Long-toed Salamander
Encyclopedia
The long-toed salamander (Ambystoma macrodactylum, Baird 1849) is a mole salamander
in the family Ambystomatidae. This species, typically 4.1–8.9 cm (1 3/5–3½ in) long when mature, is characterized by its mottle
d black, brown and yellow pigmentation, and its long outer fourth toe on the hind limbs. Analysis of fossil records, genetics
, and biogeography
suggest that A. macrodactylum and A. laterale are descended from a common ancestor that gained access to the western Cordillera with the loss of the mid-continental seaway
toward the Paleocene
.
The distribution of the long-toed salamander is primarily in the Pacific Northwest
, with an altitudinal range of up to 2800 metres (9,186.4 ft). It lives in a variety of habitats including temperate rainforests, coniferous forests, montane
riparian zones, sagebrush
plains, red fir
forests, semi-arid sagebrush, cheatgrass plains, and alpine meadows along the rocky shores of mountain lakes. It lives in slow-moving streams, ponds and lakes during its aquatic breeding
phase. The long-toed salamander hibernates during the cold winter months, surviving on protein
energy reserves stored in the skin and tail.
There are five subspecies
having different genetic and ecological histories that are phenotypically
expressed in a range of color and skin patterns. Although the long-toed salamander is classified as a species of Least Concern
by the IUCN, many forms of land development threaten and negatively affect the salamander's habitat.
) from its sister
taxon Dicamptodontidae. The Ambystomatidae are also members of suborder Salamandroidea
, which includes all the salamanders capable of internal fertilization. The sister species to A. macrodactylum is A. laterale, distributed in eastern North America. However, the species-level phylogeny
for Ambystomatidae is tentative and in need of further testing.
stripe of tan, yellow or olive-green. This stripe can also be broken up into a series of spots. The side of the body can have fine white or pale blue flecks. The belly is dark-brown or sooty in color with white flecks. Root tubercle
s are present, but they are not quite as developed as other species such as the Tiger Salamander
.
The egg
s of this species look similar to those of its cousins, the northwestern salamander (Ambystoma gracile) and the tiger salamander (Ambystoma tigrinum). Like many amphibians, the eggs of the long-toed salamander are surrounded by a gelatinous capsule. This capsule is transparent, making the embryo visible during development. Unlike A. gracile eggs, there are no visible signs of green algae
, which makes egg jellies green in color. When in its egg, the long-toed salamander embryo
is darker on top and whiter below compared to a tiger salamander embryo that is light brown to grey above and cream-colored on the bottom. The eggs are about 2 mm (0.078740157480315 in) or greater in diameter with a wide outer jelly layer. Prior to hatching—both in the egg and as newborn larva
e—they have balancers, which are thin skin protrusions sticking out the sides and supporting the head. The balancers eventually fall off and their external gills grow larger. Once the balancers are lost the larvae are distinguished by the sharply pointed flaring of the gills. As the larvae mature and metamorphose
, their limbs with digits become visible and the gills are absorbed.
The skin of a larva is mottled with black, brown, and yellow pigmentation. Skin color changes as the larvae develop and pigment cells migrate and concentrate in different regions of the body. The pigment cells are called chromatophore
s, which are derived from the neural crest
. There are three types of pigment chromatophores in salamanders, including yellow xanthophores, black melanophores, and silvery iridiophores (or guanophores). As the larvae mature the melanophores concentrate along the body and provide the darker background. The yellow xanthophores arrange along the spine and on top of the limbs. The rest of the body is flecked with reflective iridiophores along the sides and underneath.
As larvae metamorphose, they develop digits out of their limb bud protrusions. A fully metamorphosed long-toed salamander has four digits on the front hands and five digits on the rear feet. Its head is longer than it is wide, and the long outer fourth toe on the hind limb of mature larvae and adults distinguishes this species from others and is also the etymological
origin of its specific epithet: macrodactylum (Gr. makros = long and Gr. daktylos = toe). The adult skin has a dark brown, dark grey, to black background with a yellow, green, or dull red blotchy stripe with dots and spots along the sides. Underneath the limbs, head, and body the salamander is white, pinkish, to brown with larger flecks of white and smaller flecks of yellow. Adults are typically 3.8 – long.
riparian, sagebrush
plains, red fir
forest, semi-arid sagebrush, cheatgrass plains, to alpine meadows along the rocky shores of mountain lakes. Adults can be located in forested understory
, hiding under coarse woody debris
, rocks, and in small mammal burrows. During the spring breeding season adults can be found under debris or the shoreline shallows of rivers, streams, lakes, and ponds. Ephemeral waters are often frequented.
