Melanism as a potential thermal benefit in eastern fox squirrels (Sciurus niger)
DOI:
https://doi.org/10.2478/eje-2019-0013Keywords:
Eastern Fox Squirrel, Melanism, Sciurus niger, ThermoregulationAbstract
Melanistic fox squirrels (Sciurus niger) have expanded westward and increased in frequency in the Omaha, Nebraska, and Council Bluffs, Iowa, metropolitan areas. The selective advantage of melanism is currently unknown, but thermal advantages have been hypothesized, especially in winter. No difference in metabolic response curves were measured between melanistic (black) and rufus (orange) fox squirrels. When exposed to sunny skies, both melanistic and rufus squirrels had higher surface (skin and fur) temperature as ambient temperatures increased. Melanistic squirrel surface temperatures did not differ when squirrels were exposed to sunny or cloudy skies. However, rufus individuals showed significantly lower increases in surface temperatures when under cloudy skies. During fall months, rufus individuals were about 1.5 times more active throughout the day than melanistic individuals. However, in winter, melanistic fox squirrels were approximately 30% more active in the mornings (before 13:00) compared to rufus squirrels. Pre-winter body condition was higher in melanistic (25.5 ± 1.8 g/cm) compared to rufus (20.30 ± 3.6 g/cm) fox squirrels; however, there were no significant differences between melanistic (22.8 ± 1.4 g/cm) and rufus (23.9 ± 0.8 g/cm) fox squirrel post-winter body condition. The results of this study indicate that melanistic fox squirrels may have a slight winter thermal advantage over rufus fox squirrels by maintaining higher skin temperatures.References
Altman, P. & Shapiro, D. (1974) Testing assumptions of data selection in
focal animal sampling. Behaviour, 67,115-133.
Arenz, C. (1997) Handling fox squirrels: ketamine-hydrochloride versus
a simple restraint. Wild. Soc. Bull., 25,107-109.
Armitage, K. (2009) Fur color diversity in marmots. Ethol., Ecol. and
Evol., 21,183-194.
Audubon, J. (1843) The Missouri River Journals of John James Audubon.
University of Nebraska Press, D. Patterson, Ed. 512pp.
Banfield, A. W. F. (1974) The mammals of Canada. University of Toronto
Press, Toronto, Canada. 438pp.
Barnes, T. L., R. M. Kubik, C. N. Cadaret, K. A. Beede, E. M. Merrick, S.
Chung, T. S. Schmidt, J. L. Petersen, and D. T. Yates. 2017. Identifying
hyperthermia in heat-stressed lambs and its effects on b
agonist-stimulated glucose oxidation in muscle. Proc. Amer. Soc.
Ainim. Sci. 68:25-29.
Bittner, T., King, R. & Kerfin, J. (2002) Effects of body size and melanism
on the thermal biology of garter snakes (Thamnophis sirtalis).
Copeia, 2,477-482.
Campbell, K. L. & Hochachka, P. W. (2000) Thermal biology and metabolism
of the American shrew-mole, Neurotrichus gibbsii. J.
Mammal., 82,578-585.
Caro, T. (2005) The adaptive significance of coloration in mammals.
Biosci., 55,125-136.
Clusella-Trullas, S., van Wyk, J. H. & Spotila, J. R. (2009) Thermal benefits
of melanism in cordylid lizards: a theoretical and field test.
Ecol., 90,2297-2312.
Cooper, C. E., Walsberg, G. E. & Withers, P. C. (2003) Biophysical properties
of the pelt of a diurnal marsupial, the numbat (Myrmecobius
fasciatus), and its role in thermoregulation. J. Exper. Biol.,
206,2771-2777.
Ellis, H. I. (1980) Metabolism and solar radiation in dark and white herons
in hot climates. Physiol. Zool., 53,358-372.
Foresman, A. (1995) Opposing fitness consequences of colour pattern
in male and female snakes. J. Evol. Biol., 8,53-70.
Fratto, M. & Davis, A. (2011) Do black-furred animals compensate for
high solar absorption with smaller hairs? A test with a polymorphic
squirrel species. Current Zool., 57,731-736.
