|Jim Harding, Michigan State University Department of Zoology|
18 July 2013: DeGraaf, Richard M.; Rudis, Deborah D. 2001 citation corrected to DeGraaf, Richard M.; Yamasaki, Mariko. 2001.
|Jeffrey Beane, North Carolina State Museum of Natural Sciences|
Three reviews are also referred to repeatedly, including a management report focused on mitigating the impacts of timber harvesting on four-toed salamanders , an entry on four-toed salamander in a guide to the herpetofauna of Missouri , and a 1997 review of four-toed salamander addressing habitat requirements .
Four-toed salamanders reach maximum lengths of 4 inches (10 cm). Sexual maturity is reached between 2 and 3 years of age. According to a review, four-toed salamanders can live for more than 9 years. They breed in fall, hibernate during winter, and lay their eggs in spring. The small larvae metamorphose following short embryonic and larval stages. Recently metamorphosed juveniles are generally less than 1 inch (2.5 cm) in length .
Seasonality: Adult four-toed salamanders breed in fall. Observations of four-toed salamanders in southern Michigan suggest mating occurs from at least mid-September to late October . A male and female were observed together on 8 October on a site in Arkansas . Four-toed salamanders captured on 2 November bred in captivity starting 6 November. Successful breeding until December led to the conclusion that the end of the breeding season in the wild is due to cool weather, and that breeding may potentially occur during warm days of winter and perhaps early spring . A review suggests that four-toed salamanders may be active at lower temperatures than other salamanders in the same family, possibly remaining active near freezing temperatures. However, it concedes that activity is more common from around 50 °F (10 °C) to more than 68 °F (20°C) and notes observations of four-toed salamanders in Illinois at air temperatures from 45 to 81 °F (7-27 °C) .
Four-toed salamanders hibernate through the winter. Observations in Michigan suggest that they hibernate in groups from November to April . A review notes that four-toed salamanders in Massachusetts hibernate from late November to late March . For information on habitat used during winter, see Cover Requirements.
Four-toed salamanders migrate to nesting areas and lay eggs in spring; individuals in northern populations tend to start these behaviors later than individuals in southern populations [36,95]. In Michigan [13,14,19,88], Rhode Island , and Massachusetts (Wells 2003, cited in ), migration to breeding sites and nesting were observed from late March to May. Four-toed salamanders were active in May in south-central New York and in mid-June in northern Wisconsin . In northern Ohio, four-toed salamanders moved toward nesting ponds in mid-March. The latest nests were observed in the northern portion of the state in mid- to late May, and the earliest nests were observed in the southern portion of the state beginning in early April . Nesting in March and early April has been reported in Virginia [93,94,95], Missouri , and near the Tennessee-North Carolina border . Four-toed salamanders were active in February in Arkansas  and Florida  and have been observed nesting in February in Virginia [94,95] and near the Tennessee-North Carolina border .
Development: It typically takes about 40 to 60 days for four-toed salamander eggs to hatch. The four-toed salamander's embryonic period under artificial conditions is typically 40 to 45 days [6,50]. The embryonic period was 38 days in a nest in Michigan; eggs were laid about 19 April and hatched on 27 May . On sites in New York, the incubation period ranged from 52 to 60 days (Bishop 1941, cited in ). A nest in the coastal plain of Virginia had an incubation period of 61 days . Blanchard  suggests that embryonic developmental rate is influenced by moisture and temperature. For information on development in the embryonic stage, see Babcock .
Larvae generally mature in 6 weeks or less [8,10,24]; the rate may be influenced by food availability  and the presence of predators . Larvae metamorphosed from 23 to 27 days after hatching in an artificial environment and metamorphosed 21 days after hatching in a pond on the George Washington National Forest, Virginia. All larvae in the pond had metamorphosed by 27 June . A review notes the occurrence of recently metamorphosed juveniles (metamorphs) and larvae on 5 August in Illinois . An experiment found development rate did not differ between larvae receiving 1 ml of food every other day and those receiving 3 ml of food every other day . In contrast, larvae in another experiment grew larger and faster (P<0.001) when fed 5 ml of food every other day than larvae fed 1 ml of food every day . Another experiment found that the presence of a predator began reducing growth rate about 27 days into the larval period . For information on larval development, see Blanchard  and Chalmers and Loftin .
Metamorphosis of four-toed salamanders occurs when larvae reach about 0.7 to 0.9 inch (1.8-2.3 cm) in total length . The average size of larvae prior to metamorphosis in a pond on the George Washington National Forest was 0.7 inch (1.75 cm) . According to reviews, metamorphs average about 0.75 to 1 inch (2.0-2.5 cm) in length [17,59]. Recently metamorphosed four-toed salamanders in Michigan averaged 0.5 inch (1.3 cm) in body length (not including tail) on 30 July and grew to an average of just under 0.8 inch (2.0 cm) in body length by early November .
In less than 2 years, subadult four-toed salamanders can reach adult size, typically from 2.5 to 3.5 inches (6-9 cm) in length . Female four-toed salamanders tending nests in coastal and south-central Virginia ranged from 2.4 to 3.7 inches (6.1-9.5 cm) in length and averaged 3.1 inches (7.8 cm) . The length of females attending nests in eastern Wisconsin averaged 3.3 inches (8.5 cm) and ranged from 2.6 to 3.7 inches (6.6-9.5 cm) . Adult female salamanders at 3 sites near Ann Arbor, Michigan, were an average of 0.4 inch (9.5 mm) longer than males . The largest four-toed salamander observed in Missouri was 3.2 inches (8.1 cm) long . The record length of a four-toed salamander is 4 inches (10.2 cm) (Conant and Collins 1991, cited in ). Several sources investigate the variation in the proportional length of the four-toed salamander's tail at different ages and in varying conditions [8,10,16].
Reproductive maturity is reached between 2 and 3 years of age [16,94]. Observations from southern Michigan suggest that four-toed salamanders begin breeding about 2 years and 4 months after hatching . Wood  suggests that some four-toed salamanders may begin breeding at more than 2.5 years of age, about a year after reaching adult size.
Movement: The distances traveled by dispersing or migrating four-toed salamanders are unknown. A review reports four-toed salamanders 498 feet (152 m), 650 feet (198 m), and 660 feet (201 m) from nesting habitat in Massachusetts. In Quebec, a four-toed salamander was found 235 feet (72 m) from nesting habitat . The manner in which four-toed salamander populations fluctuated at 11 ponds in Great Smoky Mountains National Park, on the border of Tennessee and North Carolina, suggests some level of interpond dispersal. Ten of these ponds occurred in 2 neighboring watersheds and averaged less than 3.4 miles (5.5 km) from each other . A female Jordon's salamander (Plethodon jordani), a member of the Plethodontidae family, that was displaced 197 feet (60 m) from her capture site returned to within 23 feet (7 m) of her capture site within 12 hours .
Reproduction: Female four-toed salamanders lay clutches of up to about 50 eggs in solitary or group nests. Some females brood the nest for some or most of the embryonic period. Females do not breed every year. Egg hatching rates can be low and apparently increase when brooded. Juvenile sex ratios in southern Michigan were near 1:1, with females comprising 56.9 to 57.8% of collected individuals .
Four-toed salamander nests contain eggs of one or more females, with less than 50 eggs comprising individual clutches. Observations of four-toed salamander nests in Michigan suggest that single clutches were comprised of less than 40 eggs . In eastern Wisconsin, nests of 40 eggs or less were considered single clutches . The occurrence of 80 ova in a mature female led the researcher to consider this the maximum size of a single clutch in south-central and coastal Virginia . The number of eggs in nests observed in New York averaged 24.4 and ranged from 12 to 65 . In south-central and coastal Virginia, 40% of nests had 30 to 50 eggs, and nest size ranged from 6 to 868 eggs . In eastern Wisconsin, the number of eggs in nests ranged from 17 to 200 eggs and averaged 51.3 eggs . Communal nests of over 500  and 800 eggs  in the coastal plain of Virginia and over 1,000 eggs in southern Michigan  have been documented. The proportion of nests considered communal ranged from less than 5% near the Tennessee-North Carolina border  to 46% in eastern Wisconsin . Hypotheses for the occurrence of communal nests include limited nesting sites  and dilution of predation risk .
Four-toed salamanders often brood their nests. The presence of fungi-inhibiting bacteria on four-toed salamander skin  and possible consumption of fungus-infested eggs by attending females  imply that the brooding process may reduce the risk of loss of an entire nest to fungi. Due to the lack of response to predators and possible low palatability of eggs (see Predators), nest defense is not considered a likely explanation for brooding behavior. In eastern Wisconsin, half of the nests were attended by a single female and half were unattended . In southern Michigan 5 nests were unattended, 10 nests were attended by 1 female, 2 nests were attended by 2 females, and 1 nest was attended by 3 females . Successive brooding of nests by females was observed in one study in northern Virginia  but not in a second study . In southern Michigan, solitary nests were generally tended by the female until hatching , but in coastal and south-central Virginia 60% of nests were abandoned . Communal nests had lower desertion rates than solitary nests at Shenandoah Mountain in Virginia . Females tending group nests apparently do not brood the other females' eggs and spend only slightly less time on their eggs than females attending solitary nests . Communal and solitary nests in artificial habitat had similar reproductive successes, averaging 34.7 and 33.7 hatchlings/female, respectively . Brooding behavior does not appear to have significant energy costs [48,50].