This species
is one of the most widely distributed salamander
s in North America, second only to the tiger salamander
. Its altitudinal range runs from sea level up to 2800 metres (9,186.4 ft) spanning a wide variety of vegetational zones. The range includes isolated endemic populations in Monterey Bay
and Santa Cruz, California
. The distribution reconnects in northeastern Sierra Nevada, California running continuously along the Pacific Coast
to Juneau, Alaska
, with populations dotted along the Taku
and Stikine River
valleys. From the Pacific coast the range extends longitudinally
to the eastern foothills of the Rocky Mountains
in Montana
and Alberta
.
of a calm pond. The number of eggs in a single mass ranges in size, possibly up to 110 eggs per cluster. Females invest a significant amount of resources into egg production, with the ovaries accounting for over 50% of the body mass in the pre-breeding season. A maximum of 264 eggs have been found in a single female—a large number considering each egg is approximately 0.5 millimetre (0.0196850393700787 in) in diameter. The egg mass is held together by a gelatinous outer layer protecting the outer capsule of individual eggs. The eggs are sometimes laid singly, especially in warmer climates south of the Canada and US border. The egg jellies contribute a yearly supply of biological material that supports the chemistry and nutrient dynamics of shallow-water aquatic ecosystem
s and adjacent forest ecosystems. The eggs also provide habitat for water molds, also known as oomycetes.
e hatch from their egg casing in two to six weeks. They are born carnivores, feeding instinct
ively on small invertebrate
s that move in their field of vision. Food items include small aquatic crustacean
s (cladocera
ns, copepod
s and ostracod
s), aquatic diptera
ns and tadpole
s. As they develop, they naturally feed upon larger prey. To increase their chances for survival, some individuals grow bigger heads and become cannibals
, and feed upon their own brood mates.
), they absorb their gills and metamorphose
into terrestrial juveniles that roam the forest undergrowth
. Metamorphosis has been reported as early as July at sea level, for A. m. croceum in October to November and even January. At higher elevations the larvae may overwinter
, develop, and grow for an extra season before metamorphosing. In lakes at higher elevations, the larvae can reach sizes of 47 millimetres (1.9 in) snout to vent length (SVL) at metamorphosis, but at lower elevations they develop faster and metamorphose when they reach 35 – SVL.
burrow
s or rock fissure
s. The adult diet consists of insects, tadpoles, worms, beetles and small fish. Salamanders are preyed upon by garter snakes, small mammals, birds, and fish. An adult may live 6–10 years, with the largest individuals weighing approximately 7.5 gram (0.26455471578834 oz), snout to vent lengths reaching 8 cm (3.1 in), and total lengths reaching 14 cm (5.5 in).
of the long-toed salamander varies greatly with elevation and climate. Seasonal dates of migration to and from the breeding ponds can be correlated with bouts of sustained rainfall, ice thaw, or snow melt sufficient to replenish the (often) seasonal ponds. Eggs may be spawned
at low elevations as early as mid-February in southern Oregon
, from early January to July in northwestern Washington, from January to March in southeastern Washington, and from mid-April to early May in Waterton Lakes National Park
, Alberta. The timing of breeding can be highly variable; of notable mention, several egg masses in early stages of development were found on July 8, 1999 along the British Columbia
provincial border outside Jasper, Alberta
. Adults migrate seasonally to return to their natal
breeding ponds, with males arriving earlier and staying longer than females, and some individuals have been seen migrating along snow banks on warm spring days. Gender differences (or sexual dimorphism
) in this species are only apparent during the breeding season, when mature males display an enlarged or bulbous vent area.
The time of breeding depends on the elevation and latitude of the salamander's habitat. Generally, the lower-elevation salamanders breed in the fall, winter, and early spring. Higher-elevation salamanders breed in spring and early summer. In the higher climates especially, salamanders will enter ponds and lakes that still have ice floating.
