Journal of Herpetology, Vol. 41, No. 3, pp. 401–409, 2007 Copyright 2007 Society for the Study of Amphibians and Reptiles
Comparative Life Histories of Two Sympatric Ambystoma Species at a Breeding Pond in Massachusetts1 REBECCA N. HOMAN,2,3 BRYAN S. WINDMILLER,4
AND
J. MICHAEL REED2
2
4
Department of Biology, Tufts University, Medford, Massachusetts 02155, USA Hyla Ecological Services, 336 Baker Avenue, Concord, Massachusetts 01742, USA
ABSTRACT.—Spotted Salamanders (Ambystoma maculatum) and members of the Blue-Spotted Salamander complex (Ambystoma laterale-jeffersonianum complex) often share terrestrial and wetland habitats, allowing controlled comparison of their life-history strategies. We examined population sizes, sex ratios, breeding frequencies, recruitment rates, and age structures, in sympatric populations of Spotted Salamanders and members of the Blue-Spotted Salamander complex across five years. We saw declines in breeding population size that were larger for Blue-Spotted Salamanders than for Spotted Salamanders (55.2% vs. 33.3%), although members of the Blue-Spotted Salamander complex consistently had larger breeding populations. However, members of the Blue-Spotted Salamander complex also had more highly skewed sex ratios than did Spotted Salamanders (female : male, mean , 23:1 vs. 0.8:1), greater intervals between breeding, lower recruitment (0.9 vs. 5.7 juveniles/female/year), and a younger average age (3.7 vs. 5.2 years). In addition, the sex ratio of BlueSpotted Salamanders became more skewed over time, with a dramatic reduction in the number of males. Much of our demographic data at this site suggest that the lower reproductive success of Blue-Spotted Salamanders may reduce the relative likelihood of their persistence compared to Spotted Salamanders. However, yearly breeding population sizes, reproductive ages, and lack of juvenile demographic data imply that more study is needed to understand the relative likelihood of persistence for these two groups of pondbreeding amphibians.
Amphibian declines and extinctions are occurring worldwide (reviewed by Blaustein and Wake, 1990; Wyman, 1990; Bury, 1999). Although distinguishing between declines and natural population fluctuations without longterm studies may be difficult (e.g., Pechmann et al., 1991; Reed and Blaustein, 1995), the mechanisms contributing to some particular species’ declines have been identified. Mechanisms include introduced species (Gamradt and Kats, 1996), increased UV-B radiation (Blaustein et al., 1994), pathogen outbreaks (Kiesecker et al., 2001), and pollution (Hopkins et al., 1997). Possibly the most prevalent mechanism, however, is habitat fragmentation (deMaynadier and Hunter, 1998, 1999; Clark et al., in press) and loss (Wyman, 1990; Blaustein et al., 1994; Pounds et al., 1999; Homan et al., 2004). Habitat loss may be a particularly important concern for amphibian species that use both aquatic and terrestrial habitats during their life cycle because it can impact both habitats (Duellman and Trueb, 1986; Windmiller, 1996; Petranka, 1998). Mole Salamanders (Ambystoma spp.), for example, spend the majority of their time in 1 Howard Whiteman served as editor for this manuscript. 3 Corresponding Author. Present address: Department of Biology, Denison University, Granville, Ohio 43023, USA; E-mail:
[email protected]
terrestrial habitats surrounding breeding wetlands. Although partial habitat loss can cause population declines, the details of how active habitat loss affects demographic traits are poorly studied. In addition, a population’s capacity to recover from a sudden decline, regardless of its cause, is affected in part by demographic traits such as age structure, sex ratio, and breeding frequency. We studied demographic characteristics of two sympatric Ambystoma species, Spotted Salamanders (Ambystoma maculatum) and members of a Blue-Spotted Salamander (Ambystoma laterale-jeffersonianum) complex. These species spend more than 11 months of the year in upland forest habitat surrounding their breeding ponds, to which they show high fidelity (Downs, 1989a,b; Windmiller, 1996; Regosin et al., 2005). Spotted Salamander demography and ecology are fairly well studied, including research on time intervals between breeding, fecundity, recruitment, age structure, survivorship, and habitat requirements and patterns of use (e.g., Husting, 1965; Flageole and Leclair, 1992; Blackwell et al., 2004; Porej et al., 2004). The Blue-Spotted Salamander complex is more poorly studied (e.g., Clanton, 1934; Uzzell, 1964; Wilbur, 1971, 1977), with most research focusing on reproduction (Bogart and Licht, 1986; Lowcock et al., 1991; Lowcock, 1994). As commonly occurs with Blue-Spotted Salamanders, our study population coexisted with primarily