Hatching rates can be low but apparently increase when the eggs are brooded. Hatching rates at 2 ponds at Shenandoah Mountain in Virginia were 8.9% and 20.8%. Survival rate of embryos before desertion was significantly (P<0.001) higher than after desertion, and eggs tended by a female for any duration had significantly (P<0.01) higher survival than eggs that were never observed with a brooding female . Duration of brooding at these sites may or may not be correlated with embryonic survival [47,48].
Not all reproductive females breed every year. During a 10-year period, 44% of females in northern Virginia skipped breeding in one or more years. Females that skipped breeding grew significantly (P<0.037) more than females that reproduced. Due to increased size, females that skip breeding could potentially lay larger clutches in subsequent nesting seasons . In a combined laboratory and field study on the George Washington National Forest, the amount of food provided had significant (P=0.025) impacts on the number of females that returned to breed the following year . Rainfall may also influence the number of females that breed [27,50]. Precipitation near the Tennessee-North Carolina border was positively related (P=0.12, r=0.78) to the number of nesting females .
Breeding behavior in a laboratory environment was described by Blanchard  and Branin . Branin  noted that breeding activities occurred primarily at night, and some four-toed salamander aggregations included over a dozen individuals. A brief summary of breeding behavior as well as information on conspecific aggression and voluntary tail dropping is included in Daniel . Carreno and others  found no evidence for kin recognition in four-toed salamander larvae, while evidence of sibling recognition in larvae and maternal recognition of eggs is described by Harris and others .PREFERRED HABITAT:
General: Thurow  describes 4 general types of four-toed salamander habitats with closed-canopy forest and slow or still water:
Although four-toed salamanders disperse through areas not generally considered suitable habitat, presence of forested habitat with adequate cover could promote dispersal. Four-toed salamanders have been observed crossing roads, near pastures, and in forests with open canopies. Observations in Arkansas led the author to speculate that four-toed salamanders might have used small streams and moss mats to travel through a 10-year-old loblolly pine plantation . The possibility of at least some dispersal between ponds in Great Smoky Mountain National Park was attributed in part to the undisturbed nature of the area .
Four-toed salamanders generally avoid the borders between forests and more open cover types. In Kentucky, four-toed salamanders were observed in the interiors of bottomland and upland habitats but not by the edges of these communities, which bordered reclaimed grasslands . In Maine, four-toed salamanders were rarely captured within 230 feet (70 m) mature forest-conifer plantation edges or in mature forest-regenerating clearcut edges . Few four-toed salamanders were captured in the ecotone between mesic hardwood bottom and a xeric upland sand ridge community in Georgia . Other factors that likely influence four-toed salamander abundance, such as distance from suitable breeding habitat, were not discussed in these studies.COVER REQUIREMENTS:
Four-toed salamander larvae need water to develop properly. Out of water, their gills do not reduce in size and the larvae grow very little, if at all . Thus, water bodies occupied by four-toed salamander larvae need to persist through the larval period, which can extend into August in some areas (see Life and Annual Cycles) .
Four-toed salamander larval ponds and pools lack fish ([3,10,17,59,88], also see Predators), and are often temporary ponds. Salamander species that exploit these ephemeral ponds avoid predators, such as fish, associated with permanent water . In southeast Michigan, four-toed salamanders were only observed in temporary ponds .
According to a review , the highest water temperatures observed in occupied four-toed salamander habitats was 67 °F (19.5 °C) in Illinois and from 70 °F to 73 °F (21-23 °C) in Virginia. An egg mass that was 76 °F (24.5 °C) was observed in coastal Virginia. The author suggests water bodies that exceed 77 °F (25 °C) would not provide suitable habitat but concedes it is possible that southern ecotypes could tolerate higher temperatures .
Water bodies occupied by four-toed salamander larvae are still or slow-moving [36,88,95]. In Virginia, streams occupied by four-toed salamander larvae had flow rates less than 0.2 mile (0.3 km)/hour . In southeastern Missouri, four-toed salamander eggs were laid near pools in streams but not near relatively fast-moving water . In Maine salamanders generally did not nest along shorelines with flowing water . The author of a review notes that he has never observed four-toed salamander larvae in large streams . Several studies cited in Berger-Bishop and Harris  indicate faster larval growth rates in ponds compared to streams for red salamanders (Pseudotriton ruber), brook salamanders (Eurycea spp.), and dusky salamanders (Desmognathus spp.), all of which are in the same family as four-toed salamanders.
Characteristic four-toed salamander larval habitat has been described as shaded [3,10], but four-toed salamanders do occur in open-canopy pools [83,87,95]. Shade likely cools water temperatures and is probably associated with shorelines with moss and downed wood used for nesting . Four-toed salamander larvae may become heat stressed in ponds with temperatures of 77 °F (25 °C) or higher , so reduced shade could result in thermal stress in larvae. Reduction in shade also has the potential to increase mortalities due to increased UV-B exposure, which reduces survival in embryonic and larval stages of some salamanders .
Shade is also associated with greater evapotranspiration rates, so shaded ponds may have shorter hydroperiods than open ponds. All 3 ponds with four-toed salamander breeding activity documented by Skelly and others  had open canopies. Cool, shaded water had lower larval salamander growth and survival rates that were mitigated by the addition of high quality food. Hydroperiods were estimated as 2.5 weeks shorter following succession to a closed canopy .
Little is known regarding the acid sensitivity of adult four-toed salamanders, their larvae, or their eggs. The pH of a baldcypress pool used by four-toed salamanders in the Virginia coastal plain was 5.0 . In Maine, marshes, swamps, and low-acidity fens were used by four-toed salamanders, but high-acidity fens and bogs were not used .Terrestrial habitats:
Ground cover and coarse woody debris: Four-toed salamanders are often found under moss, logs, bark, or leaf litter on the forest floor [17,32,59,80,88]. Of all four-toed salamanders found in mature upland conifer forest of Wisconsin from August to late October, 55% were found under shelter on the soil surface, 9% were exposed on the forest floor, and the rest were under ground. Four-toed salamanders were found on organic soil (45%), rotting wood (23%), leaf litter (18%), and moss (14%) . In Arkansas, individuals were found under moss on a decaying shortleaf pine branch, in hardwood and hardwood-pine leaf litter, and under logs. According to Saugey and Trauth , most records of four-toed salamanders in the Arkansas National Heritage database were of individuals found under moss mats or logs . In Missouri, four-toed salamanders have been found under rocks and rotten logs and in leaf litter in seepage areas .
Salamanders in the Plethodontidae family, and amphibians in general, are associated with forest floor litter and coarse woody debris, probably due to their need for moist, cool, wind-free microhabitats [5,33,37,55,69,71,75,77,78]. The amount of moderately to well-decayed coarse woody debris on dry sites in western North Carolina was positively (P=0.01) associated with Plethodontid salamander numbers . Salamander abundance in the Blue Ridge Mountains of North Carolina was positively (P≤0.05) correlated with amount of coarse woody debris . In eastern Georgia salamander abundance was negatively (P=0.03) correlated with percent cover of bare ground . Recolonization of southern Appalachian clearcut sites by Plethodontid salamanders 4 to 6 years after timber harvest was associated with the development of the litter layer . In deciduous forest of New York, litter depth was positively (P=0.019) related to eastern red-backed salamander (Plethodon cinereus) activity . In Maine, salamanders as a group tended to occur in areas with more hardwood litter, less bare soil, and more cover of snags, stumps, and snag and stump root channels . In hardwood and balsam fir (Abies balsamea) stands in New Hampshire, herpetofaunal diversity and evenness were positively correlated (r=0.82) with litter depth . Litter and coarse woody debris also provide habitat for the arthropods that comprise the four-toed salamander's diet [58,71]. See Food Habits for more information on four-toed salamander prey species.
Four-toed salamanders also use subterranean shelter, possibly most frequently in the winter. In mature upland conifer forest of Wisconsin, 36% of the four-toed salamanders observed from August to late October were found under the soil surface, typically in rotten stumps . Observations of four-toed salamanders in late autumn and early spring suggest that individuals overwinter in cavities in rotten wood, channels left in soil by decayed plant roots, and hollows and crevices in the ground under leaf litter . A review notes four-toed salamander's use of subterranean habitats "in unfavorable weather" , and another review states that holes, channels, and crevices in the ground are used by overwintering four-toed salamanders . When overwintering in these microsites, four-toed salamanders may occur in groups, which may include other species such as spring peepers (Pseudacris crucifer), western chorus frogs (Pseudacris triseriata), wood frogs (Rana sylvatica cantabrigensis), Jefferson salamanders (Ambystoma jeffersonianum), and eastern newts (Notophthalmus viridescens) 
Canopy cover: Forest stands with metamorphosed four-toed salamanders vary in canopy cover but typically are shaded enough to support moss and/or provide leaf litter and coarse woody debris. In Arkansas, four-toed salamanders were found in stands with dense hardwood understories and also in stands with open canopies following thinning and midstory-removal harvest. Although several of the stands were in or near disturbed habitats or close to roads and/or pastures, important ground cover characteristics were prevalent on all sites . In Maine, salamanders as a group tended to occur in areas with more cover, less ambient light, and more hardwood and conifer canopy than most stands . Salamander abundance has been positively associated with canopy cover [46,55] and basal area  following timber harvests.