Adults aggregate in large numbers (>20 individuals) under rocks and logs along the immediate edge of the breeding sites and breed explosively over a few days. Suitable breeding sites include small fish-free ponds, marshes, shallow lakes and other still-water wetlands. Like other ambystomatid salamanders, they have evolved a characteristic courtship dance where they rub bodies and release pheromones from their chin gland prior to assuming a copulatory mating
position. Once in position, the male deposits a spermatophore
, which is a gooey stalk tipped with a packet of sperm, and walks the female forward to be inseminate
d. Males may mate more than once and may deposit as many as 15 spermatophores over the course of a five hour period. The courtship dance for the long-toed salamander is similar to other species of Ambystoma and very similar to A. jeffersonianum. In the long-toed salamander, there is no rubbing or head-butting; the males directly approach females and grab on, while the females try to rapidly swim away. The males clasp the female from behind the forelimbs and shake, a behavior called amplexus
. Males sometimes clasp other amphibian species during breeding and shake them as well. The male only grabs with the front limbs and never uses his hind limbs during the courtship dance as he rubs his chin side to side pressing down on the female's head. The female struggles but later becomes subdued. Males increase the tempo and motions, rubbing over the female's nostrils, sides, and sometimes the vent. When the female becomes quite docile the male moves forward with his tail positioned over her head, raised, and waving at the tip. If the female accepts the males courtship, the male directs her snout toward his vent region while both move forward stiffly with pelvic undulations. As the female follows, the male stops and deposits a spermatophore, and the female will move forward with the male to raise her tail and receive the sperm packet. The full courtship dance is rarely accomplished in the first attempt. Females deposit their eggs a few days after mating.
In some lowland areas the adult salamanders will remain active all winter long, excluding cold spells. However, during the cold winter months in the northern parts of its range, the long-toed salamander burrows below the frost-line in a coarse substrate to hibernate in clusters of 8–14 individuals. While hibernating, it survives on protein energy reserves that are stored in its skin and along its tail. These proteins serve a secondary function as part of a mixture or concoction of skin secretions that is used for defense. When threatened, the long-toed salamander will wave its tail and secrete an adhesive white milky substance that is noxious and likely poisonous. The color of its skin can serve as a warning to predators (aposematism
) that it will taste bad. Its skin colors and patterns are diverse, ranging from a dark black to reddish brown background that is spotted or blotched by a pale-reddish-brown, pale-green, to a bright yellow stripe. An adult may also drop part of its tail and slink away while the tail bit acts as a squirmy decoy; this is called autotomy
. The regeneration
and regrowth of the tail is one example of the developmental physiology
of amphibians that is of great interest to the medical profession.
. Conservation priorities focus at the population level of diversity, which is declining at rates ten times that of species extinction. Population level diversity is what provides ecosystem services
, such as the keystone role that salamanders play in the soil ecosystems, including the nutrient cycling that supports wetland and forested ecosystems.
Two life-history features of amphibians are often cited as a reason why amphibians are good indicators of environmental health or 'canaries in the coal mine'. Like all amphibians, the long-toed salamander has both an aquatic and terrestrial life transition and semi-permeable skin. Since they serve different ecological functions in the water than they do in land, the loss of one amphibian species is equivalent to the loss of two ecological species. The second notion is that amphibians, such as long-toed salamanders, are more susceptible to the absorption of pollutants because they naturally absorb water and oxygen through their skin. The validity of this special sensitivity to environmental pollutants, however, has been called into question. The problem is more complex, because not all amphibians are equally susceptible to environmental damage because there is such a diverse array of life histories among species.
