and the total amount of energy reserves used for running a given distance (see Lomolino 1983 for additional details of laboratory methods). invariably void of food, and the characteristics of its snow-cover prevented tunneling. Winds at the ice surface were consistently less than 5 kg h"'. Total distance traveled by these mammals was measured using a modified activity wheel attached to a 1 m handle (see Lomolino 1983, p. 151). and velocity was calculated from the time it took to travel a measured distance. Experiments were terminated when the individuals could no longer re-initiate running after repeated prodding. Results and discussion Effects of temperature and velocity on conductance and metabolism Because total thermal conductance in mammals increases in proportion to M"'^ (Herreid and Kessel 1967, Bradley and Deavers 1980). I expressed conductance in units of ml O, g ' " h ' " C ' . This corrected for differences in body mass and allowed calculation of thermal conductance as the negative slope of the line relating metabolic rate (in ml O, Og" ^ h ') to ambient temperature. As predicted, metabolic rate increased with velocity and decreased as ambient temperature increased (Figs 1-3). Thermal conductance of Microtus at rest (ambient temperature = - 1 4 to +2i)°C) did not differ significantly from that reported by Bradley (1976) for this speeies in central New York State. USA (Tab. 1). In addition, the regression line for resting metabolie rate (RMR) of Microius intercepts the abscissa at 39.7''C. which is not different (P > 0.20) from the mean body temperature Field experiments In addtition to laboratory studies. I also investigated dispersal abilities of Peromyscus and Blarina under more realistic conditions by releasing them onto the ice of the St. Lawrence River during February 1979. These studies were conducted at relatively cold temperatures (^ -L*i°C) to avoid ice-melt and unsafe conditions which exist during warmer periods. As in the laboratory experiments, individuals were released during their major activity period. The ice was 1!O[,AR(T1C ECOLOGY \1 AMBIENT TEMPERATURE iC) Fig. 2. Active metabolic rates of Peromyscus leucopus as a function of ambient temperature (mean velocity = 2.3 km h ' ' , CT - thermal conductance in ml O^ g""'^ h"' °C"'). reported for Microtus by Bradley (1976; T^ (SD) = 38.5 (1.04), N - 109, t - 1.15). Running resulted in a significant increase in thermal conductance for both Microtus and Peromyscus (Tab. 1). That is, these species lost heat much more rapidly while running, and the heat produced by running did not compensate for the Increased conductance. In contrast, thermal conductance for Blarina while running was significantly tower than that reported for resting Blarina by Deavers (1976; see also Platt 1974). Because running had a significant effect on thermal conductance, overall effects of velocity and temperature on metabolic rate may be best expressed by including an interaction term (V*AT) in any model that is used to predict metabolic rate (regression model is MR (in ml 0 ; g-' h-') = k,(M-"^) (delta T) + k2(M-'''') (V) + kj(V) (delta T); M = mass, V = velocity in km h"' and delta T - lower critical temperature minus ambient temperature). Multiple regression analysis of metabolic rate for Microtus revealed that the interaction between ambient temperature and velocity was significant (P = .02; N - 58, r^ of the entire model = 0.81, F = 75.45 and P < O.(X)Ol). Thermal conductance was also affected by the range of temperatures over which experiments were conducted. For Microtus, thermal conductance was much higher for experiments run at subfreezing temperatures (P < 0.01; Tab. 1 and Fig. 1). For Peromyscus thermal conductance remained fairly constant (Fig. 2). Estimated thermal conductance for active Blarina (Fig. 3) was highest for individuals run between 0 and iCC, but decreased for individuals run at subfreezing temperatures (ambient temperature 0°C). Either the increased heat of activity contributed to thermoregulation or these shrews exhausted their aerobic capacities. Indeed, active metabolic rates of Blarina at subfreezing temperatures were over seven times the minimal metabolic rate reported for Blarina (Martinsen 1969). In summary, thermal conductance of the three species was not constant, but varied with running activity 216 and ambient temperature. In contrast, other studies on metabolism of small mammals during activity and thermal stress report relatively constant thermal conductances (e.g. see Hart 1950, 1952, Hart and Heroux 1955, Packard 1968, Bradley 1976, Deavers and Hudson 1977; but see also Wunder 1970). Apparently, in these species increased heat production of activity compensated for increases in rate of heat loss due to changes in posture and perfusion. Jansky (1959), however, reported that the thermal conductance of Clethrionomys glareolus decreased with activity, which is opposite to what I found for M. pennsylvanicus and P. leucopus in this study. Jansky suggested that some of the heat produced by exercise was used in thermoregulation, and thus metabolic rates increased less rapidly with decreasing temperatures for active vs resting individuals. Similarly, Platt (1974) reported that the heat produced by activity in B. brevicauda was used for thermoregulation, i.e. thermal conductance was lower for active vs resting shrews as reported in this study. Therefore, although many species exhibit a relatively constant thermal conductance, this is certainly not the rule for mammals. The observed increase in thermal conductance for Microtus at subfreezing temperatures may have resulted from increased blood flow to the extremities which would prevent freezing, but concomitantly, raise conductance. Because perfusion rates were not measured during these experiments, the above explanation remains