Canopy cover influences groundlayer characteristics. Open-canopied forests are generally associated with drier, hotter forest floors than closed-canopied forests [20,46,85]. Temperatures at the litter-soil boundary in a clearcut watershed in the southern Appalachians were higher than in adjacent forested watershed and had average daily maximum temperatures over 104 °F (40 °C) in the summer . In low-elevation hardwood forests of southwest Virginia, soil temperatures were hottest in treatments with the least canopy cover. Leaf litter in treatments that did not impact the canopy retained more moisture than leaf litter in the clearcut, leave-tree, and shelterwood treatments .Nest sites: Four-toed salamanders typically lay their eggs in moss, other vegetation, decayed wood, or leaf litter that is above or very near water, so larvae can drop or wriggle into suitable habitat. Female four-toed salamanders may return to the same pond every time they lay eggs, and nests have been observed in the same locations in different years. Females returned exclusively to the pond where they laid their first clutch during a 10-year period in northern Virginia . Five of the nest sites used on a site in southern Michigan in 1981 were the same as nest sites used in 1980 , and there is evidence for reuse of nest sites in Maine (Chalmers 2004, cited in ).
Association with water: Due to the need for recently hatched four-toed salamander larvae to reach appropriate habitat, nests are located very close to water, typically within inches of the water surface on substrates overhanging water. The inclusion of hydrologic variables in the model created to predict use of wetlands and nesting sites by four-toed salamanders in Maine suggests the importance of larval habitat characteristics in nest site selection . Near Ann Arbor, Michigan, nests were located near or 2.5 to 7 inches (6-18 cm) directly over water . Near Ithaca, New York, nests were 3 to 6 inches (8-15 cm) above the water, despite water levels dropping between egg laying and the survey. In Wisconsin nest sites were 2.8 to 7.5 (7-19 cm) above the surface . A nest observed in Pennsylvania was 1.4 inches (3.5 cm) above the surface of Hickory Run Lake . All nests on a site in southern Michigan were located above water on islets . Nests were not found in moss on logs in areas where the water dried out . Only nests in moss clusters beside pools were productive in Missouri . The locations of many nests suggest that females commonly swim to nesting sites [14,19,25,95].
Eggs are also laid on shorelines, typically on steep slopes above the water . Steep slopes from nests to water, characteristic of four-toed salamander nest sites in Maine, likely allowed larvae to move to water easily. Structures along shorelines that resulted in steep gradients from nesting substrates to water included wood, earthen banks, boulders, fern litter, and live vegetation such as red maple, common winterberry (Ilex verticillata), and tussock sedge (Carex stricta) .
Salamander nests are located above water of varying depths. The water depth below four-toed salamander nests on a site in Wisconsin was from 0.6 to 4.7 inches (1.5-12 cm) . In Virginia, the water near nests ranged from a few inches to several feet deep . In Maine, deep near-shore water and deep maximum basin depth were characteristic features of four-toed salamander nest sites .
Substrate: Four-toed salamanders typically lay their eggs in moss but lay in other substrates that provide adequate protection from desiccation, such as rotten wood, leaf litter, and clumps of grasses (Poaceae), sedges (Carex spp.), and/or rushes (Juncus spp.). Mosses provide concealment from predators and a moist environment with comparatively consistent temperatures and pH compared to exposed areas [25,88,90]. Mosses may have properties that reduce the likelihood of eggs being infected with bacteria or fungi . On a site in southern Michigan, 89% of nests in one year and 93% of nests in the following year were in clumps of sphagnum moss . All 32 nests observed in swamps near Ithaca, New York, were covered in 0.75 to 2.5 inches (2-6 cm) of loose moss that was growing on fallen and rotting logs . A nest observed in Pennsylvania was 3.2 inches (8 cm) below the surface of a moss mat . Seventy-eight percent of nests in coastal Virginia were laid above rhizoids or roots, with nearly 20% on the rhizoids of mosses and liverworts or on sedge roots . Four-toed salamander nests in wetlands in Maine occurred in deep sphagnum and other mosses on a variety of substrates including wood, boulders, earthen banks, and clusters of common winterberry stems .
Four-toed salamanders use several genera of mosses for nesting. Use of sphagnum is widespread [19,42,95]. In some areas, such as southern Michigan , the majority of nests were in sphagnum. Four-toed salamander nests have be found in Climacium spp. mosses in Missouri , New York , and Virginia . Use of Thuidium and Mnium spp. mosses for nesting has been reported in New York  and Virginia . Several other mosses including species in the genera Atrichum, Entodon, and Leptodictyum were used for nesting in Virginia .
Other substrates that prevent eggs from drying are also used for nesting [17,88]. Clumps of grass, sedges, and rushes have been reported as nesting sites [17,19,36,47,88]. In Maine, the only nests not located on mosses were on tussock sedge . Liverworts, such as those in the genera Lophocolea, Pallavicinia, and Scapania, were occasionally used for nesting in Virginia . Four-toed salamanders have been observed nesting in leaf litter in Missouri [36,53] and Michigan  and in rotten wood in Virginia , Maine , and Michigan . However, shorelines not used for nesting in occupied wetlands in Maine generally had woody debris .
Vegetation: In Maine, plant species that occurred along the shorelines of occupied wetlands were bluejoint reedgrass, sphagnum, white meadowsweet (Spiraea alba), steeplebush (Spiraea tomentosa), and sensitive fern. However, white meadowseet and leatherleaf (Chamaedaphne calyculata) did not generally occur at nesting sites. Sheep-laurel (Kalmia angustifolia) was generally absent from nesting sites and occupied wetlands .FOOD HABITS:
Moisture levels may affect four-toed salamander foraging time [37,58]. In Shenandoah National Park, Virginia, the number of prey captured by eastern red-backed salamanders, a Plethodontid insectivore, was significantly (P<0.0005) positively correlated with the amount of rain in the previous 3 days. In 3-day periods with no rain, 14% to 23% of eastern red-backed salamanders did not capture any food, while all individuals captured some prey in 3-day periods with more than 1.6 inches (41 mm) of rain. Thus, retreats such as underground burrows that are used during dry conditions do not appear to provide access to prey . Adults may be active at lower humidity levels than juveniles, due to juveniles's greater susceptibility to drying .
The extent to which reduced foraging opportunities impact four-toed salamanders is unknown. Many Plethodontid salamanders have low food requirements, probably due to their low metabolic rate, small size, and cool habitats. An Allegheny Mountain dusky salamander (Desmognathus ochrophaeus) weighing just over a gram reproduced on only 12 mealworms/year (Fitzpatrick 1973a, cited in ), and 74% of slender salamanders (Batrachoseps spp.) kept at room temperature survived over a year without food (Feder, unpublished data cited in ). However, increased food availability has been associated with higher percentage of reproductive four-toed salamander females .PREDATORS:
Although four-toed salamander eggs are eaten by several species, they appear relatively unpalatable to some predators. Predators of four-toed salamander eggs include beetles such as Pterostichus spp., centipedes (Chilopoda), and amphibians such as eastern newts [22,54]. In a laboratory experiment, 2 beetles ate 22% of four-toed salamander eggs in 12 days, as did 2 centipedes, while 3 eastern newts ate 8% of the four-toed salamander eggs in the same period . Stream beetles ate significantly (P=0.009) more Ocoee salamander (Desmognathus ocoee) eggs than four-toed salamander eggs, despite puncturing them at the similar frequencies . Four-toed salamander adults have also been observed eating four-toed salamander eggs, although it is uncommon (Harris and others 1995, cited in ).
Few predators of four-toed salamander larvae and adults have been documented, but several adult parasites have been noted. The most commonly documented predators of four-toed salamander larvae are eastern newts [22,51,91]. In an experiment, four-toed salamander larval survival and growth rates were lower in treatments with eastern newts than in treatments lacking eastern newts . Fish have only been documented eating larvae in a laboratory environment, likely due to the lack four-toed salamanders cooccurring with fish in the wild . The only report of predation on an adult was by a pygmy rattlesnake (Sistrurus miliarius) in west-central Arkansas . A review notes that larger salamander species are likely predators or competitors of four-toed salamanders . Parasites of four-toed salamander adults include a nematode (Cosmocercoides dukae), a fluke (Gorgoderina bilobata) , and a protozoan (Haptophrya michiganensis) .MANAGEMENT CONSIDERATIONS:
Threats: According to reviews, major threats to four-toed salamanders are the loss, degradation, and fragmentation of habitat . Reduction of hydroperiods, decreases in pH of ponds, and increases in water temperature and sedimentation can have negative impacts on four-toed salamander larvae [17,88]. For more information on the direct and indirect effects of changes to water quality, see Bol and others . Removal or compaction of living and dead ground cover limits the availability of adult habitat. Fragmentation could restrict movement to breeding grounds and between populations . Roads may pose dispersal barriers and result in substantial mortality if located along migration routes [17,34,83]
For speculation on possible effects of climate change on four-toed salamanders in Nova Scotia, see Herman and Scott .
