Melanism of coyotes (Canis latrans) in Florida.
Coyotes (Canis latrans) are common throughout North America, with a notable range expansion over the past century into the eastern United States and Canada. However, coyotes, along with other medium sized Cams species have prehistorically and historically occupied, and been extirpated from, the southeastern U.S.A. (Berta, 2001; Nowak, 2002). The most recent expansion into, and throughout, Florida began around the 1950s and has expanded to include every Florida county (Brady and Campbell, 1983; Wooding and Hardisky, 1990; Maehr et al., 1996; Main et al., 1999; Main et al., 2000). The current range expansion is likely due to intermixed causes but is presumably aided by human-altered habitats (Paradiso, 1966; Richens and Hugie, 1974; Parker, 1995; Gompper, 2002) and a vacant niche left by the extirpation of the red wolf (C. rufus).
Melanism in canids occurs from a if-locus mutation ([K.sup.B]) (Anderson et al., 2009). One line of evidence suggests the mutation first appeared 12,000-120,000 y ago and subsequently disappeared in wild canids, but persisted in domestic dogs (C. lupus familiaris). Preservation of this gene in domestic dogs, and subsequent interspecific hybridization with wild canids (C. lupus, C. latrans), then dispersed this mutation throughout the genus in North America (Anderson et al, 2009). Another line of reasoning has suggested the mutation may have originated in eastern wolves (C. lycaan) instead of domestic dogs (Rutledge et al, 2009). Melanism has been common in C. rufus (Lowery, 1974; Whitaker and Hamilton, 1998) and therefore used as a distinguishing characteristic between C. rufus and C. latrans (Halloran, 1958; see Gipson, 1976), but recent genetic research has shown a close relationship between the two (vonHoldt et al, 2011). Futhermore, the occurrence of melanism in coyotes is not well understood throughout its range. It appears melanism is relatively rare in coyotes (Mowry and Edge, 2014), with one study documenting 5-9% occurrence in an eastern Canis population (Gipson, 1976).
Possible explanations for the maintenance of dark-coated polymorphs include camouflage (Caro, 2014), thermoregulation (Ducharme et al, 1989), and/or pleiotropy (Ducrest et al, 2008). Environment matching has been well documented in mammals (Ulmer, 1941; Anderson et al, 2009; McRobie et al, 2009). Melanism occurrence in Canis has been positively linked to habitat type (Jolicoeur, 1959; Dekker, 1998; Gipson et al, 2002; Anderson et al, 2009), likely for either protective concealment or predator concealment. Strong correlations have also been shown between fur color and substrate color in prey species (e.g., Dice, 1930; Blair, 1943; Majerus and Mundy, 2003). Deforestation, tree density, tree species, and fire have all been shown to affect pelage darkness in prey species (Creed and Sharp, 1958; Kiltie, 1989; Wauters et al, 2004). Polymorphism in coat color can result in individual heterogeneity in predation risk (Dice, 1947; Kaufman, 1974; Kiltie, 1989), and polymorphic maintenance can be a result of ephemeral habitats (e.g., fire-prone; Guthrie, 1967).
Melanism in mammals has also been linked to thermoregulation in species for which darker coloring might provide more effective temperature management. Thermoregulation as a consequence of coloration depends on a range of environmental and individual properties (Walsberg, 1983). Gloger's rule, that overall dark pelage is associated with tropical climates, holds true for many mammalian species, and thermoregulation may play a role in this phenomenon (Caro, 2005). Conversely, it has been proposed dark-colored polymorphs, which may have a thermoregulatory advantage in some instances, would increase in prevalence in northern latitudes. Melanistic squirrels are indeed more abundant in the northern extent of their ranges (Hancock and Nash, 1982) and are better adapted to cold temperatures because they dissipate less heat than lighter-colored individuals (Innes and Lavigne, 1979; Ducharme et al., 1989).
Herein we describe the occurrence and frequency of coyote melanism in Florida and investigate whether habitat or geographical patterns are present, as has been suggested for other taxa.