Geen, M. R. S. & Johnston., G. R. (2014) Coloration affects heating and
cooling in three color morphs of the Australian bluetongue lizard,
Tiliqua scincoides. J. Thermal Biol., 43,54-60.
Geeslin, H. (1970) A radio-tracking study of home range, movements,
and habitat uses of the fox squirrel (Sciurus niger) in East Texas.
MSc. Thesis: Texas A & M University, College Station.
Gillooly, J. F., Brown,, J. H., West, G. B., Savage, V. M. & Charnov, E. L.
(2001) Effects of size and temperature on metabolic rate. Science,
293,2248-2251.
Grojean, R. E., Sousa, J. A. & Henry, M. C. (1980) Utilization of solar
radiation by polar animals: an optical model for pelts. Appl. Optics,
19,339-346.
Gustafson, E. J. & VanDruff, L. W. (1990) Behavior of black and grey
morphs of Sciurus carolinensis in an urban environment. Amer.
Mid. Nat., 123,186-192.
Hamilton, W. & Heppner, F. (1967) Radiant solar energy and the function
of black homeotherm pigmentation: an hypothesis. Science,
155,196-197.
Heppner, F. (1970) The metabolic significance of differential absorption
of radiant energy by black and white birds. Condor, 73,50-59.
Hubbard, J. K., Uy, J. A., Hauber, M. E., Hoekstra, H. E. & Safran, R. J.
(2010) Vertebrate pigmentation: from underlying genes to
adaptive function. Trend. Gen., 26,231-239.
Huggins, G., & Gee, K. (1995) Efficiency and selectivity of cage trap sets
for gray and fox squirrels. Wild. Soc. Bull., 23,204-207.
Ibanez, A., Pellitteri, D., Sacchi, R., Lopez, P. & Martin, J. (2016) Melaninbased
coloration covaries with hiding and exploratory behavior
in male Spanish terrapins. Ethol., 122,30-36.
Innes, S. & Lavigne, D. M. (1979) Comparative energetics of coat colour
polymorphs in the eastern grey squirrel, Sciurus carolinensis.
Can. J. Zool., 57,585-592.
Kawanishi, K., Sunquist, M. E., Eizirik, E., Lynam, A. J., Ngoprasert, D.,
Wan Shahruddin, W. N., Rayan, D. M., Sharma, D. S. K. & Steinmetz,
R. (2010) Near fixation of melanism in leopards of the Malay
peninsula. J. Zool., 282,201–206.
Keeler, C., Ridgway, S., Lipscomb, L. & Fromm, E. (1968) The genetics of
adrenal size and tameness in colorphase foxes. J. Hered., 59,82-
84.
Keeler, C., Mellinger, T., Fromm, E. & Wade, L. (1970) Melanin, adrenalin,
and the legacy of fear. J. Hered., 61,81-88.
Kiltie, R. (1989) Wildfire and the evolution of dorsal melanism in fox
squirrels, Sciurus niger. J. Mammal, 70,726-739.
Kiltie, R. (1992a) Comparisons among fox squirrels from the Mississippi
River Delta. J. Mammal., 73,906-913.
Kiltie, R. (1992b) Tests of hypotheses on predation as a factor maintaining
polymorphic melanism in coastal plain fox squirrels (Sciurus
niger L.). Biological J. Linn. Soc., 45,17-37.
Kingsley, E. P., Manceau, M., Wiley, C. D. & Hoekstra, H. E. (2009) Melanism
in Peromyscus is caused by independent mutations in
Agouti. PLoS One, 4:e6435.
Koprowski, J. (1994) Mammalian species Sciurus niger. Mammal Species
Account No. 479 9pp.
Linnen, C. R., Kingsley, E.P., Jensen, J. D. & Hoekstra, H. E. (2009) On the
origin and spread of an adaptive allele in deer mice. Science,
325,1095-1098.
Lueninghoener, E. (1973) An investigation of the melanistic phase of
the western fox squirrel (Sciurus niger rufiventer) in eastern Nebraska
and western Iowa. MSc. Thesis, University of Nebraska
at Omaha.
Luiselli, L. (1992) Reproductive success in melanistic adders: a new
hypothesis and some considerations on Andrѐn and Nilson’s
(1981) suggestions. Oikos, 64,60-604.