Forest management: Reduced cover of canopy trees, leaf litter, and well-decayed coarse woody debris likely contribute to the negative response and long recovery times of salamanders after timber harvesting. Detrimental effects of tree harvesting on salamanders have been documented in the southern Appalachians [5,46,55,75,76], Pennsylvania , and New York . In low-elevation hardwood forests of southwestern Virginia, terrestrial salamanders were significantly reduced following a clearcut (P=0.001), a leave-tree (P=0.001), a group selection (P=0.005), and 2 shelterwood (P=0.005) treatments, while terrestrial salamander abundance did not change on untreated sites or sites where the understory was removed with herbicide. Canopy cover and leaf litter cover were greatest on the control and the understory removal treatments. These plots also had higher leaf litter moisture and cooler soil temperatures . In Pennsylvania there was a significant positive relationship (P=0.01) between retained basal area of harvested stands and salamander species richness. The relative abundance of salamanders also increased significantly (P<0.001) with increasing basal areas greater than 15 m²/ha . In the southern Blue Ridge Mountains of North Carolina, Plethodontid salamanders were reduced by 30% to 50% in the 1st year and nearly 100% by the 2nd year following clearcutting. Recovery of salamanders began 4 to 6 years following timber harvesting and seemed correlated with litter layer development. Projections based on up to 15 years of data collected after timber harvesting in the southern Blue Ridge Mountains suggest that salamanders would reach predisturbance levels from 20 to 24 years following clearcutting . Estimated recovery times in western North Carolina were more than 50 years [75,76]. In hardwood stands in New York, recently disturbed stands had significantly (P<0.05) fewer eastern red-backed salamanders than adjacent old-growth controls, while abundance was similar on old-growth and 60-year-old second-growth stands . DeMaynadier and Hunter  provide a comprehensive review of salamander responses to timber harvesting based on the literature as of 1995.
Effects of logging on four-toed salamanders may be mitigated to varying extents by minimizing the extent of thinning [17,81]; incorporating undisturbed buffer strips around wetlands, ponds, and streams; reducing impacts to microhabitats such as moss and grass tussocks, leaf litter, and coarse woody debris; and reducing soil compaction by limiting disturbance to periods when soils are frozen or dry [17,34,75,83]. For specific recommendations for timber harvesting in four-toed salamander habitat in the Northeast, see Bol and others .Protecting breeding habitat and surrounding mature forest has been suggested to maintain salamander populations from disturbance [25,34,69,75]. Several sources note the importance of maintaining complexes of mature forests used by adults and the pools and wetlands used by larvae in a mosaic that allows for movement between adult and larval habitat as well as dispersal between nesting areas [17,25,27,69].
|Prescribed fire on the Nantahala National Forest, North Carolina. USDA Forest Service photo.|
Several of the studies discussed below have limitations due to small sample sizes, short-term study periods, little or no replication, no prefire data, and/or no controls [77,82]. Reviews of the effect of fire on amphibians from 1999  and 2003  are frequently cited in this section.DIRECT FIRE EFFECTS:
However, fewer captures of salamanders on burned sites compared to unburned sites [38,44,69,70] and mortalities of eastern red-backed salamanders sheltering under dead logs  indicate the potential for negative effects of fire on adult four-toed salamanders. Four-toed salamanders have not been observed on recently burned sites. On the Atlantic coastal plain in Maryland, 20 four-toed salamanders were captured in unburned pine-mixed-hardwood habitat, while none was captured in a repeatedly burned loblolly pine site. This difference was statically significant (P<0.01). The burned site was the same distance as the unburned site from a marshy area likely used for nesting, but it was 790 feet (240 m) farther from the nearest wetland than the unburned site . Unmanaged mixed-hardwood stands had higher amphibian relative abundance and surface activity than 2 regularly but infrequently burned pine plantations in South Carolina .
According to a review, aquatic life stages of salamanders are typically sheltered from direct effects of fire, so mortality is rarely documented . However, larval mortality could occur if water was heated to lethal temperatures or if temperatures reached stressful levels, likely above 77 °F (25 °C) , for several hours. Heat can also lead to lethal chemical changes in water .
Fires occurring during inactive periods such as late summer or winter would likely be least detrimental to four-toed salamanders, since use of underground burrows is more common during these periods (see Cover Requirements). The use of moist sites suggests that four-toed salamander eggs are seldom exposed to lethal fires. The higher surface-to-volume ratio of juveniles makes them more susceptible to drying [37,88]. Therefore, juveniles may be even more restricted to moist environments than adults [5,37] and may be exposed to fire less often than adults.HABITAT-RELATED FIRE EFFECTS:
Effects on aquatic habitat: Fire can have beneficial or detrimental impacts on the availability of nesting sites and larval pools, wetlands, and ponds. According to a review, fires can prevent succession of aquatic habitats such as bogs to hardwood forest; succession would reduce water levels and, presumably, available larval habitat . Reduction in vegetation also reduces evapotranspiration, raising water levels and providing more potential larval habitat . Woody debris that falls following fire can create new pools for nesting and larval habitat . However, consumption of nesting vegetation and other substrates by fire would likely negatively impact habitat, particularly because of four-toed salamander's apparent fidelity to nesting ponds .
If erosion and sedimentation occur following fire, availability of breeding sites may be reduced temporarily. The California newt (Taricha torosa), a species that nests in deep, slow-moving water, laid fewer egg masses following a chaparral wildfire that reduced the number of runs and pools in a nesting stream . A review suggests that impacts of sedimentation on nesting habitat may be greater in streams with low gradients , such as those used by four-toed salamander larvae . According to a review, sediment in streams can reach 100 times typical levels and persist for over 10 years following severe fires. Nevertheless, effects of fire and the resulting sedimentation on pond-breeding amphibians could be negligible in most circumstances .
Characteristics of larval habitats that may be impacted by fire include temperature, nutrient input, productivity, pH, evaporation rate, morphology, and water-holding capacity [34,74,77]. Reviews suggest that fire typically results in a temporary increase in pH [64,72]. This could potentially benefit acid-sensitive species . Although four-toed salamanders can occur in acidic water, they may be sensitive to low pH (see Aquatic habitats). Characteristics of temporary ponds, including pH, were not significantly altered by prescribed fire on low-elevation sites of South Carolina .Effects on terrestrial habitat
Fire often reduces leaf litter and other ground cover in salamander habitat [43,61,62,69,71,84]. A mixed pine-hardwood site occupied by four-toed salamander had significantly greater litter depth than an unoccupied burned site on the Atlantic coast plain of Maryland . Similar changes have been observed following fire in other areas within the four-toed salamander's distribution. In south-central Pennsylvania, average litter cover the spring following a fall fire was 52.3%, and the litter layer averaged 0.5 inch (1.15 cm) deep, compared to 76.8% average litter cover and an average litter depth of 2.8 inches (7.15 cm) on an adjacent unburned site. Living ground cover was also reduced, with the unburned site having 13.7% cover of shrubs and mosses and the burned site lacking living ground cover. On the burned site cover of mineral soil was 27.6%, while on the unburned site it was only 0.1% . In bottomland hardwood forests in Georgia, litter was significantly deeper (P<0.025) and percent cover of bare ground was significantly smaller (P<0.003) on unburned plots compared to burned plots . Prescribed fires and understory removal followed by prescribed fires resulted in significantly (P<0.0001) reduced leaf litter compared to untreated plots in southern Appalachian upland hardwood forest in North Carolina .
Loss of leaf litter may also affect four-toed salamanders by reducing the availability of prey. If four-toed salamanders feed only in wet litter, as is the case with eastern red-backed salamanders , reduction of leaf litter likely reduces foraging habitat. Reductions in leaf litter associated with timber harvesting resulted in a decline in the abundance of macroarthropods in the leaf litter in the southern Appalachians . See Food Habits for a discussion of the possible repercussions of reduced food availability on four-toed salamanders.
The litter that accumulates within a few years of a disturbance apparently provides adequate habitat for salamanders, suggesting that impacts to certain four-toed salamander habitat features may be short lived. In northern hardwoods of New Hampshire the amount of leaf litter increased from nearly zero to as much as 20% of precutting levels within 4 years of clearcutting . Plethodontid salamanders in the southern Blue Ridge Mountains of North Carolina were detected in clearcut stands 4 to 6 years after harvesting, which coincided with development of the litter layer . Differences in leaf litter depth between burned and control sites in a southern Appalachian deciduous forest in eastern Tennessee were no longer significant 3 years following fire . Living ground cover was similar in burned and unburned vegetation by the end of the summer following a fall fire in south-central Pennsylvania .
Moss provides cover, foraging habitat, and nesting habitat for four-toed salamanders on many sites, so the impact of fire on moss will likely influence four-toed salamanders. Recovery of moss following fire varies with species [2,63]. For instance, juniper haircap moss (Polytrichum juniperinum) can colonize sites within 4 years of fire, while late-successional species such as splendid feather moss (Hylocomium splendens) may take over 50 years to reach prefire levels. A bog in western Canada experienced substantial colonization of upright haircap moss (Polytrichum strictum) within 2 years of fire, with greater colonization in low, wet areas. Colonization of upright haircap moss appeared to facilitate the establishment of sphagnum mosses . Mosses often used by four-toed toed salamander are discussed in Nest sites.
Effects on coarse woody debris: Reduction in coarse woody debris due to fire may negatively impact four-toed salamanders. A loblolly pine stand in Maryland that was repeatedly burned under prescription had significantly (P<0.05) less coarse woody debris and significantly (P<0.01) fewer four-toed salamanders than an unburned mixed pine-hardwood stand .
