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Ambystoma maculatum (Shaw, 1802)
Spotted Salamander
Wesley K. Savage
Kelly R. Zamudio
1. Historical versus Current Distribution. Spotted salamanders
(Ambystoma maculatum) are distributed throughout the interior and
Atlantic Coastal Plains of the eastern United States, primarily in hardwood and mixed
coniferous-deciduous forest habitats (Bishop, 1943; Pope, 1944; Anderson, 1967b;
Upchurch, 1971; Lang, 1972; Schuette, 1980; Kats et al., 1988; Lovich and Fisher, 1988;
Beane and Gaul, 1991; C. Phillips, 1991a,b, 1992, 1994; Schwaner and Anderson, 1991; E.E.
Brown, 1992; Petranka, 1998). This species prefers lowland forests; they are
occasionally found in more open habitats such as meadows, but usually near forest
edges. Although not typically a montane species, spotted salamanders can occur at
higher elevations when suitable breeding sites are available (Thompson and Gates,
1982).
With the exception of
a few isolated populations, spotted salamanders are also absent from the Coastal Plain of
North Carolina, as well as southeastern portions of Virginia, Maryland, Delaware, and
New Jersey. No specimens have been recorded from the Florida Peninsula or the
Coastal Plain of the Florida Panhandle to southern Georgia.
There is no evidence
to suggest that current and historical distributions differ; however, range reductions
undoubtedly have occurred, and continue to occur, due to habitat alteration.
Despite these changes, new county records (e.g. Brinkman et al., 2001; Cochran and
Cochran, 2001; Scott et al., 2001) documenting the geographic distribution of spotted
salamanders have been published in recent years. Moreover, two new county records
extend the range of this species into Minnesota (C. Hall, in
review), indicating that the extent of the range is still being
identified.
Smith (1961)
mentioned geographic variation between populations in northeast and southern Illinois in
the average sizes of adults, number of teeth, number of dorsal spots, costal groove
counts, and contrast between head spot and body spot color. Likewise, DuShane and
Hutchinson (1944) raised larvae from independent populations in a common garden
experiment and demonstrated significant differences between these populations in
developmental rates and size at metamorphosis. This variation has led some to
suggest the presence of two distinct subspecies of spotted salamanders (Smith,
1961).
There is indirect
evidence that ranges may have been reduced substantially during the Pleistocene glacial
cycles, causing geographic discontinuity and resulting in the genetic differentiation
between two highly differentiated lineages (C. Phillips, 1994; Zamudio and Savage,
2003). Post-glacial recolonization resulted in the expansion and recontact of these
two lineages in at least three major regions: (1) the southern Interior Lowlands of
Missouri and Illinois; (2) the Interior Lowlands of Ontario, Canada; and (3) from the
southern Appalachian Highlands to the coast of South Carolina (Zamudio and Savage,
2003). Three fossil vertebral elements assigned to spotted salamanders date from
the late Pleistocene and were collected in a cave near St. Louis, Missouri (Holman,
1965b), near the western extent of the species' current range. A second fossil
form (A. minshalli) has been proposed as ancestral to A.
maculatum (Holman, 1975) and is clearly a member of the maculatum
group. These fossils, collected in Nebraska and Kansas (Estes and Tihen, 1963;
Tihen and Chantell, 1963), date back to the Upper Miocene, suggesting that this group was
well differentiated before Plio-Pleistocene climatic changes. The presence of
fossils in these regions indicates that the historical range of spotted salamanders
coincides in part with the contemporary range and that members of the spotted salamander
lineage once extended farther west into the Great Plains.
2. Historical versus Current Abundance. Although there are no quantitative
assessments of declines in abundance for spotted salamanders, their habitat requirements
suggest that, as with other pond-breeding species, they are adversely affected by
deforestation and wetland destruction (Petranka, 1998). Habitat loss,
acidification, metal concentrations, environmental contaminants, and fish introductions
are certainly factors that could contribute to declines of spotted salamanders, and some
have been shown to negatively affect this species (Pough, 1976; Clark, 1986b; Blem and
Blem, 1989, 1991; Sadinski and Dunson, 1992; Brodman, 1993; Rowe and Dunson, 1993; but
see Cook, 1983). Acid rain has received particular attention in the Northeast as a
factor reducing survivorship (e.g., Portnoy, 1990). Future spotted salamander
declines are possible because these animals have not evolved mechanisms to tolerate
acidic conditions or introduced fishes, suggesting they will respond negatively to these
threats (Tome and Pough, 1982; Clark, 1986b; Sexton et al., 1994; see also Petranka,
1998). Because overall range reductions caused by changing landscape features
coincide with human land use, we expect that current abundances are lower than historical
numbers.
3. Life History Features.
A. Breeding.
Reproduction is aquatic.
i. Breeding migrations. Many life history aspects of spotted salamanders vary
tremendously across their geographic range, most likely due to large differences in
environmental conditions. The pattern of variation is complex and does not seem to
be determined exclusively by latitude or geographic locality. Throughout their
range, individuals migrate from terrestrial overwintering sites into seasonally available
aquatic habitats to breed. Although the vast majority of individuals are
reproductively active, a small percentage of non-reproductive individuals also migrate
(Shoop, 1967). Why these non-reproductive animals migrate is not known.
Breeding individuals are easily identified by body size and characteristics of the vent:
males have a conspicuously swollen vent covered with rough papillae; females have a
rounded, smooth vent, and are generally larger in body size (Wilson, 1976; Sexton et al.,
1986). Finkler et al. (2003) identified sex-related differences in terrestrial and
aquatic locomotor performance in breeding spotted salamanders.
Males typically
arrive earlier, anywhere from 1–6 d, than females at ponds (Bishop, 1941b; Hillis,
1977; Douglas, 1979; Sexton et al., 1986). This appears to be due to a
differential response between the sexes to temperature cues for the onset of migration
(Sexton et al., 1990) or to locomotor performance (Finkler et al., 2003).