Lurz, P. W. W. & Lloyd, A. J. (2000) Body weights in grey and red squirrels:
do seasonal weight increases in conifer woodland? J. Zool.,
252,531-547.
McNab, B. K. (2002) The Physiological Ecology of Vertebrates. Cornell
University Press. 576pp.
McNab, B. K. (2012) Extreme Measures. Chicago: The University of Chicago
Press. 312pp.
McRobie, H., Thomas, A. & Kelly, J. (2009) The genetic basis of melanism
in the gray squirrel (Sciurus carolinensis). J. Hered.,
100,709-714.
McRobie, H. R., King, L. M., Fanutti, C., Coussons, P. J., Moncrief, N. D.
& Thomas, A. P. (2014) Melanocortin 1 receptor (MC1R) gene
sequence variation and melanism in the gray (Sciurus carolinensis),
fox (Sciurus niger), and red (Sciurus vulgaris) squirrel. J.
Hered., 105,423-428.
Nachman, M. W., H. E. Hoekstra & S. L. D’Agostino. (2003) The genetic
basis of adaptive melanism in pocket mice. Proceedings of the
National Academy of Sciences of the United States of America,
100,5268–5273.
Protas, M. E. & Patel, N. H. (2008) Evolution of coloration patterns. Ann.
Rev. Cell Develop. Biol., 24:425-446.
Robertson, G. I. (1973) Distribution of color morphs of Sciurus carolinensis
in eastern North America. MSc. Thesis, University of Western
Ontario. 78pp.
Rosenblum, E. (2005) The role of phenotypic plasticity in color variation
in Tularosa Basin lizards. Copeia, 2005,586-596.
SAS Institute, Inc. (2002) Statistical analysis system user’s guide: statistics,
version 8. SAS Institute Inc., Clay, North Carolina, USA.
Schneider, A., David, V. A., Johnson, W. E., O’Brien, S. J., Barsh, G. S.,
Menotti-Raymond, M. & Eizirik, E. (2012) How the leopard
hides its spots: ASIP mutations and melanism in wild cats. PloS
one, 7:e50386.
Schulte-Hostedde, A, Zinner, B., Millar, J. S. & Hickling, G. J. (2005) Restitution
of mass-size residuals: validating body condition indices.
Ecol., 86,155-163.
Sherbrooke W, Castrucci, A. & Hadley, M. (1994) Temperature effects
on in vitro skin darkening in the Mountain Spiny Lizard, Sceloporus
jarrovii: a thermoregulatory adaptation? Physiol. Zool.,
67,659-672.
Short, H. & Duke, W. (1971) Seasonal food consumption and body
weights of captive tree squirrels. J. Wild. Manage., 35,435-439.
Sikes, R., Gannon, W. & American Care and Use Committee of the
American Society of Mammalogists. (2011) Guidelines of the
American society of mammalogists for the use of wild mammals
in research. J. Mammal., 92,235-253.
Steele, M. A. & Koprowski, J. L. (2001) North American Tree Squirrels.
Smithsonian Institution Press. 201pp.
Tanaka, K. (2005) Thermal aspects of melanistic and striped morphs of
the snake Elaphe quadrivirgata. Zool. Sci., 22,1173-1179.
Walsberg, G. E., Campbell, G. S. & King, J. R. (1978) Animal coat color
and radiative heat gain: a re-evaluation. J. Comp. Physiol.,
126,211-22.
Walsberg, G. E. (1988) The significance of fur structure for solar heat
gain in the rock squirrel, Spermophilus variegatus. J. Exp. Biol.,
138,243-257.
Walsberg G. (1983) Coat color and solar heat gain in animals. BioSci.,
33,88-91.
Walsberg, G. E. (1990) Convergence of solar heat gain in two squirrel
species with contrasting coat colors. Physiol. Zool., 63,1025-
1042.
Walsberg, G. E. (1992) Quantifying radiative heat gain in animals. Am.
Zool., 32,217-224.
Walsberg, G. E. & Schmidt, C. A. (1989) Seasonal adjustment of solar
heat gain in a desert mammal by altering coat properties independently
of surface coloration. J. Exper. Biol., 142,387-400.