The consistent moisture levels of coarse woody debris may provide refuge for salamanders following fires that consume substantial amounts of leaf litter. Presence of coarse woody debris following disturbance may be especially important on dry sites [71,75]. As of 2008, information on loss of large amounts of coarse woody debris from wildfire in salamander habitats in the eastern United States was lacking; most of the studies described here investigate the impacts of low-severity fires [43,61,71].
Some fires increase coarse woody debris and could increase nesting habitat by blocking streams, forming pools and/or providing substrates where females can lay eggs. Following a mixed-severity wildfire in western Montana, potential long-toed salamander (Ambystoma macrodactylum) breeding sites increased due to fallen trees blocking intermittent streams and creating new pools .
Effects on canopy cover: Increases in solar radiation could reduce habitat quality for four-toed salamanders (see Canopy cover). The significant (P<0.05) reductions in canopy cover and deciduous tree density on repeatedly burned loblolly pine sites in Maryland were suggested as possible explanations for four-toed salamander absence from the repeatedly burned sites . Increased light may reduce habitat quality due to higher temperatures, greater UV-B exposure , and drier vegetation around ponds. However, increased productivity and longer hydroperiods due to reduced evapotranspiration following reduction in canopy cover could potentially benefit salamanders . For more information, see Aquatic habitats.
Landscape-scale considerations: Reduction in four-toed salamander microhabitats could interfere with successful migration into nesting ponds and/or dispersal between populations. Desiccation and predation likely pose greater risks to salamanders migrating or dispersing through burned habitat than to those in unburned habitat [20,77,84]. The consistent use of the same nesting ponds by four-toed salamanders in northern Virginia  and the generally low mobility of salamanders suggest obstructions to movement could compromise the long-term persistence of four-toed salamanders at a given site .
Landscape-scale factors such as distance to water and topography may have greater influences on salamanders than fire. Distance to water and mesic aspects were significantly (P≤0.032) associated with eastern red-backed salamander captures in oak-dominated forest in the Virginia Piedmont, while fire treatments were not . Slope location had more impact on salamander abundance in southwestern North Carolina than prescribed fire treatments. This may be partly related to differences in severity on different parts of the slope (see next paragraph) .
Fire Characteristics: Although high-severity fires are rare in the moist habitats occupied by four-toed salamanders (see Fire Ecology), they would likely have large, long-term impacts. Little of the current information on salamanders' response to fire is based on high-severity fires [38,71]. Although a fire in southwestern North Carolina was severe in upland areas, in midslope and riparian areas the fire consumed comparatively little vegetation . The most severe fire in a southern Appalachian upland hardwood forest resulted in 25% tree mortality and insignificant impacts on coarse woody debris or duff depths . High-severity fires would be more likely to consume coarse woody debris, burn deep into litter and duff, and reduce canopy cover. Many shelters would likely be consumed, leaving salamanders more vulnerable to overheating or desiccation. After a fire in the Jemez Mountains of New Mexico, 24-hour average daily temperatures in potential salamander shelters were much higher in areas burned in high-severity and moderate-severity fires than those burned in low-severity fires . For a discussion of the effect of canopy removal and ground disturbance on four-toed salamanders, see Forest management.
It has been suggested that large wildfires that occur during dry periods, when salamanders are generally limited to damp areas or underground burrows, may have less impact on salamanders than prescribed fires that are more likely to occur in moist or humid conditions when salamanders are active . Fire during periods of four-toed salamander activity, such as the spring migratory and nesting and fall breeding seasons, could result in greater mortality due to more individuals being caught in exposed areas or migrating through recently burned areas [77,84]. However, season of burning (spring, winter, or summer) did not influence eastern red-back salamanders or amphibians in general in shelterwood-harvest oak forests of the Virginia Piedmont .
Frequent fires are likely to have greater impacts on four-toed salamanders and their habitat than single or infrequent fires [38,69]. A loblolly pine site that burned 5 or 6 times in 11 years had significantly fewer four-toed salamanders than a nearby unburned pine-mixed hardwood site. Repeated burning likely explains the significant (P<0.05) reductions in habitat characteristics important to salamanders such as coarse woody debris and canopy cover . Data from timber harvesting studies suggest that long return-intervals of severe disturbances would minimize impacts on salamanders  and the litter layer .
Fire Ecology and Fire Regimes: Four-toed salamanders occur in forests with varied fire regimes (see the Fire Regime Table of plant communities with four-toed salamanders). Their association with moist areas near pools, streams, and other aquatic habitats suggests that their habitat would generally burn less frequently than upland forest types. Drought likely increases the risk of fire in four-toed salamander habitat. For more information on fire regimes within the four-toed salamander's range, see the FEIS reviews of the dominant plant species in four-toed salamander habitats, such as pitch pine, eastern white pine, white oak, and sugar maple (Acer saccharum), and the Fire Regime Table. Find fire regime information for the plant communities in which this species may occur by entering the species name in the FEIS home page under "Find Fire Regimes".
FIRE MANAGEMENT CONSIDERATIONS:
The lack of data addressing the impacts of fire on four-toed salamanders limits the generalizations that can be made regarding fire in four-toed salamander habitats. However, it is likely that low-severity, infrequent fires have few impacts on four-toed salamanders. Fires during or prior to active periods are likely to have greater impacts than fires at other times, since salamanders would be directly exposed to fire or recently burned habitats. It has been recommended that some portion of forests near nesting and larval habitat be maintained in an undisturbed, mature state to ensure the long-term persistence of salamanders, such as four-toed salamanders, with high nesting site fidelity and low dispersal ability that require cool, moist forest floors [44,69]. Prescribed burning may benefit some four-toed salamander larval habitats by increasing hydroperiods and food availability . More information on four-toed salamander response to fires of varying severities are needed [77,82], including postfire dispersal ability and population-level effects of changes in microsite temperatures, litter and soil moisture levels, and water chemistry .
Due to potential negative impacts on amphibians, plowing firebreaks is discouraged around wetlands, and the Forest Service no longer uses retardants containing sodium ferrocyanide in riparian areas [9,77].
|Fire regime information on vegetation communities that may provide habitat for four-toed salamanders. For each community, fire regime characteristics are taken from the LANDFIRE Rapid Assessment Vegetation Models . These vegetation models were developed by local experts using available literature, local data, and/or expert opinion as documented in the PDF file linked from the name of each Potential Natural Vegetation Group listed below. Cells are blank where information is not available in the Rapid Assessment Vegetation Model.|
|Vegetation Community (Potential Natural Vegetation Group)||Fire severity*||Fire regime characteristics|
|Percent of fires||Mean interval
|Great Lakes Woodland|
|Great Lakes pine barrens||Replacement||8%||41||10||80|
|Surface or low||83%||4||1||20|
|Great Lakes Forested|
|Northern hardwood maple-beech-eastern hemlock||Replacement||60%||>1,000|
|Conifer lowland (embedded in fire-prone system)||Replacement||45%||120||90||220|
|Conifer lowland (embedded in fire-resistant ecosystem)||Replacement||36%||540||220||>1,000|
|Great Lakes floodplain forest|
|Surface or low||93%||61|
|Great Lakes spruce-fir||Replacement||100%||85||50||200|
|Minnesota spruce-fir (adjacent to Lake Superior and Drift and Lake Plain)||Replacement||21%||300|
|Surface or low||79%||80|
|Great Lakes pine forest, jack pine||Replacement||67%||50|
|Surface or low||10%||333|
|Surface or low||67%||500|
|Maple-basswood mesic hardwood forest (Great Lakes)||Replacement||100%||>1,000||>1,000||>1,000|
|Surface or low||89%||35|
|Northern hardwood-eastern hemlock forest (Great Lakes)||Replacement||99%||>1,000|
|Surface or low||76%||11||2||25|
|Surface or low||81%||85|
|Red pine-eastern white pine (frequent fire)||Replacement||38%||56|
|Surface or low||26%||84|
|Red pine-eastern white pine (less frequent fire)||Replacement||30%||166|