Migrations take place at night during or following early spring rains correlated with
increasing air temperatures; in more northern regions, migrations follow periods of
increased temperature and heavy snowmelt or rain (Wright, 1908; Wright and Allen, 1909;
Blanchard, 1930; Bishop, 1941b, 1943; Baldauf, 1952; Whitford and Vinegar, 1966; Wilson,
1976; Hillis, 1977). The exact role of each of these ecological features in the
onset of migrations is still unclear. A detailed study by Sexton et al. (1990)
showed a threshold system of rainfall and temperature cues and a correlation of
immigration with soil temperatures (4.5 ˚C, 30 cm below the surface) when the
thermal profile was reversed.
The onset of breeding
varies greatly across their range and can occur as early as December in southern
populations or as late as April at higher latitudes (Brimley, 1921a; Blanchard, 1930;
Dempster, 1930; King, 1939; Pawling, 1939; Welter and Carr, 1939; Gray, 1941; Baldauf,
1952; Hardy, 1952; Moulton, 1954b; Peckham and Dineen, 1954; Green, 1955; Seibert and
Brandon, 1960; Whitford and Vinegar, 1966; Worthington, 1968, 1969; Minton, 1972, 2001;
Keen, 1975; Mount, 1975; Harris, 1980; Walls and Altig, 1986; Talentino and Landre, 1991;
Pinder and Friet, 1994; Brodman, 1995). There is a rough latitudinal pattern in
the degree of breeding synchrony within populations: in more southern populations the
breeding season may last over 2 mo, usually with 2–3 major bouts of activity
following heavy rains (Peckham and Dineen, 1954; Mount, 1975; Harris, 1980; Sexton et
al., 1986); breeding in northern regions is more synchronized and can be restricted to a
few days (2–5 d; Wilson, 1976; Talentino and Landre, 1991; Brodman, 1995; Petranka,
1998). In a Missouri population, Sexton et al. (1986) estimated that the breeding
season lasts 45 d for males, 37 d for females. In North Carolina, Stenhouse (1985a)
reported 56 and 73 d in consecutive years. Husting (1965) recorded breeding
seasons of 9–29 d over 5 yr in Michigan; in an Indiana population, breeding
averaged 25 d (Peckham and Dineen, 1954). Over 4 yr, Wilson (1976) recorded
breeding seasons that averaged 18.5 d. By contrast, breeding seasons in Ohio lasted
only 3–5 d (Brodman, 1995); 2–3 d in Massachusetts (Talentino and Landre,
1991). During the breeding season both sexes lose weight. In Missouri, Sexton
et al. (1986) reported average weight losses of 13% and 38%, for males and females,
respectively; whereas in Massachusetts, Windmiller (1996) found values of 4.5% and
24.1%.
Return rates of
adults to breeding ponds suggest that while individuals in some populations breed
annually, others may skip years; however, mark–recapture studies may underestimate
the number of animals breeding in consecutive years because they do not account fully for
dispersal of adults to other sites. Thus it is unknown whether adults are capable
of sustained annual breeding or if the sexes differ in that regard. High annual
return rates were recorded at a Rhode Island breeding pond (89.5%; Whitford and Vinegar,
1966). Douglas and Monroe (1981) reported six of eight (75%) tagged individuals
returning to a Kentucky breeding pond in two consecutive years; however, these samples
sizes were relatively small. In Missouri, 38% of marked females and 30% of marked
males returned to breed the following year (Phillips and Sexton, 1989). Less
consistent breeding patterns were found in a Michigan population, where annual return
rates ranged from 18–55% over the course of five years (Husting, 1965). In New
York, Wilson (1976) recaptured a total of only 12 males and 1 female in the four years of
his study, representing 8.7% of males and 0.7% of females. These longer-term
studies suggest that there may be large temporal as well as inter-population differences
in breeding patterns.
Numerous studies have
investigated migratory orientation of spotted salamanders during the breeding
season. Adults usually exit ponds near where they entered, suggesting that they use
the same migratory route between terrestrial home ranges and breeding sites (Shoop,
1965a, 1968; Wilson, 1976; Douglas and Monroe, 1981; Kleeberger and Werner, 1983;
Stenhouse, 1985a; Sexton et al., 1986; Phillips and Sexton, 1989; see also Petranka,
1998). In addition, the order of male arrival was correlated between years in one
population in North Carolina (Stenhouse, 1985a), suggesting that males may be returning
to the same home ranges after breeding. Downs (1989d) observed some adults
returning to the same home burrow after emigrating from breeding ponds in Ohio.
Post-breeding adults
move on average 115.7 m from the pond edge to their terrestrial home ranges (range,
0–249 m; average of adult movement distances reported from six studies; Wacasey,
1961; P.K. Williams, 1973; Douglas and Monroe, 1981; Kleeberger and Werner, 1983;
Madison, 1997). Semlitsch (1998) reviewed adult movement patterns in six species of
ambystomatids (including spotted salamanders) and concluded that terrestrial buffer zones
of breeding ponds would have to extend 164.3 m from the edge to encompass movements of
95% of the adults in a population.
Mark–recapture
studies and displacement experiments suggest that two cues may be important in migratory
orientation. Olfaction was suggested as an orientation mechanism in a laboratory
choice experiment where adult salamanders preferred substrate saturated with their home
pond odors (McGregor and Teska, 1989). Shoop (1968) and Whitford and Vinegar
(1966) displaced adult individuals 500 m and 128 m from their home ponds. Most
individuals successfully oriented back to their home ponds; a higher percentage of those
released in and adjacent to a seepage returned to their home pond, suggesting they may be
using rheotaxic orientation in addition to olfaction (Whitford and Vinegar, 1966).