tentative. Obviously, more focused studies on the factors affecting thermal conductance is warranted. Winter dispersal abilities Estimates of maximum winter dispersal distances from both laboratory and field experiments are presented in Tab. 2. Although the limited sample sizes do not justify AMBIENT TEMPERATURE (C) Fig. 3. Active and resting metabolic rates (closed and open circles, respectively) of Blarina brevicauda as a function of ambient temperature (mean velocity = 1.3 km h ', CT = thermal conductance of active individuals in ml O-. g ""'' h"' =c') HOLARCTIC ECOLOGY 12: Tab. 2. Distance traveled by Microtus pennsylvanicus, Peromyscus leucopus and Blarina hrevicauda ;it witilcr temperatures in the laboratory (LAB) or on the ice of the St. Lawrence River (FIELD). Values presented are species means with standard deviations included in parentheses unless otherwise indicated. Parameter Microfus LAB N 4 Peromyscus FIELD LAB 4 23.0 (4.1) -24.8 (8.0) 3.31(1.94) 0.24(0.15) Blarina FIELD 1 15.0 -14.8 0.83 0.07 20.9 2.86 LAB 6 Mass (g) Temperature (C) Velocity (km h"') Distance (km) Total 0^ consumption (L) Estimated fat use g (% of mass)* Cost of transport - in TNZ*' (77)59) 29.6 (8.0) • 7.3 (0.78) 2.02(0.07) 5.82(1.72) 0.98(0.19) 0.49(1.7%) 5.76(1.24) 2.18 4 27.4 (2.4) 7,1 (1.4) 2.36(0.21) 4.(K)(3.1.1) 0.47(0.28) 4.49(1.05) 2.25 22.0 (1.5) 4,6 (1.1) 1.15(0.18) 1.26(L22) 0.41(0.064) 0.14(0.6%) 9.84 2.46 1'his includes distance traveled by an individual during an aborted run: without this value, mean distance traveled by Microtus = Liters of O. consumed while running only. Fat utilization was calculated assuming conversion factor of 2 liter Oi per g fat used (see Schmidt-Nielsen 1975, p. 2U). •Cost nf Transport (COT in ml O, g"' km"') in thermal neutral zone (TNZ) was calculated using the formula COT = 8.46(M"''); see Taylor et al. (1970). speculation on intraspecific patterns, these data are sufficient to provide a first estimate of cross-ice dispersal abilities and comparisons among species. As predicted, winter dispersal distances increased with body size of the species. The mean maximum dispersal distance for Microtus, the largest species in this study, was considerably greater than that for Peromyscus which, in turn, was greater than that for Blarina, the smallest species studied (Tab. 2). In fact, winter dispersal abilities of Microtus may have been underestimated because the distance traveled by one individual injured during a laboratory trial was included in calculating this mean. Without this value, the mean dispersal distance of Microtus was 6.77 (SD = 0.59) km. On the other hand, dispersal distances of Blarina may be somewhat inflated because distance estimates increased with date of capture for this species (see Appendix E of Lomolino 1983), and most Blarina were captured in late March and April after ice break-up on the St. Lawrence River (all Microtus and Peromysctis were captured during March when the ice cover remained intact). 1 he effects of ambient temperature on dispersal distance is also consistent with predictions based upon bioenergetic considerations. Dispersal distance of Peromy'.fcus at VC was more than 16 timers greater than that for individuals running at -23°C (Tab. 2), Similarly, dispersal abilities of Blarina running at 5°C were approximately 18 times that for Blarina running at -15°C. By calculating total oxygen consumption for mammals run in the laboratory, I was able to estimate cost of transport (in ml O; g ' km"') in amount of fat stores utilized during running (assuming 2 I O3"' fat; see Schmnidt-Nielsen 1975. p. 211). Cost of transport at winter temperatures was over twice as high as that predicted for a mammal at thermal neutrality (see Taylor et al. 197(1). and was highest for individuals run at the coldest temperatures. Blarina exhibited the highest cost HOLARCTIC ECOLOGY M.i of transport of the three speeies studied, primarily beeause of its small size. Because cost of transport for Microtus was higher than that for Peromyscus at the same temperature, the higher winter dispersal ability of Microtus probably does not derive from it being more efficient at locomotion. Microtus must be able to utilize more energy stores for winter dispersal. Accordingly, total and percent fat utilized during runing was greater for Microtus than for Peromyscus (Tab. 2). The winter dispersal distances reported in Tab. 2 are theoretical maxima because they are straight-line distances run at relatively warm temperatures (> 0°C). Consequently, actual winter dispersal abilities of these species are probably less than those reported in this study (see Lomolino 1988 for a record of natural crossice movements by mammals along the St. Lawrence River). Moreover, because Peromyscus is nocturnal, temperatures it normally experiences during cross-ice movements should be considerably lower than those for diurnal species such as Microtus and Blarina (nighttime temperatures in the Thousand Island Region of the St. Lawrence River average 1 2 ^ lower than daytime temperatures; Lomolino 1983 and 1988). Therefore, because of the positive relationship between dispersal abilities and ambient temperatures, the actual cross-ice dispersal ability of I'eromysciis may approximate or, possibly, be less than that of Blarina. Summary and conclusion Consistent with bioenergetie considerations, winter dispersal abilities of three species of small mammals increased with body size of the species and with ambient temperatures. The greater dispersal ability of Microtus pennsylvanicus in comparison with Peromyscus leucopus results from its ability to utilize more energy re217 Denman. N. S. 1965. Colonization of the islands of the Gulf of St. Lawrence by mammals. - Ecology 46: 340-341. Hart, J. S. 1950. Interrelations of daily metabolic cycle, activity, and environmental temperatures of mice. - Can. J. Res. 28: 293-307. - 1952. Use of daily metabolic periodicities as a measure of the energy expended by activity of voluntary mice. - Can. J. Zool. 30: 90. - and Heroux. O. 1955. Exercise and temperature regulation in lemmings and rabbits. - Can. J. Biochem. Physiol. 