We collected 244 coyote carcasses during 2011-2014 throughout Florida. Most of the carcasses collected were trapped, hunter-killed, or hit by a car. Upon receipt carcasses were sexed, weighed, and necropsied. Pulp cavity-tooth width was used to determine age (Knowlton and Whittemore, 2001). Phenotypic expression of melanism was documented before necropsy, and melanistic individuals were photographed (Fig. 1).
We used generalized linear models implemented with the "glm" function in program R 3.0.0 (R Core Team, 2013) to evaluate rates of melanism. We treated Florida counties as our units of analysis, but Eglin Air Force Base was treated as a separate unit (Fig. 2) due to its classification as a contiguous trapping unit for the U.S. Department of Agriculture. We assumed a binomial distribution and fit models using a logit link. Flabitat covariates (e.g., mean and standard deviation of canopy cover) were calculated for each sampling unit using the National Land Cover Database (NLCD) 2001 tree canopy layer (http://www.mrlc.gov/nlcd2001.php). Geographic position covariates were calculated using the centroid of each county and calculating the northing, easting, and north-westing in meters from an Albers projection. We ranked models using Akaike's Information Criterion adjusted for sample size ([AIC.sub.c]; Akaike, 1973; Burnham and Anderson, 2002), and models with [[DELTA]AIC.sub.c] [less than or equal to] 2 were considered equally supported by the data (Burnham and Anderson, 1998). Models with pretending variables were removed from the candidate set (Anderson, 2008).
Of the 244 coyotes collected over 4 y, 18 (7.4%) were melanistic. All melanistic individuals exhibited a mostly black-dark grey coat, with a white pectoral spot and varying amounts of white fur on the feet (Fig. 1). Weights of melanistic individuals fell within the 95% confidence interval of individuals with typical coloration, respective of sex and age class. Melanistic coyotes were documented in the panhandle and northern peninsula of Florida (counties: Santa Rosa, Okaloosa, Gulf, Franklin, Bay, Levy, and Marion; Fig. 1). Correlation between mean canopy cover and all geographic covariates was at least 0.68. Our candidate model set suggested no competing models existed, and canopy cover best explained the variation in our data (Table 1). The incidence of melanism was positively related to mean canopy cover (Pcanopy mean = 0.11, se = 0.03, P < 0.001). Across the state rates of melanism varied considerably, from zero to more than 50% (Fig. 2), but predictive power varied with amount of canopy cover (Fig. 3).
The gene mutation that causes melanism in canids and its movement into wild canid populations has been identified (Anderson et al, 2009); however, the maintenance and potential benefits of melanism in canids, specifically coyotes, remains somewhat speculative and unknown. Data on melanism in canids from other states in limited, but our rate of melanism in Florida was similar to that reported by Gipson (1976) in Arkansas, although our observed occurrence and frequency of melanism varied spatially from locally abundant to absent. Mowry and Edge (2014) reported an apparent high regional presence of melanism in northeast Georgia, which likely mirrors our findings in areas of high canopy cover. Relatively high frequencies of melanism have been observed in red wolf populations (Sealander, 1956), which could point to past inter-breedings as the species ranges progressively overlapped, however recent genetic research has shown a close relationship between their lineages (vonHoldt et al, 2011). Melanistic individuals had a white pectoral spot similar to previous reports for melanistic coyotes and red wolves (Sealander, 1956; Gipson, 1976).
Florida's temperate climate would seemingly negate any thermogenic advantage of melanism, as has been suggested for smaller-bodied mammals (e.g., Innes and Lavigne, 1979; Ducharme et al, 1989). Gloger's rule, which asserts more heavily pigmented individuals are found at the more humid extents of their range (e.g., near the equator), also does not appear to hold true for coyotes in Florida. Although melanism is presumably present in southern portions of Florida and credible anecdotal sightings exist, our findings suggest the trait is exceedingly rare.