Walsberg, G. & Wolf, B. (1995) Effects of solar radiation and wind speed
on metabolic heat production by two mammals with contrasting
coat colours. J. Exper. Biol., 198,1499-1507.
Wauters, L. & Dhondt, A. (1989) Body weight, longevity and reproductive
success in red squirrels (Sciurus vulgaris). J. Anim. Ecol.,
58,637-651.
Wilson, J. (2013) Western expansion of melanistic fox squirrels (Sciurus
niger) in Omaha, Nebraska. Am. Mid. Nat., 170,393-401.
Wooden, K. M. & Walsberg, G. E. (2000) Effect of wind and solar radiation
on metabolic heat production in a small desert rodent,
Spermophilus tereticaudus. J. Exper. Biol., 203,879-888.
focal animal sampling. Behaviour, 67,115-133.
Arenz, C. (1997) Handling fox squirrels: ketamine-hydrochloride versus
a simple restraint. Wild. Soc. Bull., 25,107-109.
Armitage, K. (2009) Fur color diversity in marmots. Ethol., Ecol. and
Evol., 21,183-194.
Audubon, J. (1843) The Missouri River Journals of John James Audubon.
University of Nebraska Press, D. Patterson, Ed. 512pp.
Banfield, A. W. F. (1974) The mammals of Canada. University of Toronto
Press, Toronto, Canada. 438pp.
Barnes, T. L., R. M. Kubik, C. N. Cadaret, K. A. Beede, E. M. Merrick, S.
Chung, T. S. Schmidt, J. L. Petersen, and D. T. Yates. 2017. Identifying
hyperthermia in heat-stressed lambs and its effects on b
agonist-stimulated glucose oxidation in muscle. Proc. Amer. Soc.
Ainim. Sci. 68:25-29.
Bittner, T., King, R. & Kerfin, J. (2002) Effects of body size and melanism
on the thermal biology of garter snakes (Thamnophis sirtalis).
Copeia, 2,477-482.
Campbell, K. L. & Hochachka, P. W. (2000) Thermal biology and metabolism
of the American shrew-mole, Neurotrichus gibbsii. J.
Mammal., 82,578-585.
Caro, T. (2005) The adaptive significance of coloration in mammals.
Biosci., 55,125-136.
Clusella-Trullas, S., van Wyk, J. H. & Spotila, J. R. (2009) Thermal benefits
of melanism in cordylid lizards: a theoretical and field test.
Ecol., 90,2297-2312.
Cooper, C. E., Walsberg, G. E. & Withers, P. C. (2003) Biophysical properties
of the pelt of a diurnal marsupial, the numbat (Myrmecobius
fasciatus), and its role in thermoregulation. J. Exper. Biol.,
206,2771-2777.
Ellis, H. I. (1980) Metabolism and solar radiation in dark and white herons
in hot climates. Physiol. Zool., 53,358-372.
Foresman, A. (1995) Opposing fitness consequences of colour pattern
in male and female snakes. J. Evol. Biol., 8,53-70.
Fratto, M. & Davis, A. (2011) Do black-furred animals compensate for
high solar absorption with smaller hairs? A test with a polymorphic
squirrel species. Current Zool., 57,731-736.
Geen, M. R. S. & Johnston., G. R. (2014) Coloration affects heating and
cooling in three color morphs of the Australian bluetongue lizard,
Tiliqua scincoides. J. Thermal Biol., 43,54-60.
Geeslin, H. (1970) A radio-tracking study of home range, movements,
and habitat uses of the fox squirrel (Sciurus niger) in East Texas.
MSc. Thesis: Texas A & M University, College Station.
Gillooly, J. F., Brown,, J. H., West, G. B., Savage, V. M. & Charnov, E. L.
(2001) Effects of size and temperature on metabolic rate. Science,
293,2248-2251.
Grojean, R. E., Sousa, J. A. & Henry, M. C. (1980) Utilization of solar
radiation by polar animals: an optical model for pelts. Appl. Optics,
19,339-346.
Gustafson, E. J. & VanDruff, L. W. (1990) Behavior of black and grey
morphs of Sciurus carolinensis in an urban environment. Amer.
Mid. Nat., 123,186-192.
Hamilton, W. & Heppner, F. (1967) Radiant solar energy and the function
of black homeotherm pigmentation: an hypothesis. Science,
155,196-197.