33: 428-435. Hatt, R. T., Vantyne, J., Stuart. L. C. and Pope, C. H. 1948. Island life in Lake Michigan. - Cranbrook Inst. Sci, Bull. 27: 1-175. Herreid. C. F. Ill, and Kessel, B. 1967. Thermal conductance in birds and mammals. - Comp. Physiol. 21: 405-414. Jackson. H. H. T. 1919. An apparent effect of winter inactivity upon the distribution of mammals. - J. Mammal. I: 58-64. Jansky, L. 1959. Working oxygen consumption in two species of wild rodents {Microlus arvalis and Clelhrionomys glareolus). - Physiol. Bohemoslow. 8: 471-478. Linstedt.S.L. and Calder, W. A. III. 1981. Body size, physiological time, and longevity of homeothermic animals. Quart. Rev. Biol. 56: 1-16. Acknowledgements - D. Murrish, J. Titus and D. Wagner - and Boyce. M. 1985. Seasonality, fasting endurance and provided equipment, technical assistance and advice throughbody size in mammals. - Am. Nat. 125: 873-878. out this study. I thank B. Calder, W. McShea. D. Murrish, B. Lomolino. M. V. 1983. Island biogeograpohy. immigrant seWunder and two anonymous reviewers for their comments on lection, and body size of mammals on islands. - Ph.D. an earlier version of this manuscript. This study was supported thesis. State Univ. New York at Binghamton, USA. in part, by a grant from the Society of Sigma xi. - 1984. Immigrant selection, predatory exclusion and the distributions of Microtus pennsylvanicus and Blarina brevicauda on islands. - Am. Nat. 123: 468-483. - 1988. Winter immigration abilities and insular community References structure of mammals in temperate archipelagoes. - In: Aitchlson. C. W. 1987a. Review of winter trophic dynamics of Downhower, J. (ed.), Biogeography of the island region of soricine shrews. - Mammal. Rev. 17: 1-24. Western Lake Erie. Ohio Univ. Press. Columbus. OH. - 1987b. Winter energy requirements of soricine shrews. - Martinsen, D. L. 1969. Energetics and activity patterns of Mammal. Rev. 17: 25-38. shorttailed shrews (Blarina) on restricted diets. - Ecology Banfield. A. W. F. 1954. The role of ice in the distribution of 50: 505-510. mammals. - J. Mammal. 35; 104-107. Morrison, P. 1960. Some interrelations between weight and Beer. J. R., Lukens, P. R. and Olson, D. 1954. Small mammal hibernation function. -Bull. Mus. Comp. Zool., Harvard populations on islands of Basswood Lake, Minnesota. 124: 75-91. Ecology 35: 437-445. Packard, G. C. 1968. Oxygen consumption oi Microlus montaBradley, S. R. 1976. Temperature regulation and bioenergetics nus in relation to ambient temperatures. - J. Mammal. 49: of some microtine rodents. - Ph.D. thesis, Cornell Univ., 215-220. USA. Platt, W. J. 1974. Metabolic rates of short-tailed shrews. - . and Deavers. D. R- 1980. A re-examination of the relaPhysiol. Zoo!. 47: 75-90. tionship between thermal conductance and body weight in Pruitt, W. O., Jr. 1951. Mammals of the Chase Osbom Remammals. - Comp. Biochem. Physiol. 65: 465-476. serve. Sugar Island, Michigan. - J. Mammal. 32: 470-473. Buckner. C. H. 1964. Metabolism, food consumption, and Randolph, J. C. 1980a. Daily energy metabolism of two rofeeding behavior in four species of shrews. - Can. J. Zool. dents {Peromyscus leucopus and Tamias siriatus) in their 42: 259-272. natural environment. - Physiol. Ztxil. 53: 70-81. Calder, W. A. III. 1987. Scaling energetics of homeothermic - 1980b. Daily metabolic patternsof short-tailed shrews(B/«vertebrates: an operational allometry. - Ann. Rev. Physiol. rina brevicauda) in three natural seasonal temperature re49: 107-120. gimes. - J. Mammal. 61: 638-638. Cameron, A. W. 1958. Mammals of the islands in the Gulf of Schmidt-Nielsen. K. 1975. Animal physiology: adaptation and St. Lawrence. - Natt. Mus. Can. Bull. No. 154. environment. - Cambridge Univ. Press. MA. Deavers. D. R. 1976. Water metabolism and thermoregulation Taylor, C. R., Schmidt-Nielsen. K. and Rabb. J. L. 1970. in two rodents (Clethrionomys grapperi and Peromyscus Scaling of energetic cost of running to body size in mamleucopus) and an insectivore {Blarina hrevicauda) inhabitmals. Am. J. Physiol 219: 1104-1107. ing the same mesic environment. - Ph. D. thesis, Cornell Wunder, B. A, 1970. Energetics of running activity in MerUniv., USA. riam's chipmunk, Eutamias merriami. - Comp. Biochem. - and Hudson, J. W. 1977. Effect of cold exposure on water Physiol. 33: 821-836. requirements of three species of small mammals. - J. Appl. - 1975. A model for estimating metabolic rate of active or Physioi. 43: 121-125. resting mammals. - J. Theor. Biol. 49: 345-354. serves during running. The low winter dispersal ability of Blarina brevicauda, which is less than a third the size of Microlus or Feromyscus, results from the former's high cost of transport (ml O, g"' km"') at winter temperatures and its relatively low energy stores and/or energy utilization during running. The potential influence of subfreezing temperatures and activity on bioenergetics of small mammals certainly merits more attention in future studies. From an ecological standpoint, however, it is critical that we develop better estimates of energy stores available for activitives such as winter dispersal. Such information, combined with existing knowledge on physiological ecology, should provide valuable insights into the influence of bioenergetics on dispersal abilities and endurance times, and., in turn, the ecology and evolution of terrestrial mammals. HOLARCTIC ECOLOGY http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ecography Wiley

Bioenergetics of cross‐ice movements by Microtus pennsylvanicus, Peromyscus leucopus and Blarina brevicauda

Lomolino, Mark V.