Rheotropism was also suggested in individuals migrating through runoff in two Michigan
ponds following heavy rains (Finneran, 1951). These data are suggestive but not
conclusive and underscore the need for a rigorously controlled experimental test of
orientation mechanisms.
ii. Breeding
habitat. In addition to ephemeral, fishless wetlands, spotted salamanders will
breed in roadside ditches and tire ruts in dirt roads, artificial ponds, floodplain
wetlands, and marshes. Although they typically use ephemeral habitats, breeding has
been documented in permanent ponds containing fishes (Husting, 1965; Harris, 1984; Figiel
and Semlitsch, 1990; see also Petranka, 1998), as well as in a fish-free lake in New York
(Bahret, 1996). Populations in the Atlantic Coastal Plain sometimes breed in stream
backwaters containing predatory fishes; larvae typically will not survive in these
habitats unless there is sufficient submergent vegetation (Husting, 1965; Harris, 1984;
Figiel and Semlitsch, 1990).
In breeding ponds,
adults aggregate in large polyandrous groups for courtship and mating, referred to as a
nuptial dance or “liebesspiel” (O'Donnell, 1937). In the presence of
females, courting males deposit spermatophores in an area of approximately 1 m2 on
the pond bottom. Spermatophores are usually attached to leaves, twigs, and other
submerged vegetation (Breder, 1927; Bishop, 1943; Petranka, 1998). Arnold (1976)
showed in experimental field enclosures that males produce on average 40 spermatophores
the first night when in the presence of a female (range, 10–81), and spermatophore
production decreases rapidly on successive nights. A male vigorously courts a
female by repeatedly nudging her with his snout, swinging his head back and forth along
her dorsum, and lifting his head under her chin (Arnold, 1976). A sexually
receptive female will also nudge males and search for spermatophores by stepping from
side to side with her hindlimbs while moving forward. Sound production has been
reported during lulls in courtship (Breder, 1927), although it is unknown whether there
is any courting significance because sounds were emitted more often in the presence of
same-sex individuals (Wyman and Thrall, 1972 ). Once a female finds a
spermatophore, she orients towards it tactually, squats, arches the base of her tail and
removes the sperm mass from the gelatinous base with her vent. Females pick
up multiple sperm masses, and paternity analyses of experimental matings (Tennessen and
Zamudio, 2003) and wild-collected clutches (E.M. Myers and K.R.Z., unpublished data)
confirm that multiple paternity is common in this species and that eggs are frequently
fertilized by sperm storage.
Arrival time at
breeding ponds has significant impact on male reproductive success. In experimental
enclosures in the field, Tennessen and Zamudio (2003) enclosed mating trios (one female
and two males) in control enclosures and both males were allowed to mate at the same
time; in experimental enclosures one male was introduced in the mating chamber 2 hr
before the second male. Paternity analyses of the resulting offspring indicate that
early arrival at a mating aggregation is an important determinant of reproductive
success. In control enclosures, the two males fathered similar proportions of
offspring; in experimental enclosures, the early arriving male sired significantly more
offspring than the late-arriving male (Tennessen and Zamudio, 2003).
Sex ratios of spotted
salamanders are always male-biased in breeding ponds and vary from 1.5–3.5:1
(Peckham and Dineen, 1954; Husting, 1965; Whitford and Vinegar, 1966; Hillis, 1977;
Stenhouse, 1985a; Sexton et al., 1986; Downs, 1989d; Flageole and Leclair, 1992).
Differences in age at maturity, reproductive frequency, and survival may explain the
strongly male-biased sex ratios (Wacasey, 1961; Flageole and Leclair, 1992). This
ratio, combined with the short breeding season, produces extreme sexual competition among
males. Sexual interference by spermatophore “capping” is a common
behavior for males. When males encounter other spermatophores, they deposit a
secondary spermatophore upon it, but it is unknown whether males can discriminate their
own spermatophores from those of other males (Arnold, 1976). Spermatophores can be
found in stacks 2–6 high, and the female presumably picks up the top-most sperm
mass.
B. Eggs.
i. Egg deposition sites. Egg masses are either scattered individually in breeding
ponds or deposited in aggregates of 50 clutches or more. Single eggs have been
found on land near a pond (Brimley, 1921a; Smith, 1921). Reported mean numbers of
eggs/mass are highly variable across regions, ranging from 58–155 (Bishop, 1941b;
Seibert and Brandon, 1960; Woodward, 1982; Stangel, 1988; Downs, 1989d; Talentino and
Landre, 1991). Egg masses are deposited in firm and compact masses on sticks,
submergent vegetation, small branches, or directly on the pond bottom. The thick,
firm jelly coat on eggs serves to protect them from desiccation (Nyman, 1987), physical
disturbances, and predation (Cory and Manion, 1953; Ward and Sexton, 1981; Semlitsch,
1988).
Some females deposit
eggs containing hydrophobic proteins in the outer jelly layer producing white or milky
egg masses in which the embryos are not visible (Hardy and Lucas, 1991). These
white and clear forms are present among individuals within populations, but there is no
evidence of differences in egg viability or hatching size related to this
polymorphism. However, Brodman (1995) demonstrated that white egg masses in an Ohio
population contained significantly more eggs than clear egg clutches (103.5 ± 11.7
and 66.1 ± 4.3, respectively), suggesting the advantage may lie in higher
fecundity. Metts (2001) also found that white egg masses contain more eggs than
clear ones, but that clear egg masses have significantly better hatching success than
white masses. The functional role or advantage of the white protein is still
unclear (Ruth et al., 1993).
ii. Clutch size. Females deposit 2–4 egg masses, each containing from
1–250 eggs (Bishop, 1941b; Shoop, 1974; Wilson, 1976; Petranka, 1998).