Heppner, F. (1970) The metabolic significance of differential absorption
of radiant energy by black and white birds. Condor, 73,50-59.
Hubbard, J. K., Uy, J. A., Hauber, M. E., Hoekstra, H. E. & Safran, R. J.
(2010) Vertebrate pigmentation: from underlying genes to
adaptive function. Trend. Gen., 26,231-239.
Huggins, G., & Gee, K. (1995) Efficiency and selectivity of cage trap sets
for gray and fox squirrels. Wild. Soc. Bull., 23,204-207.
Ibanez, A., Pellitteri, D., Sacchi, R., Lopez, P. & Martin, J. (2016) Melaninbased
coloration covaries with hiding and exploratory behavior
in male Spanish terrapins. Ethol., 122,30-36.
Innes, S. & Lavigne, D. M. (1979) Comparative energetics of coat colour
polymorphs in the eastern grey squirrel, Sciurus carolinensis.
Can. J. Zool., 57,585-592.
Kawanishi, K., Sunquist, M. E., Eizirik, E., Lynam, A. J., Ngoprasert, D.,
Wan Shahruddin, W. N., Rayan, D. M., Sharma, D. S. K. & Steinmetz,
R. (2010) Near fixation of melanism in leopards of the Malay
peninsula. J. Zool., 282,201–206.
Keeler, C., Ridgway, S., Lipscomb, L. & Fromm, E. (1968) The genetics of
adrenal size and tameness in colorphase foxes. J. Hered., 59,82-
84.
Keeler, C., Mellinger, T., Fromm, E. & Wade, L. (1970) Melanin, adrenalin,
and the legacy of fear. J. Hered., 61,81-88.
Kiltie, R. (1989) Wildfire and the evolution of dorsal melanism in fox
squirrels, Sciurus niger. J. Mammal, 70,726-739.
Kiltie, R. (1992a) Comparisons among fox squirrels from the Mississippi
River Delta. J. Mammal., 73,906-913.
Kiltie, R. (1992b) Tests of hypotheses on predation as a factor maintaining
polymorphic melanism in coastal plain fox squirrels (Sciurus
niger L.). Biological J. Linn. Soc., 45,17-37.
Kingsley, E. P., Manceau, M., Wiley, C. D. & Hoekstra, H. E. (2009) Melanism
in Peromyscus is caused by independent mutations in
Agouti. PLoS One, 4:e6435.
Koprowski, J. (1994) Mammalian species Sciurus niger. Mammal Species
Account No. 479 9pp.
Linnen, C. R., Kingsley, E.P., Jensen, J. D. & Hoekstra, H. E. (2009) On the
origin and spread of an adaptive allele in deer mice. Science,
325,1095-1098.
Lueninghoener, E. (1973) An investigation of the melanistic phase of
the western fox squirrel (Sciurus niger rufiventer) in eastern Nebraska
and western Iowa. MSc. Thesis, University of Nebraska
at Omaha.
Luiselli, L. (1992) Reproductive success in melanistic adders: a new
hypothesis and some considerations on Andrѐn and Nilson’s
(1981) suggestions. Oikos, 64,60-604.
Lurz, P. W. W. & Lloyd, A. J. (2000) Body weights in grey and red squirrels:
do seasonal weight increases in conifer woodland? J. Zool.,
252,531-547.
McNab, B. K. (2002) The Physiological Ecology of Vertebrates. Cornell
University Press. 576pp.
McNab, B. K. (2012) Extreme Measures. Chicago: The University of Chicago
Press. 312pp.
McRobie, H., Thomas, A. & Kelly, J. (2009) The genetic basis of melanism
in the gray squirrel (Sciurus carolinensis). J. Hered.,
100,709-714.
McRobie, H. R., King, L. M., Fanutti, C., Coussons, P. J., Moncrief, N. D.
& Thomas, A. P. (2014) Melanocortin 1 receptor (MC1R) gene
sequence variation and melanism in the gray (Sciurus carolinensis),
fox (Sciurus niger), and red (Sciurus vulgaris) squirrel. J.
Hered., 105,423-428.
