Sampling of terrestrial salamanders reveals previously unreported atypical color morphs in the southern red-backed salamander Plethodon serratus.
There have been many reports in the literature of atypical color morphs in amphibians in the United States (see summaries in Gilboa and Dowling, 1974; Dyrkacz, 1981; Bechtel, 1995), including the eggs (Underhill, 1968), larvae (Bartley, 1959; Brandon and Rutherford, 1967; Mitchell and Church, 2002), and adults (Piatt, 1931; Seeliger, 1945; Thurow, 1955; Smith and Michener, 1962; Rubin, 1963; Houck, 1969; Lotter, 1977; Mitchell and Mazur, 1998; Jongsma, 2012) of salamanders. The terrestrial Eastern Red-backed Salamander, Plethodon cinereus, is included in the reports (Mitchell and Mazur, 1998; Sawyer and Novick, 2011) but not the closely related Southern Red-backed Salamander, Plethodon serratus. While much is known about the common, more widely distributed, and more widely studied P. cinereus, far less is known about the more geographically restricted P. serratus, including habitat use and the occurrence frequency and types of color morphs.
Four main color morphs have been described in the literature for P. cinereus (see Mitchell and Mazur, 1998): (1) the namesake red-backed phase in which the salamander exhibits a broad reddish to yellowish middorsal stripe, (2) the lead-backed phase wherein the aforementioned dorsal stripe is absent, (3) the erythristic phase wherein the salamander is uniformly red, lacking the lateral black pigment (Tilley et al., 1982), and (4) the leucistic phase wherein the skin coloration of the salamander appears milky. Two color morphs have been described for P. serratus (Petranka, 1998; Johnson, 2000; Trauth et al., 2004), the red-backed (striped) and lead-backed (unstriped) phases. Although reference is made to the existence of these color morphs in P. serratus (Johnson, 2000), the frequency of occurrence of the color morphs is lacking, in contrast to the extensive literature examining differences in the color phases among populations of P. cinereus.
In 2010 and 2011, we conducted 5 weekly rounds of leaf litter and natural cover object searches per season (Spring: Apr. and May, and Fall: Sept. and Oct.) in the Sinkin Experimental Forest, U.S. Department of Agriculture, Dent County, Missouri, U.S.A. (37[degrees]28'15.01"N, 91[degrees]15'58.52"W). A total of 800 individual plots (200 plots per season) were sampled, with half of the plots near ridge tops and half near the bottoms of slopes. The habitat was mature upland oak-pine-hickory forests in the Ozark Mountains. We conducted diurnal area-constrained searches of 3 x 3 m plots, each searched only once. We captured, identified, and measured (snout-vent length, SVL, mm) salamanders we encountered. We considered salamanders under 32 mm SVL to be juveniles (Herbeck and Semlitsch, 2000), and salamanders captured with a SVL above 33 mm, that did not exhibit the determining sexual characteristics, as unknown. We determined the sex of the individual when possible using presence of mental glands and evident nasolabial cirri in males and apparent eggs visible through the abdominal wall in females as determining characteristics. We released the salamanders back into the plots after data were collected. We also recorded the type of cover under which each salamander was found (leaf litter, rocks, or woody debris, including logs, bark, and sticks).
During these surveys, we found 1876 Plethodon serratus, 20 P. albagula, and four Eurycea longicauda melanopleura (Table 1). Of the 1876 P. serratus encountered, all but six exhibited the red-backed phase. Three of the non-red-backed phases were caught within a 24 h period in the fall of 2010, after heavy rains. Two lead-backed phases (35 mm SVL, 30 Sept. 2010, and 40 mm SVL, 6 May 2011), one silver-backed phase, with a light grey dorsal stripe (32 mm SVL, 29 Sept. 2010) and one ghost-backed phase, with a white dorsal stripe (39 mm SVL, 22 Sept. 2011), of P. serratus were found under leaf litter. Two hypomelanistic (leucistic), or milky, versions of the red-backed phase (32 mm SVL, 29 Sept. 2010 and 31 mm SVL, 24 May 2011) were found under rocks (Fig. 1). The large lead-backed P. serratus found on 6 May 2011 was a gravid female. The majority of salamanders (75%) were found in leaf litter, followed by under woody cover (14%) and rocks (11%). Two adults of P. serratus were encountered in burrows of cicadas (Drake et al., 2012).