After egg deposition,
chlamydomonad algae (Oophila amblystomatis) enter the inner jelly
capsules of individual eggs and presumably aids in increased oxygen supply to developing
embryos (Breder, 1927; Gilbert, 1942, 1944; Hutchison and Hammen, 1958; Hammen and
Hutchison, 1962; Gatz, 1973a; Bachmann et al., 1986). In laboratory experiments,
embryos with algal symbionts hatched sooner than clutches with reduced algal growth
(Gilbert, 1942). Embryonic mortality is variable and can be high, ranging from
0–100% (Pough, 1976; Harris, 1980; Cook, 1983; Clark, 1986b; Stenhouse, 1987;
Stangel, 1988; Ireland, 1989; Brodman, 1995). Eggs laid later in the breeding season
had higher rates of survivorship in a North Carolina pond, suggesting that within-year
timing of breeding can have important implications for individual fitness (Harris,
1980). Egg mortality is increased by low pH, predation, and freezing in shallow
areas of ponds (Pough, 1976; Wilson, 1976; Ireland, 1989). Incubation times range
from 8–60 d (Bishop, 1941b, 1943; Whitford and Vinegar, 1966; Worthington, 1968,
1969; Shoop, 1974; Keen, 1975; Freda, 1983; Sexton et al., 1986; Stangel, 1988; Nyman,
1991; Talentino and Landre, 1991), and hatchlings from a Mississippi pond measured 14.8
mm ± 1.46 (Walls and Altig, 1986). However, all developmental features are
temperature-dependent (Voss, 1993a) and vary depending on the population and region
(DuShane and Hutchinson, 1944).
C.
Larvae/Metamorphosis.
i. Length of larval stage. Duration of the larval stage is highly variable and
lasts anywhere from 6 wk to > 12 mo (Bishop, 1941b, 1943; Dundee, 1947; Worthington,
1968; Freda, 1983; Nyman, 1991; Talentino and Landre, 1991). Metamorphic patterns
can vary within a population across years (Phillips, 1992), as well as among individuals
within populations (Ireland, 1973). Most larvae transform from June–August
(Petranka, 1998), but overwintering larvae have been found in spring-fed ponds (Bleakney,
1952; Whitford and Vinegar, 1966; Ireland, 1973; Hillis and Miller, 1976; Stangel, 1988;
Phillips, 1992). Overwintering larvae in Missouri reach, on average, 69 mm TL and
transform as late as May (Phillips, 1992). Larvae range in size from 27–75
mm TL at metamorphosis, and these lengths vary greatly across populations (Bishop, 1941b,
1943; Dundee, 1947; Worthington, 1968; Freda, 1983; Harris, 1984; Nyman, 1991; Talentino
and Landre, 1991; Phillips, 1992; see also Petranka, 1998). Survival to
metamorphosis is low, usually ≤ 13% of hatched larvae. In some cases, entire
cohorts die due to intense predation and wetland drying (Shoop, 1974; Stenhouse, 1985b,
1987; Stangel, 1988; Ireland, 1989; Figiel and Semlitsch, 1990; Rowe and Dunson,
1995).
ii. Larval requirements.
a. Food. Larvae are gape-limited and size-selective feeders, ingesting a range of
aquatic invertebrates including zooplankton, coleopterans, isopods, ostracods, odonates,
and trichopterans. Smaller larvae feed primarily on zooplankton; as they grow in
size, consumption shifts towards larger prey such as chironomids, chaoborids, and isopods
(Nyman, 1991). Branch and Altig (1981) and Freda (1983) reported that the
predominant prey items of larvae were cladocerans and copepods. However, Harris
(1995) observed a higher reduction of isopods and amphipods relative to zooplankton
under experimental conditions. Freda (1983) also described stomach contents
containing eastern newt (Notophthalmus viridescens) larvae with mean SVL
63% of the body size of the larval spotted salamander predators.
b. Cover. In the presence of predators, refugia such as submerged vegetation are
necessary for larval survivorship (Walls, 1995). Spotted salamanders are
vulnerable to predation by other ambystomatids, such as marbled salamanders (A.
opacum). Interestingly, while spotted salamander larvae require cover,
their use of cover does not increase in the presence of competing ambystomatids (Walls,
1995) or fishes (Ireland, 1989; but see Figiel and Semlitsch, 1990). In contrast,
Brodman et al. (2002) found that the presence of other Ambystoma caused spotted
salamander larvae to occupy refuges more and decrease their activity, and in the presence
of A. laterale (blue-spotted salamanders; a potential competitor), to
change their activity and use of microhabitat in opposite directions from that of its
congener. Stratification (floating in the water column, usually at night) is
present in some populations, although its function is not well understood (but see Lannoo
and Bachmann, 1984b). Branch and Altig (1981) reported larval stratification in
Mississippi ponds. In New Jersey, small larvae tend to remain in leaf litter, while
larger larvae stratify in the water column (Nyman, 1991; but see Anderson and Graham,
1967).
iii. Larval polymorphisms. Have not been described for spotted salamanders.
Given the widespread distribution and numerous population studies on this species, it is
unlikely that polymorphisms exist.
iv. Features of metamorphosis. Timing of metamorphosis varies greatly, even within
populations, and larval overwintering occurs in some populations that breed in permanent
ponds (Phillips and Sexton, 1989; Whitford and Vinegar, 1966). Metamorphosis
typically occurs 8–16 wk after hatching, when larvae reach 27.0–32.0 mm SVL
(Worthington, 1968; Talentino and Landre, 1991). In many populations that breed in
seasonal and semipermanent wetlands, larval survivorship is correlated with wetland
duration (Ball, 1937; Ling et al., 1986; Stangel, 1988; see also Petranka, 1998).