402
R. N. HOMAN ET AL.
TABLE 1. Recaptures of animals PIT tagged in the years 1998–2000. The year 2001 was the last possible year of capture for these individuals. Numbers in parentheses represent percentages of animals tagged in 1998, 1999, or 2000 that were recaptured in that later year. Number PIT tagged
Spotted Salamander Male Female Male Female Male Female Blue-Spotted Salamander complex Male Female Male Female Male Female
1998 65 26 1999 38 17 2000 8 16
Year of recapture
1999
2000
2001
never
24 (36.9%) 10 (38.5%)
16 (24.6%) 4 (15.4%)
11 (16.9%) 2 (7.7%)
40 (61.5%) 16 (61.5%)
21 (55.3%) 9 (52.9%)
14 (36.8%) 3 (17.6%)
16 (42.1%) 8 (47.1%)
3 (37.5%) 8 (50.0%)
5 (62.5%) 8 (50.0%)
2 (13.3%) 47 (22.1%)
0 (0%) 25 (11.7%)
13 (86.7%) 139 (65.3%)
1 (50.0%) 35 (46.7%)
0 (0%) 23 (30.7%)
1 (50.0%) 40 (53.3%)
1 (100%) 29 (37.7%)
0 (0%) 48 (62.3%)
1998 15 213 1999 2 75 2000 1 77
2 (13.3%) 55 (25.8%)
female polyploid biotypes (LLJ and LLLJ), which are thought to be ancient hybrids of Blue-Spotted Salamanders and Jefferson Salamanders (Ambystoma jeffersonianum) (Uzzell and Goldblatt, 1967; Spolsky et al., 1992a). Consequently, throughout this manuscript, we refer to this mixed population of true Blue-Spotted Salamanders and hybrids as a Blue-Spotted Salamander complex. As we will show, reproduction, population dynamics, and apparent population resistance to extirpation can be affected by the mixture of this complex. The polyploids are usually female; therefore, the sex ratio in mixed populations can be highly skewed (Macgregor and Uzzell, 1964; Wilbur, 1971; Bogart and Licht, 1986). In addition, polyploid unisexuals commonly have lower fecundity and larval survivorship relative to their diploid relatives (Wilbur, 1971; Lowcock, 1994). Our study populations lived in a forest fragment within a suburban landscape. Our goal was to assess and compare life-history traits of two sympatric populations of Ambystoma through a five-year study. To this end, for both species across years, we measured or estimated population size, sex ratios, ploidy (for the Blue-Spotted Salamander complex), recapture rates, intervals between breeding, recruitment rate, and age structure. MATERIALS AND METHODS Our study was conducted at a previously unstudied vernal pool and its surrounding
forest habitat in Sudbury, Massachusetts, U.S.A. (42u229N, W71u259W) from 1997 through 2001. The breeding pond, with a surface area of approximately 0.38 ha, was encircled by drift fence, with pitfall traps (paired 19-liter buckets) spaced every 15 m (Regosin et al., 2005; Windmiller et al., in press). The distance between the drift fence and the pond edge ranged from approximately 228 m. Animals were captured primarily during rainy spring nights, either moving toward the pond (prebreeding) or away from the pond (postbreeding). The morning following capture, unmarked animals were toeclipped with either individual or capture-year patterns, and previously captured individuals were identified. For each individual, we identified sex and measured mass to the nearest 0.1 g and snout–vent length (SVL) to the nearest 0.1 mm. Animals then were moved to the opposite side of the fence from which they were captured. In each of the years 1998–2000, a subset of Spotted Salamanders (total N 5 171, Table 1) and Blue-Spotted Salamanders (total N 5 485, Table 1) leaving the pond were taken into a lab at Tufts University and implanted with passive integrated transponder (PIT) tags (Biomark, Boise, ID). For implanting, we anesthetized animals using a solution of Tricaine methane sulfonate (MS-222, Western Chemical, Ferndale, WA) (1.5 g/L for Blue-Spotted Salamanders and 2.5 g/L for Spotted Salamanders, buffered to a pH of 7). PIT tags were implanted, using a 12-gauge needle, between the skin and
COMPARATIVE LIFE HISTORIES OF TWO AMBYSTOMA peritoneum in the side of the body just below the forelimb. Salamanders recovered from anesthesia within 20 min, although we monitored them overnight and released them the following day on the opposite side of the fence from the point of capture. Population Size and Sex Ratio.—For each year, we estimated population size and sex ratio by totaling the numbers of males and females of each species captured entering the pond. To determine whether there were significant changes in breeding population size and sex ratios over time, simple linear regressions were run for breeding population size or sex ratio and time for each species. Population sizes are also reported as part of a related study that compared our study site to a more disturbed site (Windmiller et al., in press). Ploidy.