|Surface or low||23%||220|
|Great Lakes pine forest, eastern white pine-eastern hemlock (frequent fire)||Replacement||52%||260|
|Surface or low||35%||385|
|Eastern white pine-eastern hemlock||Replacement||54%||370|
|Surface or low||34%||588|
|Vegetation Community (Potential Natural Vegetation Group)||Fire severity*||Fire regime characteristics|
|Percent of fires||Mean interval
|Eastern woodland mosaic||Replacement||2%||200||100||300|
|Surface or low||89%||4||1||7|
|Rocky outcrop pine (Northeast)||Replacement||16%||128|
|Surface or low||52%||40|
|Surface or low||65%||12|
|Oak-pine (eastern dry-xeric)||Replacement||4%||185|
|Surface or low||90%||8|
|Northern hardwoods (Northeast)||Replacement||39%||>1,000|
|Eastern white pine-northern hardwoods||Replacement||72%||475|
|Surface or low||28%||>1,000|
|Northern hardwoods-eastern hemlock||Replacement||50%||>1,000|
|Surface or low||50%||>1,000|
|Appalachian oak forest (dry-mesic)||Replacement||2%||625||500||>1,000|
|Surface or low||92%||15||7||26|
|Northeast spruce-fir forest||Replacement||100%||265||150||300|
|Southeastern red spruce-Fraser fir||Replacement||100%||500||300||>1,000|
|Vegetation Community (Potential Natural Vegetation Group)||Fire severity*||Fire regime characteristics|
|Percent of fires||Mean interval
|South-central US Woodland|
|Interior Highlands dry oak/bluestem woodland and glade||Replacement||16%||25||10||100|
|Surface or low||80%||5||2||7|
|Interior Highlands oak-hickory-pine||Replacement||3%||150||100||300|
|Surface or low||97%||4||2||10|
|Surface or low||96%||4|
|South-central US Forested|
|Interior Highlands dry-mesic forest and woodland||Replacement||7%||250||50||300|
|Surface or low||75%||22||5||35|
|Gulf Coastal Plain pine flatwoods||Replacement||2%||190|
|Surface or low||95%||5|
|West Gulf Coastal plain pine (uplands and flatwoods)||Replacement||4%||100||50||200|
|Surface or low||93%||4||4||10|
|West Gulf Coastal Plain pine-hardwood woodland or forest upland||Replacement||3%||100||20||200|
|Surface or low||94%||3||3||5|
|Surface or low||58%||100|
|Southern floodplain (rare fire)||Replacement||42%||>1,000|
|Surface or low||58%||714|
|Vegetation Community (Potential Natural Vegetation Group)||Fire severity*||Fire regime characteristics|
|Percent of fires||Mean interval
|Southern Appalachians Woodland|
|Appalachian shortleaf pine||Replacement||4%||125|
|Surface or low||92%||6|
|Table Mountain-pitch pine||Replacement||5%||100|
|Surface or low||92%||5|
|Surface or low||49%||55|
|Southern Appalachians Forested|
|Bottomland hardwood forest||Replacement||25%||435||200||>1,000|
|Surface or low||51%||210||50||250|
|Mixed mesophytic hardwood||Replacement||11%||665|
|Surface or low||79%||90|
|Surface or low||89%||6||3||10|
|Eastern hemlock-eastern white pine-hardwood||Replacement||17%||>1,000||500||>1,000|
|Surface or low||83%||210||100||>1,000|
|Oak (eastern dry-xeric)||Replacement||6%||128||50||100|
|Surface or low||78%||10||1||10|
|Appalachian Virginia pine||Replacement||20%||110||25||125|
|Surface or low||64%||35||10||40|
|Appalachian oak forest (dry-mesic)||Replacement||6%||220|
|Surface or low||79%||17|
|Southern Appalachian high-elevation forest||Replacement||59%||525|
|Vegetation Community (Potential Natural Vegetation Group)||Fire severity*||Fire regime characteristics|
|Percent of fires||Mean interval
|Gulf Coast wet pine savanna||Replacement||2%||165||10||500|
|Surface or low||98%||3||1||10|
|Longleaf pine (mesic uplands)||Replacement||3%||110||40||200|
|Surface or low||97%||3||1||5|
|Surface or low||10%||43||2||50|
|Atlantic wet pine savanna||Replacement||4%||100|
|Surface or low||94%||4|
|Coastal Plain pine-oak-hickory||Replacement||4%||200|
|Surface or low||89%||8|
|Atlantic white-cedar forest||Replacement||34%||200||25||350|
|Surface or low||59%||115||10||500|
|Surface or low||80%||9||3||50|
|Surface or low||97%||2||1||8|
|Loess bluff and plain forest||Replacement||7%||476|
|Surface or low||85%||39|
|Surface or low||93%||63|
Replacement: Any fire that causes greater than 75% top removal of a vegetation-fuel type, resulting in general replacement of existing vegetation; may or may not cause a lethal effect on the plants.
Mixed: Any fire burning more than 5% of an area that does not qualify as a replacement, surface, or low-severity fire; includes mosaic and other fires that are intermediate in effects.
Surface or low: Any fire that causes less than 25% upper layer replacement and/or removal in a vegetation-fuel class but burns 5% or more of the area [45,65].
1. Aber, John D.; Botkin, Daniel B.; Melillo, J. M. 1978. Predicting the effects of different harvesting regimes on forest floor dynamics in northern hardwoods. Canadian Journal of Forest Research. 8: 306-315. 
2. Ahlgren, C. E. 1974. Effects of fires on temperate forests: north central United States. In: Kozlowski, T. T.; Ahlgren, C. E., eds. Fire and ecosystems. New York: Academic Press: 195-223. 
3. Anton, Thomas G.; Mauger, David; Brandon, Ronald A.; Ballard, Scott R.; Stillwaugh, Donald M., Jr. 1998. Distribution, habitats, and status of four-toed salamanders in Illinois. In: Lannoo, Michael J., ed. Status and conservation of midwestern amphibians. Iowa City, IA: University of Iowa Press: 45-48. 
4. Ash, Andrew N. 1995. Effects of clear-cutting on litter parameters in the southern Blue Ridge Mountains. Castanea. 60(2): 89-97. 
5. Ash, Andrew N. 1997. Disappearance and return of Plethodontid salamanders to clearcut plots in the southern Blue Ridge Mountains. Conservation Biology. 11(4): 983-989. 
6. Babcock, S. K.; Hurney, C. A.; Vaglia, J. L.; Turner, S. D.; Cogbill, S. 2005. Embryonic development in the four-toed salamander, Hemidactylium scutatum. Integrative and Comparative Biology. Oxford: Oxford University Press. 44(6): 674. [Abstract]. Available online: http://www.sicb.org/meetings/2005/schedule/abstractdetails.php3?id=612. 
7. Benscoter, Brian W. 2006. Post-fire bryophyte establishment in a continental bog. Journal of Vegetation Science. 17: 647-652. 
8. Berger-Bishop, Laurel E.; Harris, Reid N. 1996. A study of caudal allometry in the salamander Hemidactylium scutatum (Caudata: Plethodontidae). Herpetologica. 52(4): 515-525. 
9. Bishop, David C.; Haas, Carola A. 2005. Burning trends and potential negative effects of suppressing wetland fires on flatwoods salamanders. Natural Areas Journal. 25(3): 290-294. 
10. Blanchard, Frank N. 1923. The life history of the four-toed salamander. The American Naturalist. 57(650): 262-268. 
11. Blanchard, Frank N. 1933. Late autumn collections and hibernating situations of the salamander Hemidactylium scutatum (Schlegel) in southern Michigan. Copeia. 1933(4): 216. 
12. Blanchard, Frank N. 1933. Spermatophores and the mating season of the salamander Hemidactylium scutatum (Schlegel). Copeia. 1933(1): 40. 
13. Blanchard, Frank N. 1934. The relation of the female four-toed salamander to her nest. Copeia. 1934(3): 137-138. 
14. Blanchard, Frank N. 1934. The spring migration of the four-toed salamander, Hemidactylium scutatum (Schlegel). Copeia. 1934(1): 50. 
15. Blanchard, Frank N. 1935. The sex ratio in the salamander Hemidactylium scutatum (Schlegel). Copeia. 1935(2): 103. 
16. Blanchard, Frank N.; Blanchard, Frieda Cobb. 1931. Size groups and their characteristics in the salamander Hemidactylium scutatum (Schlegel). The American Naturalist. 65(697): 149-164. 
17. Bol, Leslie; Massachusetts Division of Fisheries and Wildlife, Department of Fish and Game, Natural Heritage and Endangered Species Program. 2007. Massachusetts forestry conservation management practices for four-toed salamanders: Draft (August 2007), [Online]. Westborough, MA: Massachusetts Division of Fisheries and Wildlife, Department of Fish and Game, Natural Heritage and Endangered Species Program (Producer). Available: http://www.mass.gov/dfwele/dfw/nhesp/regulatory_review/pdf/fourtoed_salamander_cmp.pdf [2008, June 24]. 
18. Branin, M. Lelyn. 1935. Courtship activities and extra-seasonal ovulation in the four-toed salamander, Hemidactylium scutatum (Schlegel). Copeia. 1935(4): 172-175. 
19. Breitenbach, Gary L. 1982. The frequency of communal nesting and solitary brooding in the salamander, Hemidactylium scutatum. Journal of Herpetology. 16(4): 341-346. 
20. Bull, Evelyn L.; Wales, Barbara C. 2001. Effects of disturbance on amphibians of conservation concern in eastern Oregon and Washington. Northwest Science. 75: 174-179. 
21. Bury, R. Bruce; Major, Donald J.; Pilliod, David. 2002. Responses of amphibians to fire disturbance in Pacific Northwest forests: a review. In: Ford, W. Mark; Russell, Kevin R.; Moorman, Christopher E., eds. The role of fire in nongame wildlife management and community restoration: traditional uses and new directions: Proceedings of a special workshop; 2000 December 15; Nashville, TN. Gen. Tech. Rep. NE-288. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northeastern Research Station: 34-42. 
22. Carreno, Carrie A.; Harris, Reid N. 1998. Lack of nest defense behavior and attendance patterns in a joint nesting salamander, Hemidactylium scutatum (Caudata: Plethodontidae). Copeia. 1998(1): 183-189. 
23. Carreno, Carrie A.; Vess, Tomalei J.; Harris, Reid N. 1996. An investigation of kin recognition abilities in larval four-toed salamanders, Hemidactylium scutatum (Caudata: Plethodontidae). Herpetologica. 52(3): 293-300. 