Abundance and size at metamorphosis are also positively correlated with length of the
hydroperiod (Rowe and Dunson, 1995; Phillips et al., 2002). However, in a short
hydroperiod year, size at metamorphosis is negatively correlated with time to emergence
from the pond, suggesting that faster growing larvae reach an optimal size when compared
with other larvae that take longer to metamorphose at smaller sizes (Phillips et al.,
2002). Likewise, mean size at metamorphosis in a year when hydroperiod is shorter
than usual is significantly smaller than mean size in a longer hydroperiod year (Phillips
et al., 2002). At high densities or in the presence of other ambystomatid larvae,
spotted salamander larvae have higher mortality, grow more slowly, and metamorphose at
smaller sizes (Wilbur, 1972; Wilbur and Collins, 1973). At a Massachusetts pond,
larvae that remain in their natal pond longer metamorphose at greater weights than
earlier metamorphosing individuals (Windmiller, 1996).
v. Post-metamorphic migrations. Newly metamorphosed animals dispersing from
breeding ponds move beneath rocks and logs near the pond margin where they are sometimes
exposed to high temperatures (Pough and Wilson, 1970) and desiccation (Shoop,
1974). Because metamorphosis varies among individuals, the seasonal migration of
juveniles away from the ponds is not as synchronized as the adult breeding
migrations. Wilson (1976) captured newly metamorphosed animals exiting a New York
pond over a period of 5 wk from 27 July–29 August. He recorded sporadic
movements ≤ 25 m a night over the course of several nights. In Massachusetts,
Windmiller (1996) recorded episodic dispersal of post-metamorphic animals from 1 July to
autumn. However, there is one report of a concentration of “hundreds”
of juveniles migrating along a dirt road adjacent to a wooded area after a summer storm
in Maryland (Hardy, 1952).
Orientation of
post-metamorphic individuals in five of six cohorts was highly non-random and biased
towards a northward direction in five Massachusetts ponds (Windmiller, 1996).
These orientation patterns seemed to reflect the emigration routes of post-breeding
parental cohorts and the location of upland forest habitat. In the one
post-metamorphic cohort that did not disperse in a northward direction, no forested land
occurred to the north of the pond. Most individuals (50%) remained within 40 m of
their natal pond as late as 8 December, while 36% were between 40–100 m and 14%
dispersed beyond 100 m. Later-metamorphosing individuals were heavier in weight and
dispersed on average 18 m farther than those metamorphosing earlier (Windmiller,
1996).
vi. Neoteny. There are no reports of non-transforming individuals in spotted
salamanders. Given the widespread distribution and numerous population studies on
this species, it is unlikely that neotenic adults exist.
D. Juvenile
Habitat. Habitat characteristics of juveniles are similar to those of adults.
Juvenile abundance declines sharply across a gradient running from relatively mature
forest to interior habitat (70–90 yr old) to recently clearcut habitat (2–11
yr old) in Maine (deMaynadier and Hunter, 1999). Juveniles are found more
frequently closer to the natal pond edge (< 75 m) and seek refuge in burrows and under
rocks and fallen logs (Wilson, 1976; Windmiller, 1996). Although usually found
only in moist forest habitats, some juveniles were collected from under driftwood on the
sandy shore of the Chesapeake Bay in Maryland (Hardy, 1952). Juveniles typically
emerge at times beginning in midsummer (Parmalee, 1993). Detailed data for the
period of juvenile development are sparse, but presumably they forage on forest floor
invertebrates in underground burrows while they mature.
E. Adult
Habitat. Spotted salamanders occur within eastern mixed-deciduous forest habitats
and are common in mesic to floodplain habitats. They primarily rely on cutaneous
respiration (Whitford and Hutchison, 1966a) and are more commonly found under large,
moist cover objects (Parmalee, 1993). As with juveniles, adult abundance declines
sharply from relatively mature forest to interior habitat to recently clearcut habitat in
Maine (deMaynadier and Hunter, 1999). Along the Atlantic Coastal Plain, spotted
salamanders are not common in the drier, sandy, upland environments and are mostly found
in hardwood, bottomland habitats with lower soil temperatures and higher soil
moisture. These habitats frequently harbor fish populations that significantly
decrease the reproductive success of spotted salamanders but do not exclude them from
breeding there (Semlitsch, 1988). Potential habitat has been described by Baldwin
and Vasconcelos (2003).
F. Home Range
Size. Burrow systems of individual adults in Kentucky and Michigan encompass
12–14 m2 and an average of 9.8 m2 of forest floor, respectively (Douglas
and Monroe, 1981; Kleeberger and Werner, 1983). In Michigan, average home range
movements of 14 ± 3 m were recorded over a 6–7 wk period. During this
time, adults were mostly found in burrows (72% of the time), but also in decaying logs
(21%) and leaf litter (7%; Kleeberger and Werner, 1983).
G. Territories.
Although territoriality has not been documented in larval salamanders, larvae exhibit
visual and movement displays that function as aggressive behavior in crowded environments
(Walls and Semlitsch, 1991). In the larval stage, refuge use and stratification
may minimize such aggressive interactions through habitat partitioning (Branch and Altig,
1981; Nyman, 1991). Adults are almost always the sole residents under cover objects
and are rarely found in close proximity in their forest habitats (Parmelee, 1993).
In laboratory trials, adults will alter their normal movement patterns to avoid
conspecifics (Ducey and Ritsema, 1988). In other laboratory trials, adults
actively defended experimental burrows and feeding areas against conspecific and
heterospecific intruders (Ducey and Ritsema, 1988; Walls, 1990; Ducey and Heuer,
1991). Conspecific interactions involve biting, head butting, and forebody raising
(Ducey and Ritsema, 1988). In one case of interspecific interactions, spotted
salamanders consumed 9% of an eastern red-backed salamander (Plethodon
cinereus), but this aggression may have been due to predation rather than
territorial defense (Ducey et al., 1994).
H.
Aestivation/Avoiding Dessication. In some areas of the range, adults are likely to
experience surface temperatures above their critical thermal maximum (34.9–35.8
˚C; Gatz, 1971, 1973b) and will usually seek refuge from heat and desiccation in
small mammal burrows. Adults have been found in burrows as deep as 1.3 m
(Semlitsch, 1983c).