—During the PIT tagging process in 1998 and 1999, we took blood samples from 121 female Blue-Spotted Salamanders to determine ploidy. While each animal was anethesthetized for PIT tagging, a single toe was clipped for aging (see below). Toe removal resulted in a small amount of bleeding, and for members of the Blue-Spotted Salamander complex, we dabbed a small amount of blood on a slide. A drop of amphibian saline was added to the slide to keep the blood isotonic. The slide then was refrigerated for not more than 3 h, at which time photographs of erythrocytes were taken at 203 magnification. Long and short axes of erythrocytes were measured from the photographs and cell area was calculated using the formula for an ellipse. An individual’s average erythrocyte area was calculated from six to 12 erythrocytes depending on the number of isotonic cells present in the sample. Based on previous studies, individuals with mean erythrocyte areas of , 873 m2 were designated diploid; mean area . 991 m2 were designated polyploid (Downs, 1978; Macgregor and Uzzell, 1964; Austin and Bogart, 1982). Recapture Rates.—Using captures of PITtagged animals, we determined the percentage of animals PIT tagged in 1998 that were first recaptured in 1999, 2000, or 2001 or that were never recaptured and the percentage of all recaptures that occurred within one, two, or three years of the previous capture. In addition, we used a chi-square goodness-of-fit test to look for differences in breeding frequency among the two species. Recruitment Rates.—We monitored drift fences during summer and early fall to capture metamorphosed juveniles of each species emerging from the breeding pond. Recruitment rate was estimated from 1997–2001 as the number of juveniles emerging from the pond divided by the number of adult females entering the pond
403
the previous spring. To look for differences in mean recruitment over time for the two species, we conducted a Student’s t-test. Age Structure.—Each PIT-tagged animal was toe clipped, and toes were preserved in 10% formalin for a few months to three years. Subsequently, we rinsed toe bones in distilled water, allowed them to dry, and sent them to Matson’s Laboratory (Milltown, Montana) for sectioning. For each toe bone, eight crosssections (10 m thick) were made at 0.2-mm intervals and then stained with hematoxylin. After receiving the sections, we photographed and analyzed the clearest of an individual’s eight sections. Ambystoma in our region have a cyclic activity pattern, in which they are active during spring through fall and dormant during winter (Downs, 1989a,b; Windmiller, 1996). This activity pattern results in uneven bone growth that can be seen in long bone growth (Flageole and Leclair, 1992; Castenet et al., 1993; Homan et al., 2003). We treated one line of arrested growth (LAG) as one period of slow winter growth associated with dormancy and, so, was equivalent to one year. The line of metamorphosis was identified as the innermost LAG, was generally irregular in shape, and had differently stained bone inside than outside. We counted only postmetamorphic LAGs, those outside the line of metamorphosis, to estimate age in years (Flageole and Leclair, 1992; Russell et al., 1996; Homan et al., 2003). We did not count potential LAGs that were very lightly stained relative to the clearest LAGs or that could not be followed around the circumference of the bone (Russell et al., 1996). We assumed that the final LAG was either very close to, or at the edge of, the bone section, because phalanges were excised from the animals within 1–2 months following the end of winter hibernation. Age of each individual was estimated independently by two of us. We recorded the best estimate of the number of LAGs, as well as the minimum and maximum possible number of LAGs. We also assigned a confidence level, ranging from most confident (5 1) to least confident (5 3), to each age assignment. When our independent best age estimates differed by more than one year, or either of us gave a confidence level of 3, we did not include that individual in analyses. When our best estimates differed by one year, we reexamined the bone section together and attempted to agree on an age estimate (cf. Wake and Castenet, 1995). If we could not agree, that individual was removed from analyses. Once estimated ages were complete, we used ANOVAs to test for differences in average age of salamanders across years, species, and sexes.
404
R. N. HOMAN ET AL.
FIG. 1. (A) Breeding population sizes and (B) sex ratios (female: male) for the Blue-Spotted Salamander complex (closed circles) and Spotted Salamanders (open circles) across five years at a breeding pond in suburban Massachusetts. Breeding population sizes and sex ratios are estimated based on the number and sex of individuals captured entering the breeding pond.