Long-toed salamander populations are threatened by fragmentation
, introduced species
, and UV radiation. Forestry, roads, and other land developments have altered the environments that amphibians migrate to, and have increased mortality
. Places such as Waterton Lakes National Park
have installed a road tunnel underpass to allow safe passage and to sustain the migration ecology of the species.http://www.pc.gc.ca/eng/pn-np/ab/waterton/natcul/natcul1/w/1.aspx The distribution of the long-toed salamander overlaps extensively with the forestry industry, a dominant resource supporting the economy of British Columbia and the western United States. Long-toed salamanders will alter migration behaviour and are affected negatively by forestry practices not offering sizable management buffers
and protections for the smaller wetlands where salamanders breed. Populations near the Peace River Valley
, Alberta, have been lost to the clearing and draining of wetlands for agriculture. Trout
introduced for the sport fisheries into once fishless lakes are also destroying long-toed salamander populations. Introduced goldfish predate upon the eggs and larvae of long-toed salamanders. Increased exposure to UVB radiation is another factor being implicated in the global decline of amphibians and the long-toed salamander is also susceptible to this threat, which increases the incidence of deformities and reduces their survival and growth rates.
The subspecies Ambystoma macrodactylum croceum (Santa Cruz Long-toed Salamander
) is of particular concern and it was afforded protections in 1967 under the US Endangered Species Act
. This sub-species lives in a narrow range of habitat in Santa Cruz County
and Monterey County, California. Prior to receiving protections, some few remaining populations were threatened by development. The sub-species is ecologically unique, having unique and irregular skin patterns on its back, a unique moisture tolerance, and it is also an endemic that is geographically isolated from the rest of the species range. Other subspecies include A. m. columbianum, A. m. krausei, A. m. macrodactylum and A. m. sigillatum.
, where species richness
of ambystomatids are highest. The following biogeographic
interpretation on the origins of A. macrodactylum into western North America is based on a descriptive account of fossils, genetics, and biogeography. The long-toed salamander's closest living sister species is A. laterale, a native to northeastern North America. Ambystomatidae was isolated to the southeast of the mid-Continental or Western Interior Seaway
during the Cretaceous
(~145.5–65.5 Ma). While three other species of the Ambystomatidae (A. tigrinum, A. californiense, and A. gracile) have overlapping ranges in western North America, the long-toed salamander's closest living sister species is A. laterale, a native to northeastern North America. It has been suggested that A. macrodactylum speciated
from A. laterale after the Paleocene
(~65.5–55.8 Ma) with the loss of the Western Interior Seaway
opening an access route for a common ancestor into the Western Cordillera. Once situated in the montane regions of western North America, species had to contend with a dynamic spatial and compositional ecology responding to the changes in altitude, as mountains grew and the climate changed. For example, the Pacific Northwest
became cooler in the Paleocene
, paving the way for temperate forest
to replace the warmer tropical forest of the Cretaceous
. A scenario for the splitting of A. macrodacylum and other western temperate species from their eastern counterparts involves Rocky Mountain uplift in the late Oligocene
into the Miocene
. The orogeny
created a climatic barrier by removing moisture from the westerly air stream and dried the midcontinental area, from southern Alberta to the Gulf of Mexico.
Ancestors of contemporary salamanders were likely able to disperse and migrate into habitats of the Rocky Mountains
and surrounding areas by the Eocene
. Mesic forests were established in western North America by the mid Eocene
and attained their contemporary range distributions by the early Pliocene
. The temperate forest valleys and montane
environments of these time periods (Paleogene
to Neogene
) would have provided the physiographic and ecological features supporting analogs of contemporary Ambystoma macrodactylum habitats. The Cascade Range
rose during the mid Pliocene
and created a rain shadow effect causing the xerification of the Columbia Basin
and also altered ranges of temperate mesic ecosystems at higher elevations. The rise of the Cascades causing the xerification of the Columbia Basin is a major biogeographic feature of western North America that divided many species, including A. macrodactylum, into coastal and inland lineages.
of long-toed salamander. The subspecies are discerned by their geographic location and patterns in their dorsal stripe pattern; Denzel Ferguson gives a biogeographic account of skin patterns, morphology, and based on this analysis he introduced two new sub-species, A. macrodactylum columbianum and A. m. sigillatum. The ranges of sub-species are illustrated in Robert Stebbin's amphibian field guides.
A. m. croceum: Orange dorsal color on tail breaking into patches along black body and into tiny dots on head, often absent anterior to eyes. Sides have whitish flecks. Number of costal groove
s equals 13.
A. m. columbianum: Yellow to tan dorsal stripe on black body continuous blotches to spots along body ending in narrowed blotches with spot patterns distributed on the head. White flecks along sides and underside remaining as separate small flecks. Number of vomerine teeth greater than 35.