Although reference guides have indicated that "specimens lacking the red dorsal stripe have been found in Missouri" (Johnson, 2000), and anecdotal comments suggest that they may be common in some areas of southern Missouri, we found only two P. serratus exhibiting the lead-backed phase during our surveys, representing an extremely small proportion of P. serratus encountered during these surveys (~0.1%). Herbeck and Semlitsch (2000) conducted the first in-depth studies on the natural history and ecology of P. serratus in Missouri but provided no data on color morphology. Frequency of occurrence of different color morphs varies throughout the range of a species. For example it is reported that throughout the range of P. cinereus, the lead-backed phase populations appear to be disjunct (Pfingsten and Walker, 1978) and the frequency of the occurrence of the lead-backed phase of P. cinereus ranges from 0%-93%, with 6 populations comprised of 70% lead-backed individuals (Pfingsten and Walker, 1978).
Polymorphism is the simultaneous occurrence of two or more phenotypes in a population. Mechanisms for the occurrence and maintenance of polymorphism in populations can be selective, nonselective, or a combination thereof. There are several hypotheses in the literature regarding the occurrence and maintenance of polymorphism in P. cinereus, including selection on physical and physiological characters, and genetic drift or mutation. Because P. cinereus and P. serratus are in the same species group and are highly related (Highton and Larson, 1979; Highton, 1995), and because they occupy similar habitats in their respective areas of distribution (Petranka, 1998), the patterns observed in these studies are likely to apply to P. serratus.
Differences in color morph frequencies of P. cinereus have been attributed to geographic differences; red-backed color morphs are associated with cooler microclimates, often at lower elevations, while unstriped or lead-backed color morphs are associated with warmer microclimates, often at higher elevations (Anthony et al., 2008; Lotter and Scott, 1977; Moreno, 1989). Investigations into the geographic influence on color morph frequencies have not been reported for P. serratus, but may reflect a pattern similar to P. cinereus and offer an additional explanation for the low frequency of lead-backed color morphs in our study area. Given the findings of Lotter and Scott (1977) and Moreno (1989), the timing of our surveys may have contributed to the composition of our color morph frequencies, as earlier retreat underground in colder climates has been reported for lead-backed phases of P. cinereus. Gibbs and Karraker (2006) suggested increase in frequency of the lead-backed color morph in P. cinereus was due to increase in temperatures as a result of global climate change and forest disturbance.
Behavioral differences between the red-backed and lead-backed phases of P. cinereus have been reported in several studies. Venesky and Anthony (2007) found that the lead-backed morphs were more active in the presence of a predator, suggesting that the two color morphs react differently to and may be differentially selected by potential predators. Moreno (1989) found greater frequencies of lead-backed salamanders at higher ground surface temperatures and suggested that this leads to greater exposure to temperature-dependent predators. Fitzpatrick et al. (2009) reported frequency-dependent selection by avian predators for the more common of the color morphs in P. cinereus, allowing for higher survival of rare forms (rare pattern advantage). In polymorphic populations of P. cinereus, Anthony et al. (2008) also reported that pairs of same-color morphs were encountered more frequently than pairs of different-color morphs, and that striped males were, on average, paired with larger females. Red-backed individuals had more diverse and profitable diets than lead-backed salamanders, which could explain their greater attractiveness to females (Anthony et al., 2008). If these patterns are true for P. serratus as well, they could help explain why the lead-backed phase was uncommon, as lead-backed males carrying the trait would be less likely to find mates. Several authors have suggested that physiological differences between color morphs due to temperature may contribute to persisting variation (Moreno, 1989; Petruzzi et al., 2006), but Petruzzi et al. (2006) caution that there is not a simple or consistent relationship between the polymorphism and thermal niche selection.
Highton (1959) reported a genetic basis for color polymorphism in P. cinereus and suggested multiple genes may interact to produce different color morphs (Highton, 1975). Given the close phylogeneficrelationship of P. serratus and P. cinereus, it is not unreasonable to assume that color polymorphism in P. serratus also has a genetic basis.
The purpose of the dorsal stripe of Plethodon serratus is undetermined. Camouflage could be one explanation, allowing the salamander to avoid detection while it is surface active by mimicking its surroundings--in many cases, leaf litter. One counterargument, however, is that there should not be a large visual predation selection pressure, given their fossorial and nocturnal habits (Sazima and Di Bernardo, 1991). As such, albinism or atypical, less cryptic color morphs may occur with more frequency in nocturnal or fossorial animals such as the red-backed salamanders that theoretically are less dependent on camouflage to survive. Another argument proposed for the occurrence and maintenance for polymorphism is apostatic selection, the primary hypothesis for color polymorphism maintenance in cryptic animals. This suggests that visual predators focus on more common color morphs of prey, resulting in higher survival of rare forms.