RESULTS Population Size.—Members of the Blue-Spotted Salamander complex outnumbered Spotted Salamanders every year, and changes in population size occurred in a similar pattern across years for both species (Fig. 1A). Both species had their maximum breeding population sizes in 1997 (839 and 300, respectively) and were at their lowest in 2001 (376 and 200, respectively, Fig. 1A). The Blue-Spotted Salamander complex breeding population declined by 55.2% over the five-year study (linear regression, F1,3 5 66.8, r2 5 0.96, P 5 0.004), whereas Spotted Salamanders declined by 33.3% (linear regression, F1,3 5 29.0, r2 5 0.91, P 5 0.0125). Sex Ratio.—The Blue-Spotted Salamander complex sex ratios were consistently female biased, and the bias increased across the study period from 10.1 females per male to 37.1 females per male (linear regression, F1,3 5 31.0, r2 5 0.91, P 5 0.011, Fig. 1B). Spotted Salamanders, by contrast, had male biased sex ratios from 1997 through 1999 and female biased sex ratios in 2000 and 2001, increasing
over the entire study period from 0.6 females per male to 1.1 females per male (linear regression, F1,3 5 13.4, r2 5 0.82, P 5 0.035, Fig. 1B). The increase in female bias for both species appears to be driven by a decrease in males rather than by an increase in females. Male Blue-Spotted Salamanders decreased by 86.5%, and male Spotted Salamanders decreased by 49.5%, whereas females decreased by 52.1%, and 6.3%, respectively. Ploidy.—Mean erythrocyte area (6 SE) for the 121 females in the Blue-Spotted Salamander complex ranged from 661 6 28.8 m2 to 1714 6 74.6 m2. We classified approximately 14% (N 5 17) of the animals as diploid and 75% (N 5 91) as polyploid. The remaining 11% (N 5 13) of the animals had mean erythrocyte areas between 873 m2 and 991 m2; thus, they could not be classified with confidence. Recapture Rates.—Of the 170 Spotted Salamanders PIT tagged in this study, 44.1% (N 5 75) were recaptured the year following release, and 45.3% (N 5 77) were captured in at least one subsequent year. Of the 55 individuals that had only two years of recapture possibilities, one (1.8%) was captured for the first time two years after capture; of the 91 animals that had three years of recapture possibilities, none was captured for the first time three years after capture (Table 1). Of the 383 members of the Blue-Spotted Salamander complex PIT-tagged, 32.1% (N 5 123) were recaptured the year following release, and 37.1% (N 5 142) were captured in at least one subsequent year. Of the 77 individuals that had only two years of recapture possibilities, none was captured for the first time two years after initial capture; of the 228 animals that had three years of recapture possibilities, one (0.4%) was captured for the first time three years after initial capture (Table 1). Most recaptures (. 82%) occurred in the year immediately following the previous capture, regardless of species or sex (Table 2). Among recaptured animals, breeding Spotted Salamanders skipped years less often than did members of the Blue-Spotted Salamander complex (x21 5 7.56, P , 0.01, Table 2). Recruitment Rate.—From 1997 through 2001, females in the Blue-Spotted Salamander complex produced significantly fewer emerging juveniles than did female Spotted Salamanders, with means (6 SE) of 0.9 6 0.22 juveniles/ female and 5.7 6 1.07 juveniles/female, respectively (Student’s t-test, t8 5 5.07, P 5 0.001, Fig. 2). Age Structure.—Breeding females in the BlueSpotted Salamander complex that were aged from toe clips ranged from two to eight years, and from two to six years for males, with means (6 SE) of 3.81 6 0.10 (N 5 132) and 3.16 6 0.23
COMPARATIVE LIFE HISTORIES OF TWO AMBYSTOMA
405
TABLE 2. Recaptures made 1, 2, or 3 years after the previous capture. No data are included for animals PIT tagged in 2000, because 100% of recaptures would necessarily have been one year following the previous capture. # of recaptures for animals PIT tagged in
Spotted Salamander Male Female Male Female Blue-Spotted Salamander complex Male Female Male Female
1998 51 16 1999 35 12 1998 4 127 1999 1 58
(N 5 18), respectively (Fig. 3). Spotted Salamander ages ranged from two to 10 years for females and two to 13 years for males, with a mean age (6 SE) of 5.75 6 0.43 (N 5 24) and 5.04 6 0.28 (N 5 72), respectively (Fig. 3). We found no significant difference in average age of individuals PIT tagged in 1998 and 1999 (ANOVA, F1,238 5 0.099, P 5 0.754); thus, years were combined for analysis. However, salamander age depended significantly on both species and sex. The average age of the Spotted Salamander breeding population (mean 6 SE: 5.22 6 0.24 years), was significantly older than for the Blue-Spotted Salamander breeding population (3.73 6 0.10 years; F1,242 5 41.658, P , 0.001). Additionally, females of both species were significantly older than males (F1,242 5 5.236, P 5 0.023), and there was no significant
FIG. 2. Recruitment rates for the Blue-Spotted Salamander complex (closed circles) and Spotted Salamanders (open circles) over the years 1997 through 2001 at a suburban breeding pond in eastern Massachusetts.