24. Chalmers, Rebecca J.; Loftin, Cynthia S. 2006. Hemidactylium scutatum (four-toed salamander). Morphology/phenology. Herpetological Review. 37(1): 69-71. 
25. Chalmers, Rebecca J.; Loftin, Cynthia S. 2006. Wetland and microhabitat use by nesting four-toed salamanders in Maine. Journal of Herpetology. 40(4): 478-485. 
26. Coggins, James R.; Sajdak, Richard A. 1982. A survey of helminth parasites in the salamanders and certain anurans from Wisconsin. Proceedings of the Helminthological Society of Washington. 49(1): 99-102. 
27. Corser, Jeffrey D.; Dodd, C. Kenneth, Jr. 2004. Fluctuations in a metapopulation of nesting four-toed salamanders, Hemidactylium scutatum, in the Great Smoky Mountains National Park, USA, 1999-2003. Natural Areas Journal. 24(2): 135-140. 
28. Covington, W. Wallace. 1981. Changes in forest floor organic matter and nutrient content following clear cutting in northern hardwoods. Ecology. 62(1): 41-48. 
29. Crother, Brian I. 2000. Scientific and standard English names of amphibians and reptiles of North America north of Mexico, with comments regarding confidence in our understanding. Herpetological Circular No. 29. Lawrence, KS: Society for the Study of Amphibians and Reptiles. 82 p. 
30. Crother, Brian I.; Boundy, Jeff; Campbell, Jonathan A.; de Quieroz, Kevin; Frost, Darrel; Green, David M.; Highton, Richard; Iverson, John B.; McDiarmid, Roy W.; Meylan, Peter A.; Reeder, Tod W.; Seidel, Michael E.; Sites, Jack W., Jr.; [and others]. 2003. Scientific and standard English names of amphibians and reptiles of North America north of Mexico: update. Herpetological Review. 34(3): 196-203. 
31. Cummer, Michelle R.; Painter, Charles W. 2007. Three case studies of the effect of wildfire on the Jemez Mountains salamander (Plethodon neomexicanus): microhabitat temperatures, size distributions, and a historical locality perspective. The Southwestern Naturalist. 52(1): 26-37. 
32. Daniel, Paul M. 1989. Hemidactylium scutatum (Schlegel): Four-toed salamander. In: Pfingsten, Ralph A.; Downs, Floyd L., eds. Salamanders of Ohio. Columbus, OH: Ohio State University, College of Biological Sciences: 223-228. 
33. Degraaf, Richard M.; Yamasaki, Mariko. 1990. Herpetofaunal species composition and relative abundance among three New England forest types. Forest Ecology and Management. 32: 155-165. 
34. deMaynadier, Phillip G.; Hunter, Malcolm L., Jr. 1995. The relationship between forest management and amphibian ecology: a review of the North American literature. Environmental Review. 3: 230-261. 
35. deMaynadier, Phillip G.; Hunter, Malcolm L., Jr. 1998. Effects of silvicultural edges on the distribution and abundance of amphibians in Maine. Conservation Biology. 12(2): 340-352. 
36. Easterla, David A. 1971. A breeding concentration of four-toed salamanders, Hemidactylium scutatum in southeastern Missouri. Journal of Herpetology. 5(3-4): 194-195. 
37. Feder, Martin E. 1983. Integrating the ecology and physiology of Plethodontid salamanders. Herpetologica. 39(3): 291-310. 
38. Floyd, Thomas M.; Russell, Kevin R.; Moorman, Christopher E.; Van Lear, David H.; Guynn, David C., Jr.; Lanham, J. Drew. 2002. Effects of prescribed fire on herpetofauna within hardwood forests of the Upper Piedmont of South Carolina: a preliminary analysis. In: Outcalt, Kenneth W., ed. Proceedings, 11th biennial southern silvicultural research conference; 2001 March 20-22; Knoxville, TN. Gen. Tech. Rep. SRS-48. Asheville, NC: U.S. Department of Agriculture, Forest Service, Southern Research Station: 123-127. 
39. Ford, William M.; Menzel, M. Alex; McGill, David W.; Laerm, Joshua; McCay, Timothy S. 1999. Effects of a community restoration fire on small mammals and herpetofauna in the southern Appalachians. Forest Ecology and Management. 114(2-3): 233-243. 
40. Gagan, Alison Baird. 2002. The effects of prescribed fire on millipede and salamander populations in a southern Appalachian deciduous forest. Johnson City, TN: East Tennessee State University. 37 p. Thesis. 
41. Gamradt, Seth C.; Kats, Lee B. 1997. Impact of chaparral wildfire-induced sedimentation on oviposition of stream-breeding California newts (Taricha torosa). Oecologia. 110(4): 546-549. 
42. Gilbert, Perry W. 1941. Eggs and nests of Hemidactylium scutatum in the Ithaca region. Copeia. 1941(1): 47. 
43. Greenberg, Cathryn H.; Waldrop, Thomas A. 2008. Short-term response of reptiles and amphibians to prescribed fire and mechanical fuel reduction in a southern Appalachian upland hardwood forest. Forest Ecology and Management. 255(7): 2883-2893. 
44. Hanlin, Hugh G.; Martin, F. Douglas; Wike, Lynn D.; Bennett, Stephen H. 2000. Terrestrial activity, abundance and species richness of amphibians in managed forests in South Carolina. The American Midland Naturalist. 143(1): 70-83. 
45. Hann, Wendel; Havlina, Doug; Shlisky, Ayn; [and others]. 2005. Interagency fire regime condition class guidebook. Version 1.2, [Online]. In: Interagency fire regime condition class website. U.S. Department of Agriculture, Forest Service; U.S. Department of the Interior; The Nature Conservancy; Systems for Environmental Management (Producer). Variously paginated [+ appendices]. Available: http://www.frcc.gov/docs/22.214.171.124/Complete_Guidebook_V1.2.pdf [2007, May 23]. 
46. Harpole, Douglas N.; Haas, Carola A. 1999. Effects of seven silvicultural treatments on terrestrial salamanders. Forest Ecology and Management. 114: 349-356. 
47. Harris, Reid N.; Gill, Douglas E. 1980. Communal nesting, brooding behavior, and embryonic survival of the four-toed salamander Hemidactylium scutatum. Herpetologica. 36(2): 141-144. 
48. Harris, Reid N.; Hames, Whitney W.; Knight, Ivor T.; Carreno, Carrie A.; Vess, Tomalei J. 1995. An experimental analysis of joint nesting in the salamander Hemidactylium scutatum (Caudata: Plethodontidae): the effects of population density. Animal Behaviour. 50(5): 1309-1316. 
49. Harris, Reid N.; James, Timothy Y.; Lauer, Antje; Simon, Mary Alice; Patel, Amit. 2006. Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth. 3(1): 53-56. 
50. Harris, Reid N.; Ludwig, Patrice M. 2004. Resource level and reproductive frequency in female four-toed salamanders, Hemidactylium scutatum. Ecology. 85(6): 1585-1590. 
51. Harris, Reid N.; Vess, Tomalei J.; Hammond, John I.; Lindermuth, Christine J. 2003. Context-dependent kin discrimination in larval four-toed salamanders Hemidactylium scutatum (Caudata: Plethodontidae). Herpetologica. 59(2): 164-177. 
52. Herman, T. B.; Scott, F. W. 1994. Protected areas and global climate change: assessing the regional or local vulnerability of vertebrate species. In: Pernetta, John; Leemans, Rik; Elder, Danny; Humphrey, Sarah, eds. Impacts of climate change on ecosystems and species: implications for protected areas. Gland, Switzerland: International Union for Conservation of Nature and Natural Resources: 13-27. 
53. Herrington, Bob. 1999. Amphibian, reptile and small mammal diversity in a lowland hardwood forest in Marion County, Georgia. Georgia Journal of Science. 57(4): 246-254. 
54. Hess, Zachary J.; Harris, Reid N. 2000. Eggs of Hemidactylium scutatum (Caudata: Plethodontidae) are unpalatable to insect predators. Copeia. 2000(2): 597-600. 
55. Hicks, Norman G.; Pearson, Scott M. 2003. Salamander diversity and abundance in forests with alternative land use histories in the southern Blue Ridge Mountains. Forest Ecology and Management. 177: 117-130. 
56. Hossack, Blake R.; Corn, Paul Stephen. 2007. Responses of pond-breeding amphibians to wildfire: short-term patterns in occupancy and colonization. Ecological Applications. 17(5): 1403-1410. 
57. Hughes, Jeffrey W.; Fahey, Timothy J. 1994. Litterfall dynamics and ecosystem recovery during forest development. Forestry Ecology and Management. 63: 181-198. 
58. Jaeger, Robert G. 1980. Fluctuations in prey availability and food limitation for a terrestrial salamander. Oecologia. 44: 335-341. 
59. Johnson, Tom R. 2000. Four-toed salamander--Hemidactylium scutatum (Schlegel). In: Davit, Carol, ed. The amphibians and reptiles of Missouri. 2nd ed. Jefferson City, MO: Missouri Department of Conservation: [pages unknown]. 
60. Kats, Lee B.; Petranka, James W.; Sih, Andrew. 1988. Antipredator defenses and the persistence of amphibian larvae with fishes. Ecology. 69(6): 1865-1870. 