Canopy cover may promote melanism in coyotes through natural selection. Our findings, that frequency of coyote melanism increases with canopy cover, parallels findings for multiple species (e.g., Kiltie, 1989; Majerus and Mundy, 2003; Wauters et al., 2004), including other North American canids (e.g., Jolicoeur, 1958; Dekker, 1998; Gipson et al., 2002; Anderson et al., 2009). In North American gray wolves, for example, the frequency of melanism increases from open to forested habitats (Jolicoeur, 1959; Dekker, 1998; Gipson et al., 2002; Anderson et al., 2009); the inverse has been documented for white wolves (Jolicoeur, 1959; Gipson et al., 2002). Anderson et al. (2009) concluded the melanistic gene mutation has been under positive selective pressure in North American forest wolves. It is presumed a dark-colored coat provides concealment from prospective prey in forested habitats and vice versa. Higher rates of canopy cover typify the northern counties of Florida, where all our melanistic samples were obtained. However, in several well sampled counties with high canopy cover, melanism was not detected (Fig. 2), and confidence decreased at higher values of canopy cover (Fig. 3). Although the habitat mechanism by which polymorphism is maintained is clear for some species (e.g., Dice, 1930; Blair, 1943; Guthrie, 1967; Majerus and Mundy, 2003; Wauters et al., 2004), canopy cover does not appear to definitively explain the preservation of both phenotypes in coyotes.
The maintenance of polymorphism, if not thoroughly explained by habitat parameters, could suggest Kb plays a role in other traits as well. Furthermore, Coulson et al.'s (2011) model of wolf population features predicts black heterozygotes have higher annual survival, longer generation times, and greater lifetime reproductive success than either black homozygotes or normal-colored individuals. As both the homozygote and the heterozygote have black coats, camouflage or coat color alone cannot explain the polymorphism maintenance and other, less obvious functions, are likely involved. Coloration-based pleiotropic traits have been documented in other taxa (Ducrest et al., 2008) but are not well understood in mammals. Pleiotropy could influence the occurrence and frequency of melanism in coyotes, but further research is needed to elucidate gene dispersion across the landscape and disentangle pleiotropic effects.
Acknowledgments.--We thank Mike Milleson and the U.S. Department of Agriculture, Wildlife Services staff; Gator Howerton and Raymond McIntyre; Angeline Scotten and Florida Fish and Wildlife Conservation Commission staff for providing the majority of carcasses for this study. The Florida State Game Trust provided the funding for this research. Bobbi Carpenter provided invaluable technical assistance. We also thank Andrew Cox, Richard Kiltie, and anonymous reviewers for commentary on this manuscript.
Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle, p. 267-281. In: B. N. Petrov and B. F. Csaki (eds.). Second International Symposium on Information Theory. Akademiai Kiado, Budapest, Hungary.
Anderson, D. R. 2008. Model based inference in the life sciences: a primer on evidence. Springer, New York, New York.
Anderson, T. M., B. M. Vondholdlt, S. I. Candille, M. Musiani, C. Greco, D. R. Stahler, D. W. Smith, B. Padhukasahasram, E. Randi, J. A. Leonard, C. D. Bustamante, E. A. Ostrander, H. Tang, R. K. Wayne, and G. S. Barsh. 2009. Molecular and evolutionary history of melanism in North American gray wolves. Science, 323:1339-1343.
Berta, A. 2001. Mammalia 3: canivorans, p. 188-255. In: R. C. Hulbert Jr. (ed.). The fossil vertebrates of Florida. University Press of Florida, Gainesville, U.S.A.
Blair, W. F. 1943. Ecological distribution of mammals in the Tularosa Basin, New Mexico. Contrib. Lab. Vert. Biol. Univ. Michigan, 20:1-24.
Brady, J. R. and H. W. Campbell. 1998. Distribution of coyotes in Florida. Fla. Field Nat., 11:40-41.
Burnham, K. P. and D. R. Anderson. 1998. Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York, New York.
--and--. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York, New York.
Caro, T. 2005. The adaptive significance of coloration in mammals. BioScience, 55:125-136.
Coulson, T., D. R. MacNulty, D. R. Stahler, B. vonHoldt, R. K. Wayne, and D. W. Smith. 2011. Modeling effects of environmental change on wolf population dynamics, trait evolution, and life history. Science, 334:1275-1278.