# of years skipped between capture
1
2
3
50 (98.0%) 15 (93.8%)
1 (2.0%) 1 (6.2%)
0 (0%) 0 (0%)
34 (97.1%) 12 (100%)
1 (2.9%) 0 (0%)
4 (100%) 104 (81.9%)
0 (0%) 22 (17.3%)
1 (100%) 58 (100%)
0 (0%) 1 (0.8%)
0 (0%) 0 (0%)
interaction between species and sex (F1,242 5 0.012, P 5 0.913). DISCUSSION At our study area, population sizes were consistently higher for members of the Blue-
FIG. 3. Age distributions of (A) the Blue-spotted Salamander complex and (B) Spotted Salamanders in the combined years 1998 and 1999. Sample sizes are given in parentheses.
406
R. N. HOMAN ET AL.
Spotted Salamander complex than for Spotted Salamanders. Although sex ratios of our Spotted Salamander population generally fell within previous estimates from other sites (Husting, 1965; Downs, 1989b), sex ratios and ploidy estimates of the Blue-Spotted Salamander complex may offer some insight into their decline at this site. We found a strong female bias among the Blue-Spotted Salamander complex partly because of the presence of polyploid hybrids in this population, which are almost always female (Uzzell, 1964; Wilbur, 1971; Downs, 1978; Lowcock, 1994). The degree of bias increased over the study period, and the change might have been exacerbated by a selective decline of diploids rather than polyploids, as evidenced by the greater decline in presumably diploid males than females. The relatively large decline in Blue-Spotted Salamander males relative to females suggests that overall population decline was more rapid for diploids than for polyploids at this site. If a resource manager were monitoring a population by simply counting individuals, the full significance of the decline would be missed. A rapid decline of males, which are needed for both diploid and polyploid female reproduction, could eventually result in a sudden decline in this species complex years after the event that caused the initial decline in males. Polyploid members of the Blue-Spotted Salamander complex need to take up a male’s spermatophore to produce viable eggs, even though the sperm is not incorporated into the egg (Macgregor and Uzzell, 1964; Spolsky et al., 1992b). If diploid males disappear, polyploid females would need to use a spermatophore from a more distantly related species or fail to breed. To our knowledge, there is no evidence for polyploid salamanders in the Blue-Spotted Salamander complex using the spermatophores of Spotted Salamanders, the only congener at this breeding site. Our observed disproportionate decline of diploids was unexpected because studies have identified several life-history traits of polyploid unisexuals, including lower fecundity, higher embryonic and larval mortality, and delayed sexual maturity, that favor persistence of diploid bisexuals (reviewed by Lowcock, 1994). Individuals of both species breed annually, with Spotted Salamanders apparently skipping years between breeding less frequently than did members of the Blue-Spotted Salamander complex. This difference, however, may be partly an artifact caused by differential trespass rates among these species; trespass refers to individuals crossing the drift fencing that is intended to guide animals to the pit traps. In a related study (unpubl. data), we found that members of the
Blue-Spotted Salamander complex had greater trespass rates than did Spotted Salamanders, suggesting that the difference between species in skipping breeding years may be less than we recorded. We do note, however, that animals were captured both coming to the breeding pond and when leaving it such that an individual would have to trespass in both directions to avoid detection. Recruitment rates also differed between species at this pond. Spotted Salamander recruitment rates were lower than for the Blue-Spotted Salamander complex, but values fell within ranges reported in other studies (Shoop, 1974; Stenhouse, 1987; Windmiller, 1996; Paton et al., 2000). During our five-year study, members of the Blue-Spotted Salamander complex did not replace themselves, contributing to the observed population decline. Given the relatively high proportion of polyploid hybrids in this population, the low recruitment may be a result of polyploid hybrids producing fewer eggs per clutch and experiencing lower larval survivorship relative to diploids (reviewed by Lowcock, 1994). In addition, we observed female BlueSpotted Salamanders leaving the breeding pond with eggs not laid, which has been reported for other populations (Clanton 1934). Therefore, in addition to reduced fecundity and larval survivorship, polyploid females may have had trouble finding males, perhaps because the males have relatively low frequency in the population or males discriminate against polyploid unisexuals (Uzzell, 1964; Uzzell and Goldblatt, 1967). We hypothesize that pure Blue-Spotted Salamander populations would show higher recruitment rates than those we observed among a mixed-ploidy population. The final demographic variable measured here, age structure, also showed interesting differences between these two Ambystoma species. First, the higher average age of Spotted Salamanders relative to the Blue-Spotted Salamander complex suggests higher adult mortality for the latter and a greater breeding longevity for the former. Second, females of the Blue-Spotted Salamander complex may be maturing at an earlier age than Spotted Salamander females, resulting in a greater population growth potential. This difference, however, was not shown in males; therefore, it might be driven by polyploid hybrids. We set out to understand the comparative demographic traits of sympatric Ambystoma congeners. Based on our work, breeding populations of Spotted Salamanders and the BlueSpotted Salamander complex demonstrated some similarities and some important differences in their life-history patterns that might influence their relative likelihoods of persis-