61. Keyser, Patrick D.; Sausville, David J.; Ford, W. Mark; Schwab, Donald J.; Brose, Patrick H. 2004. Prescribed fire impacts to amphibians and reptiles in shelterwood-harvested oak-dominated forests. Virginia Journal of Science. 55(4): 159-168. 
62. Kirkland, Gordon L., Jr.; Snoddy, Heather W.; Amsler, Teresa L. 1996. Impact of fire on small mammals and amphibians in a central Appalachian deciduous forest. The American Midland Naturalist. 135(2): 253-260. 
63. Kirkpatrick, Helen Elizabeth. 1990. Resource competition between two co-occurring species of Polytrichum. Ann Arbor, MI: The University of Michigan. 153 p. Dissertation. 
64. Knoepp, Jennifer D.; DeBano, Leonard F.; Neary, Daniel G. 2005. (revised 2008). Chapter 3: soil chemistry. In: Neary, Daniel G.; Ryan, Kevin C.; DeBano, Leonard F., eds. Wildland fire in ecosystems: Effects of fire on soil and water. Gen. Tech. Rep. RMRS-GTR-42-vol. 4. Ogden, UT: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station: 53-72. 
65. LANDFIRE Rapid Assessment. 2005. Reference condition modeling manual (Version 2.1), [Online]. In: LANDFIRE. Cooperative Agreement 04-CA-11132543-189. Boulder, CO: The Nature Conservancy; U.S. Department of Agriculture, Forest Service; U.S. Department of the Interior (Producers). 72 p. Available: http://www.landfire.gov/downloadfile.php?file=RA_Modeling_Manual_v2_1.pdf [2007, May 24]. 
66. LANDFIRE Rapid Assessment. 2007. Rapid assessment reference condition models, [Online]. In: LANDFIRE. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Lab; U.S. Geological Survey; The Nature Conservancy (Producers). Available: http://www.landfire.gov/models_EW.php [2008, April 18] 
67. Lyon, L. Jack; Telfer, Edmund S.; Schreiner, David Scott. 2000. Direct effects of fire and animal responses. In: Smith, Jane Kapler, ed. Wildland fire in ecosystems: Effects of fire on fauna. Gen. Tech. Rep. RMRS-GTR-42-vol. 1. Ogden, UT: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station: 17-23. 
68. Madison, D. M.; Shoop, C. Robert. 1970. Homing behavior, orientation, and home range of salamanders tagged with tantalum-182. Science. 168: 1484-1487. 
69. McLeod, Roderick F.; Gates, J. Edward. 1998. Response of herpetofaunal communities to forest cutting and burning at Chesapeake Farms, Maryland. The American Midland Naturalist. 139: 164-177. 
70. Mitchell, Joseph C. 2000. Observations on amphibians and reptiles in burned and unburned forests on the upper coastal plain of Virginia. Virginia Journal of Science. 51(3): 199-203. 
71. Moseley, Kurtis R.; Castleberry, Steven B.; Schweitzer, Sara H. 2003. Effects of prescribed fire on herpetofauna in bottomland hardwood forests. Southeastern Naturalist. 2(4): 475-486. 
72. Neary, Daniel G.; Landsberg, Johanna D.; Tiedemann, Arthur R.; Ffolliott, Peter F. 2005. (revised 2008). Chapter 6: water quality. In: Neary, Daniel G.; Ryan, Kevin C.; DeBano, Leonard F., eds. Wildland fire in ecosystems: Effects of fire on soil and water. Gen. Tech. Rep. RMRS-GTR-42-vol. 4. Ogden, UT: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station: 119-134. 
73. O'Laughlin, Bridget E.; Harris, Reid N. 2000. Models of metamorphic timing: an experimental evaluation with the pond-dwelling salamander Hemidactylium scutatum (Caudata: Plethodontidae). Oecologia. 124(3): 343-350. 
74. Paton, Peter; Stevens, Sara; Longo, Linda. 2000. Seasonal phenology of amphibian breeding and recruitment at a pond in Rhode Island. Northeastern Naturalist. 7(3): 255-269. 
75. Petranka, James W.; Brannon, M. Patrick; Hopey, Mark E.; Smith, Charles K. 1994. Effects of timber harvesting on low elevation populations of southern Appalachian salamanders. Forest Ecology and Management. 67: 135-147. 
76. Petranka, James W.; Eldridge, Matthew E.; Haley, Katherine E. 1993. Effects of timber harvesting on southern Appalachian salamanders. Conservation Biology. 7(2): 363-370. 
77. Pilliod, David S.; Bury, R. Bruce; Hyde, Erin J.; Pearl, Christopher A.; Corn, Paul Stephen. 2003. Fire and amphibians in North America. In: Young, Michael K.; Gresswell, Robert E.; Luce, Charles H., guest eds. Special issue: The effects of wildland fire on aquatic ecosystems in the western USA: Selected papers from an international symposium on effects of wildland fire on aquatic ecosystems in the western USA; 2002 April 22-24; Boise, ID. In: Forest Ecology and Management. Amsterdam; London; New York: Elsevier Science B. V.; 178(1-2): 163-181. [Special Issue]. 
78. Pough, F. Harvey; Smith, Ellen M.; Rhodes, Donald H.; Collazo, Andres. 1987. The abundance of salamanders in forest stands with different histories of disturbance. Forest Ecology and Management. 20: 1-9. 
79. Price, Steven J.; Jaskula, Jeanette M. 2005. Hemidactylium scutatum (four-toed salamander) nesting ecology. Herpetological Review. 36(2): 159. 
80. Price, Steven J.; Jaskula, Jeanette M. 2005. Hemidactylium scutatum (four-toed salamander) terrestrial microhabitat. Herpetological Review. 36(2): 159. 
81. Ross, Brad; Fredericksen, Todd; Ross, Eric; Hoffman, Wayne; Morrison, Michael L.; Beyea, Jan; Lester, Michael B.; Johnson, Bradley N.; Fredericksen, Nell J. 2000. Relative abundance and species richness of herpetofauna in forest stands in Pennsylvania. Forest Science. 46(1): 139-146. 
82. Russell, Kevin R.; Van Lear, David H.; Guynn, David C., Jr. 1999. Prescribed fire effects on herpetofauna: review and management implications. Wildlife Society Bulletin. 27(2): 374-384. 
83. Saugey, David A.; Trauth, Stanley E. 1991. Distribution and habitat utilization of the four-toed salamander, Hemidactylium scutatum, in the Ouachita Mountains of Arkansas. Proceedings Arkansas Academy of Science. 45: 88-91. 
84. Schurbon, Jamie M.; Fauth, John E. 2003. Effects of prescribed burning on amphibian diversity in a southeastern U.S. national forest. Conservation Biology. 17(5): 1338-1349. 
85. Seastedt, T. R.; Crossley, D. A., Jr. 1981. Microarthropod response following cable logging and clear-cutting in the southern Appalachians. Ecology. 62(1): 126-135. 
86. Secrist, Dana E.; Maehr, David S.; Larkin, Jeffrey L.; Lacki, Michael J. 2004. Potential impacts of reintroduced elk on amphibian distribution and abundance in eastern Kentucky, USA. Natural Areas Journal. 24(1): 65-68. 
87. Skelly, David K.; Werner, Earl E.; Cortwright, Spencer A. 1999. Long-term distributional dynamics of a Michigan amphibian assemblage. Ecology. 80(7): 2326-2337. 
88. Thurow, Gordon R. 1997. Observations on Hemidactylium scutatum habitat and distribution. Bulletin of the Chicago Herpetological Society. 32(1): 1-6. 
89. Trauth, Stanley E.; Cochran, Betty G. 1991. Hemidactylium scutatum (four-toed salamander). Predation. Herpetological Review. 22(2): 55. 
90. Wallace, Robert S. 1984. Use of sphagnum moss for nesting by the four-toed salamander, Hemidactylium scutatum Schlegl. (Plethodontidae). Proceedings of the Pennsylvania Academy of Science. 58(2): 237-238. 
91. Wells, Christopher S.; Harris, Reid N. 2001. Activity level and the tradeoff between growth and survival in the salamanders Ambystoma jeffersonianum and Hemidactylium scutatum. Herpetologica. 57(1): 116-127. 
92. Whitaker, John O., Jr.; Minton, Sherman A., Jr. 1988. Reptiles and amphibians. In: Whitaker, John O., Jr.; Gammon, James R., [eds.]. Endangered and threatened vertebrate animals of Indiana their distribution and abundance. Monograph No. 5. Indianapolis, IN: Indiana Academy of Science: 67-86. 
93. Wilson, L. Wayne; Friddle, Saufley B. 1950. The herpetology of Hardy County, West Virginia. The American Midland Naturalist. 43(1): 165-172. 
94. Wood, John Thornton. 1953. Observations on the complements of ova and nesting of the four-toed salamander in Virginia. The American Naturalist. 87(833): 77-86. 
95. Wood, John Thornton. 1955. The nesting of the four-toed salamander, Hemidactylium scutatum (Schlegel), in Virginia. The American Naturalist. 53(2): 381-389. 
96. Wyman, Richard L. 1988. Soil acidity and moisture and the distribution of amphibians in five forests of southcentral New York. Copeia. 1988(2): 394-399.