Nachman, M. W., H. E. Hoekstra & S. L. D’Agostino. (2003) The genetic
basis of adaptive melanism in pocket mice. Proceedings of the
National Academy of Sciences of the United States of America,
100,5268–5273.
Protas, M. E. & Patel, N. H. (2008) Evolution of coloration patterns. Ann.
Rev. Cell Develop. Biol., 24:425-446.
Robertson, G. I. (1973) Distribution of color morphs of Sciurus carolinensis
in eastern North America. MSc. Thesis, University of Western
Ontario. 78pp.
Rosenblum, E. (2005) The role of phenotypic plasticity in color variation
in Tularosa Basin lizards. Copeia, 2005,586-596.
SAS Institute, Inc. (2002) Statistical analysis system user’s guide: statistics,
version 8. SAS Institute Inc., Clay, North Carolina, USA.
Schneider, A., David, V. A., Johnson, W. E., O’Brien, S. J., Barsh, G. S.,
Menotti-Raymond, M. & Eizirik, E. (2012) How the leopard
hides its spots: ASIP mutations and melanism in wild cats. PloS
one, 7:e50386.
Schulte-Hostedde, A, Zinner, B., Millar, J. S. & Hickling, G. J. (2005) Restitution
of mass-size residuals: validating body condition indices.
Ecol., 86,155-163.
Sherbrooke W, Castrucci, A. & Hadley, M. (1994) Temperature effects
on in vitro skin darkening in the Mountain Spiny Lizard, Sceloporus
jarrovii: a thermoregulatory adaptation? Physiol. Zool.,
67,659-672.
Short, H. & Duke, W. (1971) Seasonal food consumption and body
weights of captive tree squirrels. J. Wild. Manage., 35,435-439.
Sikes, R., Gannon, W. & American Care and Use Committee of the
American Society of Mammalogists. (2011) Guidelines of the
American society of mammalogists for the use of wild mammals
in research. J. Mammal., 92,235-253.
Steele, M. A. & Koprowski, J. L. (2001) North American Tree Squirrels.
Smithsonian Institution Press. 201pp.
Tanaka, K. (2005) Thermal aspects of melanistic and striped morphs of
the snake Elaphe quadrivirgata. Zool. Sci., 22,1173-1179.
Walsberg, G. E., Campbell, G. S. & King, J. R. (1978) Animal coat color
and radiative heat gain: a re-evaluation. J. Comp. Physiol.,
126,211-22.
Walsberg, G. E. (1988) The significance of fur structure for solar heat
gain in the rock squirrel, Spermophilus variegatus. J. Exp. Biol.,
138,243-257.
Walsberg G. (1983) Coat color and solar heat gain in animals. BioSci.,
33,88-91.
Walsberg, G. E. (1990) Convergence of solar heat gain in two squirrel
species with contrasting coat colors. Physiol. Zool., 63,1025-
1042.
Walsberg, G. E. (1992) Quantifying radiative heat gain in animals. Am.
Zool., 32,217-224.
Walsberg, G. E. & Schmidt, C. A. (1989) Seasonal adjustment of solar
heat gain in a desert mammal by altering coat properties independently
of surface coloration. J. Exper. Biol., 142,387-400.
Walsberg, G. & Wolf, B. (1995) Effects of solar radiation and wind speed
on metabolic heat production by two mammals with contrasting
coat colours. J. Exper. Biol., 198,1499-1507.
Wauters, L. & Dhondt, A. (1989) Body weight, longevity and reproductive
success in red squirrels (Sciurus vulgaris). J. Anim. Ecol.,
58,637-651.
Wilson, J. (2013) Western expansion of melanistic fox squirrels (Sciurus
niger) in Omaha, Nebraska. Am. Mid. Nat., 170,393-401.
Wooden, K. M. & Walsberg, G. E. (2000) Effect of wind and solar radiation
on metabolic heat production in a small desert rodent,
Spermophilus tereticaudus. J. Exper. Biol., 203,879-888.
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How to Cite
Ciurej, A. K., Oblander, A., Swift, A. W., & Wilson, J. A. (2019). Melanism as a potential thermal benefit in eastern fox squirrels (Sciurus niger). European Journal of Ecology, 5(2), 79-87. https://doi.org/10.2478/eje-2019-0013