COMPARATIVE LIFE HISTORIES OF TWO AMBYSTOMA tence. For example, greater average and maximum age and higher recruitment rate of Spotted Salamanders relative to the sympatric members of the Blue-Spotted Salamander complex suggest that Spotted Salamanders ought to have a demographic advantage. However, at this pond during this five-year window, members of the Blue-Spotted Salamander complex were abundant and coexisting with their congeners. The long-term coexistence of these populations would be predicted if the members of the BlueSpotted Salamander complex, particularly the unisexual hybrids that make up the majority of this population, matured early, and reproduced often as evolutionary strategies to counter the demographic advantages of the Spotted Salamanders. Although the relative age structures at our pond suggest the possibility of relative early maturity in females of the Blue-Spotted Salamander complex, we suggest that more years of age data at more ponds are needed to draw a conclusion. In addition, we have no evidence to suggest that the members of the Blue-Spotted Salamander complex at our pond are breeding more frequently than the Spotted Salamanders; in fact, our statistical analyses suggest the opposite. Based on growth potential of these two populations at this pond, we hypothesize that members of the Blue-Spotted Salamander complex may be less likely to persist than their Spotted Salamander congeners. However, factors other than reproductive rate might influence population size and, therefore, the likelihood of persistence. For example, BlueSpotted Salamanders are more tolerant of forest edge habitat or poorly drained soils than Spotted Salamanders, which may increase the niche for the former (Minton, 1972; Weller et al., 1978; Downs, 1989a; Ball, 2000). There also is evidence that adult Spotted Salamander population size could be limited by terrestrial burrows during the nonbreeding season (Madison, 1997; Regosin et al., 2003a,b; Cooperman et al., 2004) or by females during mating (cf. Houck et al. 1996). Similar studies have not been done on Blue-Spotted Salamanders. Survival and dispersal differences among these species during the juvenile life stage may be another factor that influences persistence. Juveniles tend to hold territories that are of lower quality than adult territories (Windmiller, 1996). Therefore, if breadth of habitat tolerance for juveniles is similar to that of adults for these species (Minton, 1972; Weller et al., 1978; Downs, 1989a; Ball, 2000), then BlueSpotted Salamander juveniles may be better able to persist than Spotted Salamander juveniles when space is limiting, contributing to larger adult Blue-Spotted Salamander popula-
407
tion sizes. In addition, the juvenile life stage is largely responsible for dispersal to new habitats; therefore the adult population sizes ought to depend, in part, on the relative emigration and immigration rates of these species. We suggest that more information on the dispersal behavior and survival of juvenile Ambystoma is critical to predicting population persistence. Acknowledgments.—We thank P. Paton for his thoughtful comments on this work and J. Regosin, K. Abell, E. Cavallerano, A. Cohan, J. Fahey, A. Kennedy, J. Lisk, J. Monchamp, J. O’Brien, J. Rogers, M. Russ, C. Walker, and K. Winchell for help in field work. Animal handling methods were approved by the Tufts University Animal Care and Use Committee. Funding for this study was provided by Massachusetts Environmental Trust, Massachusetts Natural Heritage and Endangered Species Program, and Tufts Institute for the Environment. We also thank the Sudbury Conservation Commission for allowing us access to this site. LITERATURE CITED AUSTIN, N. E., AND J. P. BOGART. 1982. Erythrocyte area and ploidy determination in the salamanders of the Ambystoma jeffersonianum complex. Copeia 1982:485–488. BALL, J. C. 2000. A winter/spring study of salamanders in a disturbed, fragmented habitat surrounded by farm land. Journal of the Iowa Academy of Sciences 107:175–181. BLACKWELL, E. A., G. R. CLINE, AND K. R. MARION. 2004. Annual variation in population estimators for a southern population of Ambystoma maculatum. Herpetologica 60:304–311. BLAUSTEIN, A. R., AND D. B. WAKE. 1990. Declining amphibian populations: a global phenomenon? Trends in Ecology and Evolution 5:203–204. BLAUSTEIN, A. R., P. D. HOFFMAN, D. G. HOKIT, J. M. KIESECKER, S. C. WALLS, AND J. B. HAYS. 1994. UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines? Proceedings of the National Academy of Sciences 91:1791–1795. BOGART, J. P., AND L. E. LICHT. 1986. Reproduction and the origin of polyploids in hybrid salamanders of the genus Ambystoma. Canadian Journal of Genetic Cytology 28:605–617. BURY, R. B. 1999. A historical perspective and critique of the declining amphibian crisis. Wildlife Society Bulletin 27:1064–1068. CASTENET, J., H. FRANCILLON-VIEILLOT, F. J. MEUNIER, AND A. DERICQLE`S. 1993. Bone and individual aging. In B. K. Hall (ed.), Bone, Volume 7, pp. 245–283. CRC Press, Boca Raton, FL. CLANTON, W. 1934. An unusual situation in the salamander Ambystoma jeffersonianum (Green). Occasional Papers of the Museum of Zoology of the University of Michigan 290:1–14. CLARK, P. J., J. M. REED, B. S. WINDMILLER, AND J. V. REGOSIN. In press. Comparing urbanization indices and their effects on spotted salamander (Amby-