Ecography , Volume 12 (3) – Oct 1, 1989
Download PDF
7 pages

Loading next page...
 
/lp/wiley/bioenergetics-of-cross-ice-movements-by-microtus-pennsylvanicus-ULDIF0Wm8k

References (35)

Publisher
Wiley
Copyright
Copyright © 1989 Wiley Subscription Services, Inc., A Wiley Company
ISSN
0906-7590
eISSN
1600-0587
DOI
10.1111/j.1600-0587.1989.tb00840.x
Publisher site
See Article on Publisher Site

Abstract

Lomolino. M, V. 1989. Bioenergetics of cross-ice movements by Microtus pennsylvanicus. Peromyscus leucopus and Blarina hrevicauda. Holarct, Ecol. 12: 213-218. Laboratory and field experiments were conducted to investigate bioenergetics of winter dispersal and to compare winter (cross-ice) dispersal abilities of three small mammals: Microtus pennsylvanicus. Peromyscus leucopus and Blarina brevicauda. Total metabolic rates increased with running activity and decreased as ambient temperatures increased for all species. Thermal conductance was significantly higher for running than for resting Microtus and Peromyscus, but decreased significantly with activity for Blarina. Winter dispersal abilities, calculated from treadmill experiments, increased with ambient temperature and with body size of the species. The superior dispersal ability of Microlus in comparison with Peromyscus results from the former's ability to utilize more energy reserves during running. The comparatively low winter dispersal ability of Blarina, which was less than a third of the two rodent species, resulted from its high weight specific cost of transport at winter temperatures and its relatively low energy stores and/or energy utilization during running, M. V. Lomolino, Dept of Ecology and Evolutionary Biology, Univ. of Arizona, Tucson, AZ 85721. USA. Introduction Studies of the tnatnmalian fautia iti the Thousand Island Regioti of the St, Lawrence River. New York. USA. indicated that cross-ice movements during winter play an important role in determining insular community structure of terrestrial mammals (Lomolino 1983. 1984 and 1988). Seasonally inactive speeies. which have little opportunity to utilize the winter's ice eover, are disproportionately infrequent members of insular commutiities. The paucity of winter inactive species has been reported for other insular communities in temperate regions and appears to be a general phenomenon where ice cover provides a seasonally available mode of immigration {Jackson 1919. Hatt et al, 1948. Pruitt l^.^l. Beer et al. 1954. Banfield I9M, Cameron 1958. Denman 1965), Despite the potential importance of winter immigration abilities in determining insular community structure, there is little information available on absolute or even relative, cross-ice dispersal abilities (distances) of Accepted 10 November 1988 v(j) HOLARCTIC ECOLOGY HOLARCTIC ECOLOGY 12:3 (1989) terrestrial mammals. Existing models on bioenergetics of locomotion in mammals, however, enable a first approximation of cross-iee immigration abilities (Taylor et al, 1970. Wunder 1975, see also Linstedt and Boyce 1985, Aitehison 1987a. 1987b, Calder 1987). Maximum distance a mammal can travel across ice (void of food) may be calculated as energy stores divided by energy used per km traveled. The total rate of energy use during dispersal is equal to the sum of rates of energy use for basal metabolism (Eh), thermoregulation {E|), and locomotion (E,), Each of these rates and, therefore, the total rate of energy expenditure during dispersal is a less-than-linear function of body mass (Eh a M"". E, a M"^" and E, a M""; see Wunder 1975 and references therein). In contrast, energy stores in mammals are at least a linear function of body mass (Morrison 196{), Linstedt and Calder 1981, Linstedt and Boyee 1985), Therefore, maximum winter cross-ice dispersal distances of mammals should increase with body mass. In addition, because thermoregulatory expenditures decrease as ambient temperatures increase, winter 80 -- 0123- KEY RMR AMR, 1,4 km/hr AMR, 2,0 km/hr AMR, 2.6 km/hr 60 -- UJ Fig. I, Resting and active metabolic rates (RMR and AMR) of Microlus pennsylvanicus as a function of ambient temperature and running velocity (see Tab, 1), Metabolic rates are expressed as ml O; g""^ h ' so that the slope of the line relating metabolic rate lo temperature is equal to thermal conductance (in mi O^-oih-'X-'isee methods). I< Q: 40-- _i o m < tiJ 20-- -10 0 AMBIENT +10 TEMPERATURE (C) dispersal abilities should increase with ambient temperatures. Here I test the above predictions and compare dispersal abilities of three species of small mammals at winter temperatures. seeds, peanut butter and laboratory mouse chow, whereas Blarina was fed freshly-killed lab mice iMus musculus) in addition to the above foods. All cages were kept in an environmental chamber under a natural photoperiod at \5''C. Metabolism studies were conducted using a 4-1 plexiglass chamber equipped with a treadmill. Metabolic rates were measured using an open-flow system (flow rate = 6.6 I min"') with an ADC (Model 225) infra-red Materials and methods gas analyzer to monitor CO, evolution. Oxygen conBoth laboratory and field experiments were used to sumption was calculated assuming a respiratory quoinvestigate and compare winter dispersal