I. Seasonal
Migrations. Adults move to and from breeding ponds (see "Breeding
migrations" above). Post-metamorphic animals migrate away from wetlands from
mid to late summer (see Faccio, 2003).
J. Torpor
(Hibernation). Adults and post-metamorphic animals hibernate in subterranean
burrows and likely keep from freezing by moving below the frost line.
K. Interspecific
Associations/Exclusions. The structure of larval communities has been the focus of
numerous studies on the effects of phenology, density, and interspecific competition
among sympatric ambystomatids. Spotted salamanders often breed syntopically with
congeners, including Jefferson salamanders (A. jeffersonianum), marbled
salamanders, mole salamanders (A. talpoideum), eastern tiger
salamanders (A. t. tigrinum), blue-spotted salamanders, and
small-mouthed salamanders (A. texanum). Many studies have
investigated the mechanisms of coexistence among these species, and in general, spotted
salamander larvae are inferior direct competitors because they generally are smaller than
their interspecific competitors. However, female Cope's gray treefrogs
(Hyla chrysoscelis) avoid depositing eggs in pools containing larval
spotted salamanders, suggesting that larvae prey on hatchling tadpoles (Resetarits and
Wilbur, 1989).
Brodman (1995, 1996)
found that density of each species was an important component determining the outcome of
interactions with conspecific and heterospecific competitors. Species show negative
responses, such as reduced growth rate and smaller body size at metamorphosis to
increased density (Semlitsch and Walls, 1993). Walls and Jaeger (1987) and Walls
(1996) demonstrated that spotted salamander larvae were superior exploitative competitors
when in competition with mole salamanders. However, Brodman (1999b) argued that
coexistence between spotted salamanders and Jefferson salamanders could not be explained
by the interference-exploitative competition trade-off, because spotted salamanders did
not reduce the growth of congeners at high densities. Other factors influence
interspecific competition, such as spatial or dietary partitioning through refugium
selection (Walls, 1995; Brodman, 1996), temperature preference (Anderson and Graham,
1967; Stauffer et al., 1983), or dietary differences (Nyman, 1991). Larval spotted
salamander behavior is highly variable and may explain their success in a variety of
competitive larval environments throughout their range (Brodman, 1996). For example,
spotted salamanders reduce the amount of time they spend in the water column
(stratification) in the presence of interspecific predators (Walls and Williams,
2001). Predator-mediated reduction in activity patterns potentially limits foraging
opportunities and hence potentially decreases survival in this species. Thus, in
some cases the composition of larval amphibian assemblages could exclude spotted
salamanders from communities of pond-breeding amphibians (Walls and Williams, 2001), yet
they continue to persist in many highly competitive larval environments.
Juvenile and adult
spotted salamanders live under cover objects and in burrows created by shrews, moles,
and other small mammals (Gordon, 1968; Douglas and Moore, 1981; Madison, 1997).
However, the associations among co-inhabitants of burrow systems are not well
known. Laboratory experiments show that juvenile spotted salamanders exhibit
preference for unoccupied burrows and will leave burrows already inhabited by conspecific
or heterospecific (marbled salamander) juveniles (Smyers et al., 2002). Adults
also share home ranges with other salamanders, including eastern red-backed salamanders
(Ducey et al., 1994) and mole salamanders (Walls, 1990). Spotted salamanders share
breeding habitats with numerous species, including fishes. Naive adults do not
adjust their breeding behavior in the presence of fish, nor do females reduce the number
of eggs they deposit (Sexton et al., 1994). However, larvae do seem to adopt
behaviors that protect them from fish predation (Figiel and Semlitsch, 1990).
L. Age/Size at
Reproductive Maturity. Adults generally range in size from 15–25 cm TL
(Petranka, 1998). In southern populations, individuals may take < 3 yr to reach
sexual maturity (Bishop, 1941b, 1943; Minton, 1972, 2001). In northern
populations, males reach maturity earlier than females. In a Québec
population examined using skeletochronology, the majority of animals were 2–18 yr
old with the mode at 6–8 yr. Most females matured by 7 yr at ≥ 78 mm
SVL. Males reached maturity between the ages of 2 and 6 and at ≥ 63 mm SVL
(Flageole and Leclair, 1992). In Michigan populations, males reach sexual maturity
in 2–3 yr and females in 3–5 yr (Wilbur, 1977c; see also Petranka,
1998). In Massachusetts, some males attain sexual maturity in 2 yr, while females
require an additional year (Windmiller, 1996). At this locality, the smallest
sexually mature individuals captured were 56.5 and 60.2 mm SVL for males and females,
respectively. Growth in spotted salamanders has been analyzed by Blackwell et al.
(2003) and Homan et al. (2003).
M. Longevity.
Individuals live ≤ 22–25 yr in captivity (P.H. Pope, 1928a, 1937; Snider and
Bowler, 1992), and skeletochronology indicated the oldest individual was 32 yr in a
Québec population (Flageole and Leclair, 1992). Several mark-recapture
studies at breeding ponds suggest that adult survivorship is high from one breeding
season to the next, ranging from 70–100% (Husting, 1965; Whitford and Vinegar,
1966; Douglas and Monroe, 1981; see also Petranka, 1998). Females appear to suffer
higher mortality than males (Harris, 1980).
N. Feeding
Behavior. During the breeding season adults apparently do not feed (Smallwood,
1928). In terrestrial sites, adults and juvenile spotted salamanders feed by either
protruding their heads from burrows using a sit-and-wait strategy or by foraging more
actively in wet weather on the forest floor. They are generalists on forest floor
invertebrates, consuming mollusks, earthworms, centipedes, millipedes, spiders, and a
wide variety of insects (Bishop, 1941b; Pope, 1944). Given the amount of time
adults spend in burrows and the depths at which they are found (1.3 m; Gordon, 1968;
Semlitsch, 1983c), they may also feed underground.