While the lead-backed phase of P. serratus was expected, the silver-backed, ghost-backed, and the hypomelanistic or leucistic phases were not. Reports of albinism and hypomelanism are not uncommon among salamander species, including P. cinereus (see Mitchell and Mazur, 1998), and can comprise a surprising portion of a population (Pfingsten and Walker, 1978). According to Petranka (1998), albinistic individuals comprise up to 9% of some populations of Desmognathus marmoratus, while Brandon and Rutherford (1967) reported 2-3% of larvae of Gyrinophilus in West Virginia exhibited albinism. Channell and Valentine (1972) reported one yellow albino Desmognathus fuscus out of 52 collected at a site in West Virginia. Many reports of albinism in salamanders are natural history notes of a single individual and do not include relative abundance of the anomaly in the population (Piatt, 1931; Seeliger, 1945; Thurow, 1955; Smith and Michener, 1962; Rubin, 1963; Houck, 1969; Lotter, 1977; Mitchell and Mazur, 1998).
While we detected three of the four color morphs reported for P. cinereus and added two color morphs to the list of variations for P. serratus, we did not detect any individuals exhibiting erythrism, which has not yet been reported in P. serratus. We were unable to find any reports for silver-backed morphs of either P. cinereus or P. serratus. Given the variation that occurs in populations of P. cinereus, we expect that additional surveys for P. serratus in other parts of their range will help determine whether color morph frequency varies between populations and habitats, and whether erythrism occurs in P. serratus.
Acknowledgments.--We thank Michael Osbourn, Brittany Ousterhout, Andy Senters, Grant Connette, and Katie LaJeunesse-Connette for their enthusiastic field assistance, and USDA Forest Service researchers Frank Thompson, John Kabrick, and Texas Nall for their support. Funding for this research was provided by the USDA Forest Service. We are grateful to Ray Semlitsch and two anonymous reviewers for comments that greatly improved this manuscript.
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DANA L. DRAKE (1) AND KATHERINE M. O'DONNELL, Division of Biological Science, University of Missouri, Columbia 65211. Submitted 20 January 2013; accepted 1 August 2013.
(1) Corresponding author: Drake.Dana.L@gmail.com
TABLE 1.-Terrestrial salamanders encountered during area- constrained leaf litter and cover object surveys conducted in South central Missouri in Apr.-May (Spring) and Sept.-Oct. (Fall) of 2010 and 2011. Snout-vent lengths (SVL, mm) are reported as means with one standard deviation in parentheses. Asterisks (*) indicate an unexpected color morph, (L) indicates a lead-backed color morph encountered during the surveys Species Spring 2010 Fall 2010 Sex Count SVL Count SVL P. serratus Female 79 39.3 (2.8) 1 37 Male 10 39.4 (2.4) 36 37.8 (2.7) Unknown adult 140 35.2 (2.4) 298**L 37.2 (3.4) juvenile 201 24.3 (3.2) 246 24.6 (5.5) Escaped 6 -- 1 -- Total 436 -- 582 -- P. albagula Adult 6 58.5 (9.4) 1 50 Juvenile 6 20.0 (1.6) 5 36.2 (3.4) Total 12 -- 6 -- E. longicauda melanopleura Adult -- -- 2 38 (0) Juvenile -- -- 2 26 (2.8) Total 0 -- 4 -- Species Spring 2011 Fall 2011 Sex Count SVL Count SVL P. serratus Female 160 L 38.3 (3.4) 18 41.6 (2.5) Male 24 39.5 (2.3) 38 39.8 (2.9) Unknown adult 196 * 35.1 (3.5) 159 * 37.7 (3.4) juvenile 160 26.0 (3.9) 96 26.1 (4.7) Escaped 1 -- 6 -- Total 541 -- 317 -- P. albagula Adult 1 54 -- -- Juvenile 1 24 -- -- Total 2 -- 0 -- E. longicauda melanopleura Adult -- -- -- -- Juvenile -- -- -- -- Total 0 -- 0 --
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|Title Annotation:||Notes and Discussion|
|Author:||Drake, Dana L.; O'Donnell, Katherine M.|
|Publication:||The American Midland Naturalist|
|Date:||Jan 1, 2014|
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