abilities of tient (RQ) of 0,80 (see Buckner 1964, Randolph 1980a three species of small mammals: Microtus pennsylvan- and 198(lb), icus, Peromyscus leucopus, and Blarina brevicada. Food was removed from cages 3 h prior to the start of the metabolism experiments with Microlus and Peromyscus, and 1 h prior to the start of experiments with Blarina. Metabolism runs for each species were conLaboratory experimenls ducted during each species" major activity period (i.e. The mammals used in this study were captured in New IIKM) to 16(K) h EST (Eastern Standard Time) for MicroYork State, USA. during March and April 1982, Micro- tus and Blarina and 19(K) to 23()() h for Peromyscus). Prior to each run, individuals were weighed to the lus and Peromyscus were trapped along the St. Lawrence River in Jefferson County, and Blarina was cap- nearest 0.1 g. then placed in the metabolism chamber tured in Broome County where metabolism studies for a 5 min adjustment period. Metabolic rates of Microtus were measured for resting and active individuals were conducted. All individuals were kept in scperate cages with wood (velocity = 0 to 3 km h"') at ambient temperatures shavings and soil, and food and water were supplied ad between —15 and +25°C, with the metabolism chamber libitum. Microlus and Peromvscus were fed sunflower placed in a top-loading freezer (ambient temperature < HOLARCnC ECOLOGY 12:1 Tab. I. Effects of running activity and subfreezing temperatures on thermal conductance (TCinml O^g'^^h"' "C ')for Microtm pennsylvanieus, Peromyscus leucopus and Blarina brevicauda. Values presented are means with standard deviations in parentheSpeeies Velocity (kmh"') -14 to +2(fC N TC N 0 to +25 TC N -14 to +6°C TC Microius - at rest - running all speeds L4 2.0 2.6 0.0 2.3 0.0 ].3 0.% 1.22 1.24 1.27 1.16 (0.167) (0.104)(0.178) (0.162) (0.178) _ - (0.166) (0.170) (0.253) (0.387) (0.276) 1.71 1.79 1.97 1.76 1,76 (0.189) (0.194) (0.377) (0.367) (0.325) Peromyscus liUirina 1.00 (0.160) 1.97 (0.295) 1.23 (0.148) 0.93 (0.107) " Conductances over the two temperature ranges. 0 to 25°C and -14 to +6X differed for all velocities (p <^ 0,01; t-test). " This value for resting metabolic rate in M. pennsylvanieus did not differ (t = 0.41, P > 0.50) from that reported by Bradley (1976) for this species in central New York State, USA (conductance = 0.98 (0.045), N - 53). ' Vertical bars indicate those values that did not differ from each other (P > 0.05); otherwise P < 0.01. Values for thermal conductance of Peromyscus and Blarina at rest were taken from Deavers (1976). -5°C) or walk-in environmental chamber. Almost all metabolism rates of Peromyscus and Blarina, which were recorded during maximum dispersal distance experiments, were measured for active individuals (velocity ^ 2 to 3 ktn h"') at ambient temperatures between 0 and I5°C. Maximum distances these species can travel across ice were estimated by running animals at relatively warm winter temperatures (~5°C) to minimize thermoregulatory costs (ice-melt above this temperature would preclude cross-ice movements). Running speeds were maintained at those which seemed optimal for each individual. Runs were terminated when individuals were apparently exhausted and were unable to run again after a 5 min rest period. Individuals were then removed from the chamber and weighed, and total distance traveled was recorded. Total oxygen consumption (total CO, evolution for RQ of O.SII) was recorded to estimate the cost of transport and the total amount of energy reserves used for running a given distance (see Lomolino 1983 for additional details of laboratory methods). invariably void of food, and the characteristics of its snow-cover prevented tunneling. Winds at the ice surface were consistently less than 5 kg h"'. Total distance traveled by these mammals was measured using a modified activity wheel attached to a 1 m handle (see Lomolino 1983, p. 151). and velocity was calculated from the time it took to travel a measured distance. Experiments were terminated when the individuals could no longer re-initiate running after repeated prodding. Results and discussion Effects of temperature and velocity on conductance and metabolism Because total thermal conductance in mammals increases in proportion to M"'^ (Herreid and Kessel 1967, Bradley and Deavers 1980). I expressed conductance in units of ml O, g ' " h ' " C ' . This corrected for differences in body mass and allowed calculation of thermal conductance as the negative slope of the line relating metabolic rate (in ml O, Og" ^ h ') to ambient temperature. As predicted, metabolic rate increased with velocity and decreased as ambient temperature increased (Figs 1-3). Thermal conductance of Microtus at rest (ambient temperature = - 1 4 to +2i)°C) did not differ significantly from that reported by Bradley (1976) for this speeies in central New York State. USA (Tab. 1). In addition, the regression line for resting metabolie rate (RMR) of Microius intercepts the abscissa at 39.7''C. which is not different (P > 0.20) from the mean body temperature Field experiments In addtition to laboratory studies. I also investigated dispersal abilities of Peromyscus and Blarina under more realistic conditions by releasing