O. Predators.
Larval wood frogs (Rana sylvatica), centrarchid and cyprinid fishes,
and various larval invertebrate species prey on spotted salamander eggs (Ward and Sexton,
1981; Semlitsch, 1988; Petranka, 1998; Baldwin and Calhoun, 2002). In a Virginia
population, high reproductive failure was attributed to predation by centrarchid fishes
(Ireland, 1989). Eastern newt adults will eat spotted salamander eggs (Hamilton,
1932; Wood and Goodwin, 1954), as will caddisfly and midge (Parachironomus sp.)
larvae (Murphy, 1961; Leclair and Bourassa, 1981; Stout et al., 1992).
Larvae are preyed
upon by caddisflies (Ptilostomis postica; Murphy, 1961; Rowe and
Dunson, 1993; Rowe et al., 1994; and Banksiola dossuaria; Stout et al.,
1992) and other predatory aquatic insects such as midge (Parachironomus sp.)
larvae (Petranka, 1998). Wood frog tadpoles will prey on larvae (Petranka, 1998;
Petranka et al., 1998; Baldwin and Calhoun, 2002), as will least sandpipers
(Calidris minutilla; Stangel, 1983). Larval predators also include
other Ambystoma species; in regions of sympatry, marbled salamander larvae are
already present and will prey on spotted salamander larvae when they hatch (Stewart,
1956; Husting, 1965; Stenhouse, 1985b). Thus, it is not surprising that spotted
salamander larval densities are inversely correlated with marbled salamander larval
densities (but see Worthington, 1968; Cortwright, 1988; Petranka, 1998). Jefferson
salamander and silvery salamander (A. platineum) larvae also prey on
spotted salamander larvae (Noble, 1931; Nyman, 1991; Brodman, 1996). Newly
metamorphosed animals and breeding adults are preyed on by raccoons (Huheey and Stupka,
1967) and probably other mammals such as opossums, weasels, and minks (Beachy,
1991a).
P. Anti-Predator
Mechanisms. Egg masses have a thick jelly coat that may afford some protection from
centrarchid fishes and other aquatic invertebrate predators (Ward and Sexton, 1981;
Semlitsch, 1988). There are conflicting reports on whether or not leeches prey on
eggs (Cory and Manion, 1953; Cargo, 1960). Cunnington and Brooks (2000) tested
whether adults breeding in harsher environments containing predatory fishes produced
larger eggs—which might offer some protection to larvae against predation—but
found no significant differences. Larvae possess no direct anti-predator
mechanisms (e.g., Anderson and Petranka, 2003) but are less prone to predation when
refuges are available. One experiment of microhabitat partitioning demonstrated
that spotted salamander larvae tend to occupy refuges at a higher rate and with lower
activity levels in the presence of predators (Brodman et al., 2002).
Spotted salamanders
behave aggressively towards potential predators, head butting and biting attackers
(Dodd, 1977b; Brodie et al., 1979). Adults can assume defensive postures, vocalize,
and produce noxious skin secretions from granular glands located primarily on the
dorsolateral surface of the tail and the paratoid gland on the head (Barach, 1951;
Howard, 1971; Wyman and Thrall, 1972; Brodie, 1978; Brodie et al., 1979). These
secretions are effective deterrents to predation by short-tailed shrews (Blarina
brevicauda; Brodie et al., 1979) and potentially against some reptilian
predators (Barach, 1951; Howard, 1971), presumably because they are distasteful.
Brodie (1971a) reported that the secretions “cause a drying and burning sensation
to the tongue." Nonetheless, adult spotted salamanders have been found in the
stomachs of common garter snakes (Thamnophis sirtalis, Klemens, 1993),
eastern hog-nosed snakes (Heterodon platirhinos; Babbitt, 1932), and
fishes (Salmo trutta; Bishop, 1941b).
Q. Diseases. In
egg clutches collected from several Michigan ponds and raised in the laboratory,
protozoans (Tetrahymena sp.) were found to infect and kill the developing
embryos (Ling and Werner, 1988; see also Petranka, 1998). Evidence of infection was
characterized by swelling of the epidermis, and histological preparations revealed
Tetrahymena sp. concentrations in nervous tissue. Corliss (1954)
originally found Tetrahymena sp. in egg masses and developing embryos, but no
effects were noted. Fungal infections have been observed in egg masses maintained
in the laboratory, as well as in nature, but have only been mentioned anecdotally in the
literature (e.g., Ward and Sexton, 1981).
Kingsley (1880) first
reported the occurrence of natural limb anomalies in spotted salamanders.
Polydactyly (particularly of the forelimbs), syndactyly of the proximal first digits, and
missing digits were common abnormalities observed in juveniles and adults in a New York
population (Wilson, 1976). Cases of melanism, albinism, and partial albinism are
documented in adults, but usually occur in populations at low frequencies (Brandt, 1952;
Hensley, 1959; Smith and Michener, 1962; Husting, 1965; Easterla, 1968; Mount, 1975;
Dyrkacz, 1981). In a Mississippi population, Worthington (1974) found a high
incidence of abnormal coloration, deviant counts of vertebral trunk elements, and limb
anomalies; he suggested high temperatures as a cause, although genetic and other
environmental factors could not be ruled out.
R. Parasites.
Rankin (1937) reported the following parasites from spotted salamanders in North
Carolina: Protozoa—Cytamoeba bactifera, Euglenamorpha
hegneri, Hexamitus intestinalis, Prowazekella
longifilis, Tritrichomonas augusta;
Trematoda—Brachycoelium hospitale, Diplostomulum
ambystomae; Nematoda—spirurid cysts; and Acarina—Hannemania
dunni.