408
R. N. HOMAN ET AL.
stoma maculatum) and wood frog (Rana sylvatica) presence and abundance. In Urban Herpetology. Herpetological Conservation, Volume 3. Society for the Study of Amphibians and Reptiles, Salt Lake City, UT. COOPERMAN, M. D., J. M. REED, AND L. M. ROMERO. 2004. The effects of terrestrial and breeding densities on corticosterone and testosterone levels in Spotted Salamanders, Ambystoma maculatum. Canadian Journal of Zoology 82:1795–1803. DEMAYNADIER, P. G., AND M. J. HUNTER JR. 1998. Effects of silvicultural edges on the distribution and abundance of amphibians in Maine. Conservation Biology 12:340–352. ———. 1999. Forest canopy closure and juvenile emigration by pool-breeding amphibians in Maine. Journal of Wildlife Management 63:441– 450. DOWNS, F. L. 1978. Unisexual Ambystoma from the Bass Islands of Lake Erie. Occasional Papers of the Museum of Zoology University of Michigan 685:1–36. ———. 1989a. Ambystoma laterale (Shaw), Blue-Spotted Salamander. In R. A. Pfingsten and F. L. Downs (eds.), Salamanders of Ohio, pp. 102–107. Bulletin of the Ohio Biological Survey, Columbus, Ohio. ———. 1989b. Ambystoma maculatum (Shaw), Spotted Salamander. In R. A. Pfingsten and F. L. Downs (eds.), Salamanders of Ohio, pp. 108–124. Bulletin of the Ohio Biological Survey, Columbus, Ohio. DUELLMAN, W. E., AND L. TRUEB. 1986. Biology of Amphibians. Johns Hopkins University Press, London. FLAGEOLE, S., AND R. LECLAIR JR. 1992. E´tude de´mographique d’une population de salamanders (Ambystoma maculatum) a` l’aide de la me´thode squelettochronologique. Canadian Journal of Zoology 70: 740–749. GAMRADT, S. C., AND L. B. KATS. 1996. Effect of introduced crayfish and mosquitofish on California newts. Conservation Biology 10:1155–1162. HOMAN, R. N., J. M. REED, AND B. S. WINDMILLER. 2003. Analysis of Spotted Salamander (Ambystoma maculatum) growth rates based on long-bone growth rings. Journal of Herpetology 37:617–621. HOMAN, R., B. S. WINDMILLER, AND J. M. REED. 2004. Critical thresholds associated with habitat loss for two vernal pool-breeding amphibians. Ecological Applications 14:1547–1553. HOPKINS, W. A., M. T. MENDONC¸A, AND J. D. CONGDON. 1997. Increased circulating levels of testosterone and corticosterone in Southern Toads, Bufo terrestris, exposed to coal combustion waste. General and Comparative Endocrinology 108:237–246. HOUCK, L. D., M. T. MENDONC¸A, T. LYNCH, AND D. SCOTT. 1996. Courtship behavior and plasma levels of androgens and corticosterone in male marbled salamanders, Ambystoma opacum (Ambystomatidae). General and Comparative Endocrinology 104:243–252. HUSTING, E. L. 1965. Survival and breeding structure in a population of Ambystoma maculatum. Copeia 1965:352–362. KIESECKER, J. M., A. R. BLAUSTEIN, AND L. K. BELDEN. 2001. Complex causes of amphibian population declines. Nature 410:681–684.