them onto the ice of the St. Lawrence River during February 1979. These studies were conducted at relatively cold temperatures (^ -L*i°C) to avoid ice-melt and unsafe conditions which exist during warmer periods. As in the laboratory experiments, individuals were released during their major activity period. The ice was 1!O[,AR(T1C ECOLOGY \1 AMBIENT TEMPERATURE iC) Fig. 2. Active metabolic rates of Peromyscus leucopus as a function of ambient temperature (mean velocity = 2.3 km h ' ' , CT - thermal conductance in ml O^ g""'^ h"' °C"'). reported for Microtus by Bradley (1976; T^ (SD) = 38.5 (1.04), N - 109, t - 1.15). Running resulted in a significant increase in thermal conductance for both Microtus and Peromyscus (Tab. 1). That is, these species lost heat much more rapidly while running, and the heat produced by running did not compensate for the Increased conductance. In contrast, thermal conductance for Blarina while running was significantly tower than that reported for resting Blarina by Deavers (1976; see also Platt 1974). Because running had a significant effect on thermal conductance, overall effects of velocity and temperature on metabolic rate may be best expressed by including an interaction term (V*AT) in any model that is used to predict metabolic rate (regression model is MR (in ml 0 ; g-' h-') = k,(M-"^) (delta T) + k2(M-'''') (V) + kj(V) (delta T); M = mass, V = velocity in km h"' and delta T - lower critical temperature minus ambient temperature). Multiple regression analysis of metabolic rate for Microtus revealed that the interaction between ambient temperature and velocity was significant (P = .02; N - 58, r^ of the entire model = 0.81, F = 75.45 and P < O.(X)Ol). Thermal conductance was also affected by the range of temperatures over which experiments were conducted. For Microtus, thermal conductance was much higher for experiments run at subfreezing temperatures (P < 0.01; Tab. 1 and Fig. 1). For Peromyscus thermal conductance remained fairly constant (Fig. 2). Estimated thermal conductance for active Blarina (Fig. 3) was highest for individuals run between 0 and iCC, but decreased for individuals run at subfreezing temperatures (ambient temperature 0°C). Either the increased heat of activity contributed to thermoregulation or these shrews exhausted their aerobic capacities. Indeed, active metabolic rates of Blarina at subfreezing temperatures were over seven times the minimal metabolic rate reported for Blarina (Martinsen 1969). In summary, thermal conductance of the three species was not constant, but varied with running activity 216 and ambient temperature. In contrast, other studies on metabolism of small mammals during activity and thermal stress report relatively constant thermal conductances (e.g. see Hart 1950, 1952, Hart and Heroux 1955, Packard 1968, Bradley 1976, Deavers and Hudson 1977; but see also Wunder 1970). Apparently, in these species increased heat production of activity compensated for increases in rate of heat loss due to changes in posture and perfusion. Jansky (1959), however, reported that the thermal conductance of Clethrionomys glareolus decreased with activity, which is opposite to what I found for M. pennsylvanicus and P. leucopus in this study. Jansky suggested that some of the heat produced by exercise was used in thermoregulation, and thus metabolic rates increased less rapidly with decreasing temperatures for active vs resting individuals. Similarly, Platt (1974) reported that the heat produced by activity in B. brevicauda was used for thermoregulation, i.e. thermal conductance was lower for active vs resting shrews as reported in this study. Therefore, although many species exhibit a relatively constant thermal conductance, this is certainly not the rule for mammals. The observed increase in thermal conductance for Microtus at subfreezing temperatures may have resulted from increased blood flow to the extremities which would prevent freezing, but concomitantly, raise conductance. Because perfusion rates were not measured during these experiments, the above explanation remains tentative. Obviously, more focused studies on the factors affecting thermal conductance is warranted. Winter dispersal abilities Estimates of maximum winter dispersal distances from both laboratory and field experiments are presented in Tab. 2. Although the limited sample sizes do not justify AMBIENT TEMPERATURE (C) Fig. 3. Active and resting metabolic rates (closed and open circles, respectively) of Blarina brevicauda as a function of ambient temperature (mean velocity = 1.3 km h ', CT = thermal conductance of active individuals in ml O-. g ""'' h"' =c') HOLARCTIC ECOLOGY 12: Tab. 2. Distance traveled by Microtus pennsylvanicus, Peromyscus leucopus and Blarina hrevicauda ;it witilcr temperatures in the laboratory (LAB) or on the ice of the St. Lawrence River (FIELD). Values presented are species means with standard deviations included in parentheses unless otherwise indicated. Parameter Microfus LAB N 4 Peromyscus FIELD LAB 4 23.0 (4.1) -24.8 (8.0) 3.31(1.94) 0.24(0.15) Blarina FIELD 1 15.0 -14.8 0.83 0.07 20.9 2.86 LAB 6 Mass (g) Temperature (C) Velocity (km h"') Distance (km) Total 0^ consumption (L) Estimated fat use g (% of mass)* Cost of transport - in TNZ*' (77)59) 29.6 (8.0) • 7.3 (0.78) 2.02(0.07) 5.82(1.72) 0.98(0.19) 0.49(1.7%) 5.76(1.24) 2.18 4 27.4 (2.4) 7,1 (1.4) 2.36(0.21) 4.