Bolek and Coggins
(1998) reported helminth species infecting the small and large intestine of spotted
salamanders from northwest Wisconsin. Of 20 individuals sampled, 9 were infected
by the nematode Batracholandros magnavulvaris; the trematode
Brachycoelium salamandrae was found in only three individuals but at a
higher mean intensity. Kuzmin et al. (2001) also described a nematode in the lungs
and body cavity of spotted salamanders from northwestern Wisconsin; this nematode,
Rhabdias ambystomae, is the first species of the genus described from
salamanders in North America. Leeches have also been commonly observed on adults
within and exiting breeding ponds. The impact, if any, of helminth or leech
parasitism on spotted salamander population dynamics has not been documented.
4. Conservation. Spotted salamander populations are seemingly widespread
throughout the eastern United States, frequently occurring in nature preserves and state
and federal parks, as well as in relatively undisturbed forests and private lands.
Although present in fragmented suburban areas (Klemens, 1993; Gibbs, 1998a; Wright and
Zamudio, 2002) and sometimes in highly disturbed urban areas (Klemens, 1993; DiMauro and
Hunter, 2002), spotted salamander populations decline with increasing urbanization
(Windmiller, 1996) and mere presence indicates little about long-term population
viability in these habitats. Because populations are vulnerable to human
developments that alter or eliminate habitats and corridors, they are at risk of local
extinction or even local population genetic consequences. Population comparisons
using fluctuating asymmetry in dorsal spot patterns as a correlate of habitat disturbance
showed that a population of breeding adults was significantly more asymmetrical in a
disturbed landscape (in this case, a golf course) than in a nature reserve (Wright and
Zamudio, 2002). These findings suggest that populations in the disturbed habitats
may experience reductions in fitness, potentially due to demographic/genetic bottlenecks
or developmental perturbations (due to chemical applications) as measured by fluctuating
asymmetry, despite their continued persistence in the disturbed habitat.
Connectivity among
patches of breeding habitat will decrease with habitat alteration. Thus, the
importance of individual populations increases because viable populations can rescue
nearby sinks in a metapopulation framework. Semlitsch and Bodie (1998) examined
frequency distribution of wetland sizes and concluded that even small, isolated wetlands
serve as important sources of juvenile recruits. Their loss could result in a
direct reduction of connectivity among remaining populations. Spotted salamanders
are likely to benefit from efforts to maintain connectivity among patches of upland
forest habitats and aquatic breeding sites with sufficient buffer zones (Semlitsch,
1998). Spotted salamanders are more likely to occupy ponds in more forested areas
and those that are adjacent to forest (Guerry and Hunter, 2002). Thus, the
composition and configuration of the landscape surrounding breeding ponds is associated
with the likelihood of spotted salamander presence and population persistence.
Environmental
contamination in breeding ponds may negatively affect juvenile recruitment in spotted
salamanders. Habitat acidification is a concern for this species, as hatching
success and larval development can be reduced in pH ranges of 4.5–5.5 (Pough, 1976;
Pough and Wilson, 1977; Ling et al., 1986; Sadinski and Dunson, 1992; Brodman, 1993),
levels that are not uncommon in the eastern United States (Clark, 1986b; Cook, 1983; Ling
et al., 1986; Sadinski and Dunson, 1992; Petranka, 1998). The number of eggs
present in a pond is positively correlated with alkalinity, as is hatching success
(Clark, 1986b; Petranka, 1998). Ireland (1991) demonstrated that significantly
reduced growth rates were not the result of pH alone but may be a function of anion
concentration or the combined effect of anion and hydrogen ions. Cook (1983) found
no correlation between low pH and embryonic mortality in 13 Massachusetts ponds; in
contrast, Portnoy (1990) found reduced survivorship correlated with acidification in the
Cape Cod region.
Low pH levels can
also reduce growth and survival rates, as well as alter competitive interactions between
larval spotted salamanders and Jefferson salamanders (Brodman, 1993). Acidification
is not the only threat to adult reproductive fitness. Over an 8-yr period in
eastern Virginia, reproductive activity of spotted salamanders declined severely in
breeding ponds with low pH levels and high aluminum, copper, silicon, and zinc
concentrations (Blem and Blem, 1989, 1991). Elevated hydrogen ion and aluminum
concentrations in breeding ponds may also negatively affect hatching success (Clark and
Hall, 1985). In Pennsylvania, the number of eggs present is positively correlated
with pH and pond size, but negatively correlated with cations and silica levels (Rowe and
Dunson, 1993).
During the breeding
season, road mortality is a considerable threat to migrating amphibians. Although
the direct effects of road mortality on population numbers have not been thoroughly
evaluated, several studies show that amphibian densities decrease in response to roadways
(Fahrig et al., 1995; Vos and Chardon, 1998; Trombulak and Frissell, 2000). The
direct effects of roads on mortality may not be the only consideration. In New
Hampshire, embryonic survivorship is reduced in breeding ponds contaminated with road
salt runoff (Turtle, 2000). Roads also affect animal communities by creating
habitat edges that promote invasion of exotic plants (Gaddy and Kohlstaat, 1987) and
exposing salamanders to predation. Moreover, heavily trafficked roads may entirely
block migrating salamanders from reaching a breeding pond (Trombulak and Frissell,
2000). In Massachusetts, Jackson and Tyning (1989) reported that drift fences and
two tunnels installed under a road aided migrating spotted salamanders and substantially
reduced mortality. Migratory routes under roads are not difficult to implement, and
amphibian populations would benefit from local efforts to reduce road mortality during
their short breeding seasons.
Literature references for Amphibian Declines: The Conservation Status of United States Species, edited by Michael Lannoo, are here.
Citation: AmphibiaWeb: Information on
amphibian biology and conservation. [web application]. 2010. Berkeley, California:
AmphibiaWeb.
Available: http://amphibiaweb.org/.
(Accessed: Feb 9, 2010).
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