Creed, W. A. and W. M. Sharp. 1958. Melanistic gray squirrels in Cameron County, Pennsylvania. J. Mammal., 39:532-537.
Dekker, D. 1998. Pack size and colour morphs of one wolf, Canis lupus, pack in Jasper National Park, Alberta, 1979-1998. Can. Field Nat., 112:709-710.
Dice, L. R. 1930. Mammal distribution in the Alamogordo region, New Mexico. Occas. Pap. Mus. Zool. Univ. Michigan, 213:1-32.
--. 1947. Effectiveness of selection by owls of deer mice (Peromyscus maniculatus) which contrast in color with their background. Contrib. Lab. Vert. Biol. Univ. Michigan, 34:1-20.
Ducharme, M. B., J. Larochelle, and D. Richard. 1989. Thermogenic capacity in gray and black morphs of the gray squirrel, Sciurus carolinensis. Physiol. Zool., 62:1273-1292.
Ducrest, A., L. Keller, and A. Roulin. 2008. Pleiotropy in the melanocortin system, coloration, and behavioural syndromes. Trend Ecol. Evol., 23:502-510.
Gipson, P. S. 1976. Canis in Arkansas. Southwest. Nat., 21:124-126.
--, E. E. Bangs, T. N. Bailey, D. K. Boyd, H. D. Cluff, D. W. Smith, and M. D. Jiminez. 2002. Color patterns among wolves in western North America. Wildl. Soc. Bull., 30:821-830.
Gompper, M. E. 2002. Top carnivores in the suburbs? Ecological and conservation issues raised by the colonization of north-eastern North American by coyotes. BioScience, 52:185-190.
Guthrie, R. D. 1967. Fire melanism of mammals. Am. Midi. Nat., 77:227-230.
Halloran, A. F. 1958. Black red wolves. Okla. Wildl., 14:6-8.
Hancock, D. C. and D. J. Nash. 1982. Dorsal hair length and coat color in Abert's squirrel (Sciurus aberti). West. N. Am. Naturalist, 42:297-298.
Innes, S. and D. M. Lavigne. 1979. Comparative energetics of coat colour polymorphs in the eastern grey squirrel, Sciurus carolinensis. Can J. Zool., 57:585-592.
Jolicoeur, P. 1959. Multivariate geographical variation in the wolf Canis lupus L. Evolution, 13:283-299. Kaufman, D. W. 1974. Adaptive coloration in Peromyscus polionotus. experimental selection by owls. J. Mammal., 55:271-283.
Kiltie, R. A. 1989. Wildfire and the evolution of dorsal melanism in fox squirrels, Sciurus niger. J. Mammal., 70:726-739.
Knowlton, F. F. and S. L. Whittemore. 2001. Pulp cavity-tooth width ratios from known-age and wild caught coyotes determined by radiography. Wildl. Soc. Bull., 29:239-244.
Lowery, G. H. 1974. The mammals of Louisiana and its adjacent waters. Louisiana State University Press, Baton Rouge, U.S.A.
Maehr, D. S., R. T. McBride, and I. I. Mullahey. 1996. Status of coyotes in south Florida. Fla. Field Nat., 24:101-107.
Main, M. B., S. F. Coates, and G. M. Allen. 2000. Coyote distribution in Florida extends southward. Fla. Field Nat, 28:201-203.
--, P. B. Walsh, K. M. Portier, and S. F. Coates. 1999. Monitoring the expanding range of coyotes in Florida: results of the 1997-98 statewide scent station surveys. Fla. Field Nat., 27:150-162.
Majerus, M. E. N. and N. I. Mundy. 2003. Mammalian melanism: natural selection in black and white. Trends Genet., 19:585-588.
McRobie, H., A. Thomas, and J. Kelly. 2009. The genetic basis of melanism in the gray squirrel (Sciurus carolinensis). J. Hered., 100:709-714.
Mowry, C. B. and J. L Edge. 2014. Melanistic coyotes in northwest Georgia. Southeast. Nat., 13:280-287. Nowak, R. M. 2002. The original status of wolves. Southeastern Nat., 1:95-130.