(K)(3.1.1) 0.47(0.28) 4.49(1.05) 2.25 22.0 (1.5) 4,6 (1.1) 1.15(0.18) 1.26(L22) 0.41(0.064) 0.14(0.6%) 9.84 2.46 1'his includes distance traveled by an individual during an aborted run: without this value, mean distance traveled by Microtus = Liters of O. consumed while running only. Fat utilization was calculated assuming conversion factor of 2 liter Oi per g fat used (see Schmidt-Nielsen 1975, p. 2U). •Cost nf Transport (COT in ml O, g"' km"') in thermal neutral zone (TNZ) was calculated using the formula COT = 8.46(M"''); see Taylor et al. (1970). speculation on intraspecific patterns, these data are sufficient to provide a first estimate of cross-ice dispersal abilities and comparisons among species. As predicted, winter dispersal distances increased with body size of the species. The mean maximum dispersal distance for Microtus, the largest species in this study, was considerably greater than that for Peromyscus which, in turn, was greater than that for Blarina, the smallest species studied (Tab. 2). In fact, winter dispersal abilities of Microtus may have been underestimated because the distance traveled by one individual injured during a laboratory trial was included in calculating this mean. Without this value, the mean dispersal distance of Microtus was 6.77 (SD = 0.59) km. On the other hand, dispersal distances of Blarina may be somewhat inflated because distance estimates increased with date of capture for this species (see Appendix E of Lomolino 1983), and most Blarina were captured in late March and April after ice break-up on the St. Lawrence River (all Microtus and Peromysctis were captured during March when the ice cover remained intact). 1 he effects of ambient temperature on dispersal distance is also consistent with predictions based upon bioenergetic considerations. Dispersal distance of Peromy'.fcus at VC was more than 16 timers greater than that for individuals running at -23°C (Tab. 2), Similarly, dispersal abilities of Blarina running at 5°C were approximately 18 times that for Blarina running at -15°C. By calculating total oxygen consumption for mammals run in the laboratory, I was able to estimate cost of transport (in ml O; g ' km"') in amount of fat stores utilized during running (assuming 2 I O3"' fat; see Schmnidt-Nielsen 1975. p. 211). Cost of transport at winter temperatures was over twice as high as that predicted for a mammal at thermal neutrality (see Taylor et al. 197(1). and was highest for individuals run at the coldest temperatures. Blarina exhibited the highest cost HOLARCTIC ECOLOGY M.i of transport of the three speeies studied, primarily beeause of its small size. Because cost of transport for Microtus was higher than that for Peromyscus at the same temperature, the higher winter dispersal ability of Microtus probably does not derive from it being more efficient at locomotion. Microtus must be able to utilize more energy stores for winter dispersal. Accordingly, total and percent fat utilized during runing was greater for Microtus than for Peromyscus (Tab. 2). The winter dispersal distances reported in Tab. 2 are theoretical maxima because they are straight-line distances run at relatively warm temperatures (> 0°C). Consequently, actual winter dispersal abilities of these species are probably less than those reported in this study (see Lomolino 1988 for a record of natural crossice movements by mammals along the St. Lawrence River). Moreover, because Peromyscus is nocturnal, temperatures it normally experiences during cross-ice movements should be considerably lower than those for diurnal species such as Microtus and Blarina (nighttime temperatures in the Thousand Island Region of the St. Lawrence River average 1 2 ^ lower than daytime temperatures; Lomolino 1983 and 1988). Therefore, because of the positive relationship between dispersal abilities and ambient temperatures, the actual cross-ice dispersal ability of I'eromysciis may approximate or, possibly, be less than that of Blarina. Summary and conclusion Consistent with bioenergetie considerations, winter dispersal abilities of three species of small mammals increased with body size of the species and with ambient temperatures. The greater dispersal ability of Microtus pennsylvanicus in comparison with Peromyscus leucopus results from its ability to utilize more energy re217 Denman. N. S. 1965. Colonization of the islands of the Gulf of St. Lawrence by mammals. - Ecology 46: 340-341. Hart, J. S. 1950. Interrelations of daily metabolic cycle, activity, and environmental temperatures of mice. - Can. J. Res. 28: 293-307. - 1952. Use of daily metabolic periodicities as a measure of the energy expended by activity of voluntary mice. - Can. J. Zool. 30: 90. - and Heroux. O. 1955. Exercise and temperature regulation in lemmings and rabbits. - Can. J. Biochem. Physiol. 33: 428-435. Hatt, R. T., Vantyne, J., Stuart. L. C. and Pope, C. H. 1948. Island life in Lake Michigan. - Cranbrook Inst. Sci, Bull. 27: 1-175. Herreid. C. F. Ill, and Kessel, B. 1967. Thermal conductance in birds and mammals. - Comp. Physiol. 