LOWCOCK, L. A. 1994. Biotype, genomotype, and genotype: variable effects of polyploidy and hybridity on ecological partitioning in a bisexualunisexual community of salamanders. Canadian Journal of Zoology 72:104–117. LOWCOCK, L. A., H. GRIFFITH, AND R. W. MURPHY. 1991. The Ambystoma laterale-jeffersonianum complex in Central Ontario: ploidy structure, sex ratio, and breeding dynamics in a bisexual-unisexual community. Copeia 1991:87–105. MACGREGOR, H. C., AND T. M. UZZELL. 1964. Gynogenesis in salamanders related to Ambystoma jeffersonianum. Science 143:1043–1045. MADISON, D. M. 1997. The immigration of radioimplanted Spotted Salamanders, Ambystoma maculatum. Journal of Herpetology 31:542–551. MINTON JR., S. A. 1972. Amphibians and Reptiles of Indiana. Indiana Academy of Science, Indianapolis. PATON, P., S. STEVENS, AND L. LONGO. 2000. Seasonal phenology of amphibian breeding and recruitment at a pond in Rhode Island. Northeastern Naturalist 7:255–269. PECHMANN, J. H. K., D. E. SCOTT, R. D. SEMLITSCH, J. P. CALDWELL, L. J. VITT, AND W. GIBBONS. 1991. Declining amphibian populations: the problem of separating human impacts from natural populations. Science 253:892–895. PETRANKA, J. W. 1998. Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC. POREJ, D., M. MICACCHION, AND T. E. HETHERINGTON. 2004. Core terrestrial habitat for conservation of local populations of salamanders and Wood Frogs in agricultural landscapes. Biological Conservation 120:399–409. POUNDS, J. A., M. P. L. FOGDEN, AND J. H. CAMPBELL. 1999. Biological response to climate change on a tropical mountain. Nature 398:611–615. REED, J. M., AND A. R. BLAUSTEIN. 1995. Assessment of ‘‘non-declining’’ amphibian populations using power analysis. Conservation Biology 9:1299–1300. REGOSIN, J. V., B. S. WINDMILLER, AND J. M. REED. 2003a. Influences of abundance of small mammal burrows and conspecifics on the density and distribution of Spotted Salamanders (Ambystoma maculatum) in terrestrial habitats. Canadian Journal of Zoology 81:596–605. ———. 2003b. Terrestrial habitat use and winter densities of the Wood Frog (Rana sylvatica). Journal of Herpetology 37:390–394. REGOSIN, J. V., B. S. WINDMILLER, R. N. HOMAN, AND J. M. REED. 2005. Variation in terrestrial habitat use by four pool-breeding amphibian species. Journal of Wildlife Management 69:1481–1493. RUSSELL, A. P., G. L. LAWRENCE, AND D. R. HALL. 1996. Growth and age of Alberta Long-Toed Salamanders (Ambystoma macrodactylum krausei): a comparison of two methods of estimation. Canadian Journal of Zoology 74:397–412. SHOOP, C. R. 1974. Yearly variation in larval survival of Ambystoma maculatum. Ecology 55:440–444. SPOLSKY, C. M., C. A. PHILILIPS, AND T. UZZELL. 1992a. Antiquity of clonal salamander lineages revealed by mitochondrial DNA. Nature 356:706– 708.
COMPARATIVE LIFE HISTORIES OF TWO AMBYSTOMA ———. 1992b. Gynogenetic reproduction in hybrid mole salamanders (Genus Ambystoma). Evolution 46:1935–1944. STENHOUSE, S. L. 1987. Embryo mortality and recruitment of juveniles of Ambystoma maculatum and Ambystoma opacum in North Carolina USA. Herpetologica 43:496–501. UZZELL JR., T. M. 1964. Relations of the diploid and triploid species of the Ambystoma jeffersonianum complex (Amphibia: Caudata). Copeia 1964: 257–230. UZZELL JR., T. M., AND S. M. GOLBLATT. 1967. Serum proteins of the salamanders of the Ambystoma jeffersonianum complex, and the origins of the triploid species of this group. Evolution 21:345–354. WAKE, D. B., AND J. CASTENET. 1995. A skeletochronological study of growth and age in relation to adult size in Batrachoseps attenuatus. Journal of Herpetology 29:60–65. WELLER, W. R., W. G. SPRULES, AND T. P. LAMARRE. 1978. Distribution of salamanders of the Ambystoma jeffersonianum complex in Ontario. Canadian Field Naturalist 92:174–181.
409
WILBUR, H. M. 1971. The ecological relationship of the salamander Ambystoma laterale to its all-female, gynogenetic associate. Evolution 25:168–179. ———. 1977. Propagule size, number, and dispersion pattern in Ambystoma and Asclepias. American Naturalist 111:43–68. WINDMILLER, B. S. 1996. The Pond, the Forest, and the City: Spotted Salamander Ecology and Conservation in a Human-Dominated Landscape. Unpubl. Ph.D. diss., Tufts University, Medford, MA. WINDMILLER, B. S., R. N. HOMAN, J. V. REGOSIN, L. A. WILLITTS, D. L. WELLS, AND J. M. REED. In press. Two case studies of declines in vernal pool-breeding amphibian populations following loss of adjacent upland forest habitat. Urban Herpetology. Herpetological Conservation, Volume 3, Society for the Study of Amphibians and Reptiles, Salt Lake City, UT. WYMAN, R. L. 1990. What’s happening to the amphibians? Conservation Biology 4:350–352. Accepted: 20 March 2007.