Paradiso, J. L. 1966. Recent records of coyotes, Canis latrans, from the southeastern United States. Southwest. Nat., 11:500-501.
Parker, G. 1995. Eastern coyote: the story of its success. Nimbus Publishing Limited, Halifax, Nova Scotia.
R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org/.
Richens, V. B. and R. D. Hugie. 1974. Distribution, taxonomic status, and characteristics of coyotes in Maine. J. Wildl. Manage., 38:447-454.
Rutledge, L. Y., P. J. Wilson, C. J. Kyle, T. J. Wheeldon, B. R. Patterson, and B. N. White. 2009. How the gray wolf got its color. Suence, 324:33-34.
Sealander, J. A. 1956. A provisional check-list and key to the mammals of Arkansas. Am. Midi. Nat., 56:257-296.
Ulmer, F. A. 1941. Melanism in Felidae, with special reference to genus Lynx. J. Mammal., 22:285-288.
vonHoldt, B. M., J. P. Pollinger, D. A. Earl, J. C. Knowles, A. R. Boyko, H. Parker, E. Geffen, M. Pilot, W. Jedrzejewski, B. Jedrzejewska, V. Sidorovich, C. Greco, E. Randi, M. Musiani, R. Kays, C. D. Bustamante, E. A. Osterander, J. Novembre, and R. K. Wayne. 2011. A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res., 21:1294-1305.
Walsberg, G. E. 1983. Coat color and solar heat gain in animals. BioScience, 33:88-91.
Wauters, L. A., M. Zamnetti, and G. Tosi. 2004. Is coat-colour polymorphism in Eurasian red squirrels (Sciurus vulgaris L.) adaptive? Mammalia, 68:37-48.
Whitaker, J. O. and W. J. Hamilton. 1998. Mammals of the eastern United States. Cornell University Press, Ithaca, New York.
Wooding, J. B. and T. S. Hardisky. 1990. Coyote distribution in Florida. Fla. Field Nat., 18:12-14.
GRETCHEN CAUDILL (1) and DANNY CAUDILL (2), Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, Gainesville 32601. Submitted 6 November 2014; Accepted 11 June 2015.
(1) Corresponding author: Telephone: (865) 216-9776; e-mail: email@example.com
(2) Present address: Alaska Department of Fish and Game, Fairbanks 99701
TABLE 1.--Candidate models evaluating the effects of habitat and geographic trends on rates of melanism in the coyote (Canis latrans) in Florida, U.S.A., 2011-2014. [AIC.sub.c], Akaike's Information Criterion, adjusted for sample size; [DELTA][AIC.sub.c], difference in [AIC.sub.c] values between each model and the best model; [[omega].sub.i], [AIC.sub.c] weight; model likelihood = [[omega].sub.i]/[[omega].sub.best model] K number of parameters. Models with pretending variables (Anderson, 2008) are indicated with-- Model [AIC.sub.c] [DELTA][AIC.sub.c] [Canopy.sub.mean] 48.01 0.00 [Canopy.sub.mean] + [Canopy.sub.std] 50.36 -- Northing 62.89 14.88 Easting 63.32 15.32 North-westing 65.14 17.13 Null 80.28 32.27 [Canopy.sub.std] 82.51 -- Model Model [[omega].sub.i] likelihood K Deviance [Canopy.sub.mean] 1.00 1.00 2 27.60 [Canopy.sub.mean] + [Canopy.sub.std] -- -- 3 27.52 Northing 0.00 1.00 2 42.48 Easting 0.00 1.00 2 42.91 North-westing 0.00 1.00 2 44.73 Null 0.00 1.00 1 62.14 [Canopy.sub.std] -- -- 2 62.11
|Printer friendly Cite/link Email Feedback|
|Title Annotation:||Notes and Discussion Piece|
|Author:||Caudill, Gretchen; Caudill, Danny|
|Publication:||The American Midland Naturalist|
|Date:||Oct 1, 2015|
|Previous Article:||Microcystin detected in little brown bats (Myotis lucifugus).|
|Next Article:||An unexpected journey: greater prairie-chicken travels nearly 4000 km after translocation to Iowa.|