21: 405-414. Jackson. H. H. T. 1919. An apparent effect of winter inactivity upon the distribution of mammals. - J. Mammal. I: 58-64. Jansky, L. 1959. Working oxygen consumption in two species of wild rodents {Microlus arvalis and Clelhrionomys glareolus). - Physiol. Bohemoslow. 8: 471-478. Linstedt.S.L. and Calder, W. A. III. 1981. Body size, physiological time, and longevity of homeothermic animals. Quart. Rev. Biol. 56: 1-16. Acknowledgements - D. Murrish, J. Titus and D. Wagner - and Boyce. M. 1985. Seasonality, fasting endurance and provided equipment, technical assistance and advice throughbody size in mammals. - Am. Nat. 125: 873-878. out this study. I thank B. Calder, W. McShea. D. Murrish, B. Lomolino. M. V. 1983. Island biogeograpohy. immigrant seWunder and two anonymous reviewers for their comments on lection, and body size of mammals on islands. - Ph.D. an earlier version of this manuscript. This study was supported thesis. State Univ. New York at Binghamton, USA. in part, by a grant from the Society of Sigma xi. - 1984. Immigrant selection, predatory exclusion and the distributions of Microtus pennsylvanicus and Blarina brevicauda on islands. - Am. Nat. 123: 468-483. - 1988. Winter immigration abilities and insular community References structure of mammals in temperate archipelagoes. - In: Aitchlson. C. W. 1987a. Review of winter trophic dynamics of Downhower, J. (ed.), Biogeography of the island region of soricine shrews. - Mammal. Rev. 17: 1-24. Western Lake Erie. Ohio Univ. Press. Columbus. OH. - 1987b. Winter energy requirements of soricine shrews. - Martinsen, D. L. 1969. Energetics and activity patterns of Mammal. Rev. 17: 25-38. shorttailed shrews (Blarina) on restricted diets. - Ecology Banfield. A. W. F. 1954. The role of ice in the distribution of 50: 505-510. mammals. - J. Mammal. 35; 104-107. Morrison, P. 1960. Some interrelations between weight and Beer. J. R., Lukens, P. R. and Olson, D. 1954. Small mammal hibernation function. -Bull. Mus. Comp. Zool., Harvard populations on islands of Basswood Lake, Minnesota. 124: 75-91. Ecology 35: 437-445. Packard, G. C. 1968. Oxygen consumption oi Microlus montaBradley, S. R. 1976. Temperature regulation and bioenergetics nus in relation to ambient temperatures. - J. Mammal. 49: of some microtine rodents. - Ph.D. thesis, Cornell Univ., 215-220. USA. Platt, W. J. 1974. Metabolic rates of short-tailed shrews. - . and Deavers. D. R- 1980. A re-examination of the relaPhysiol. Zoo!. 47: 75-90. tionship between thermal conductance and body weight in Pruitt, W. O., Jr. 1951. Mammals of the Chase Osbom Remammals. - Comp. Biochem. Physiol. 65: 465-476. serve. Sugar Island, Michigan. - J. Mammal. 32: 470-473. Buckner. C. H. 1964. Metabolism, food consumption, and Randolph, J. C. 1980a. Daily energy metabolism of two rofeeding behavior in four species of shrews. - Can. J. Zool. dents {Peromyscus leucopus and Tamias siriatus) in their 42: 259-272. natural environment. - Physiol. Ztxil. 53: 70-81. Calder, W. A. III. 1987. Scaling energetics of homeothermic - 1980b. Daily metabolic patternsof short-tailed shrews(B/«vertebrates: an operational allometry. - Ann. Rev. Physiol. rina brevicauda) in three natural seasonal temperature re49: 107-120. gimes. - J. Mammal. 61: 638-638. Cameron, A. W. 1958. Mammals of the islands in the Gulf of Schmidt-Nielsen. K. 1975. Animal physiology: adaptation and St. Lawrence. - Natt. Mus. Can. Bull. No. 154. environment. - Cambridge Univ. Press. MA. Deavers. D. R. 1976. Water metabolism and thermoregulation Taylor, C. R., Schmidt-Nielsen. K. and Rabb. J. L. 1970. in two rodents (Clethrionomys grapperi and Peromyscus Scaling of energetic cost of running to body size in mamleucopus) and an insectivore {Blarina hrevicauda) inhabitmals. Am. J. Physiol 219: 1104-1107. ing the same mesic environment. - Ph. D. thesis, Cornell Wunder, B. A, 1970. Energetics of running activity in MerUniv., USA. riam's chipmunk, Eutamias merriami. - Comp. Biochem. - and Hudson, J. W. 1977. Effect of cold exposure on water Physiol. 33: 821-836. requirements of three species of small mammals. - J. Appl. - 1975. A model for estimating metabolic rate of active or Physioi. 43: 121-125. resting mammals. - J. Theor. Biol. 49: 345-354. serves during running. The low winter dispersal ability of Blarina brevicauda, which is less than a third the size of Microlus or Feromyscus, results from the former's high cost of transport (ml O, g"' km"') at winter temperatures and its relatively low energy stores and/or energy utilization during running. The potential influence of subfreezing temperatures and activity on bioenergetics of small mammals certainly merits more attention in future studies. From an ecological standpoint, however, it is critical that we develop better estimates of energy stores available for activitives such as winter dispersal. Such information, combined with existing knowledge on physiological ecology, should provide valuable insights into the influence of bioenergetics on dispersal abilities and endurance times, and., in turn, the ecology and evolution of terrestrial mammals. HOLARCTIC ECOLOGY

Journal

Ecography – Wiley

Published: Oct 1, 1989

There are no references for this article.