A. m. krausei: Yellow to tan dorsal stripe continuous blotches to spots along body ending in widened blotches with spot patterns distributed on the head. White flecks along sides and underside remaining as separate small flecks. Number of vomerine teeth equaling 32. Number of costal grooves equals 12.
A. m. sigillatum: Wax yellow to tan dorsal stripe forming spotty to irregular shaped blotches along body ending in dots or specks of dorsal color on head. Number of vomerine teeth equals 44. Number of costal grooves equals 13.
A. m. macrodactylum: Citrine, dull citrine, to tan dorsal stripe that is diffuse and continuous along grayish body. Pattern ending in diffuse specks of stripe color or absent on head and snout. White flecks on sides sometimes coming together to form larger flecks. Number of vomerine teeth equaling 33, forming a distinguished transverse arc. Number of costal grooves equals 13.
analysis identifies somewhat different ranges for the subspecies lineages. The genetic analysis, for example, identifies an additional pattern of deep divergence in the eastern part of the range. The spatial distribution of populations and genetics of this species links spatially and historically through the interconnecting mountain and temperate valley systems of western North America. The breeding fidelity of long-toed salamanders (philopatry
) and other migratory behaviours reduce rates of dispersal among regions, such as within mountain basins. This aspect of their behavior restricts gene flow
and increases the degree and rates of genetic differentiation. Genetic differentiation among regions is higher in the long-toed salamander than measured in most other vertebrate
groups. Natural breaks in the range of dispersal and migration occur where ecosystems grade into drier xeric low-lands (such as prairie
climates) and at frozen or harsher terrain at high elevation extremes (2200 metres (7,217.8 ft)).
A. m. columbianum:Genetic evidence for the 'central' subspecies (A. m. columbianum) suggests that it does not extend north into British Columbia, but is restricted to the Blue
and Wallowa Mountains
of central to northeastern sections of Oregon. Populations are restricted to these areas by the Snake River Canyon (Idaho)
to the east and low dry or xeric lands in the Madras basin
to the west.
A. m. macrodactylum:The 'coastal' or 'western' subspecies (A. m. macrodactylum) lineage extends north from northeastern California, across the Klamath Siskiyou Range, through the Willamette Valley
, along the coastal mountain ranges, including the Cascade Mountains, and continuing north through British Columbia and up into Alaska.
A. m. croceum:The Santa Cruz salamander (A. m. croceum) is most closely related to the 'coastal' or 'western' subspecies. This conclusion is the most parsimonious biogeographic explanation
with nearest populations of A. m. macrodactylum separated by approximately 300 km across the Sacramento-San Joaquin River Delta, California. The isolated endemic populations in California, the Santa Cruz Long-toed Salamander
(Ambystoma macrodactlylum croceum), are listed as an endangered sub-species. Based on the biogeography and molecular clock calibrations, this sub-species may have been separated from the remainder of the distribution since the Miocene, molecular clock
calibrations estimating 13.9 million years of separation.
A. m. krausei:The 'eastern' subspecies (A. m. krausei) range is distributed throughout the interior mountains, with the western extent of its range encroaching into the low-land areas of the central interior plateau of Washington and British Columbia and the eastern extent of its range pushing through Rocky Mountain valleys into the low-land foothills and prairies of Montana and Alberta.
A. m. sigillatum:The traditional 'southern' sub-species (A. m. sigillatum) does not register a mitochondrial genetic identity. This sub-species was identified by Ferguson as forming an integrade with A. m. columbianum in south central Oregon.
Thompson and Russell found another evolutionary lineage that originates in a glacially restricted area of the Salmon River
Mountains, Idaho. With the arrival of the Holocene
interglacial
, approximately 10,000 years ago, the Pleistocene glaciers receded and opened a migratory path linking these southern populations to northern areas where they currently overlap with A. m. krausei and co-migrated north into the Peace River (Canada)
Valley. Ferguson also noted an intergradation
in the same geographic area, but between the morphological sub-species A. m. columbianum and A. m. kraisei that run parallel to the Bitteroot
and Selkirk ranges
. Thompson and Russell suggest that this contact zone is between two different sub-species lineages, because the A. m. columbianum lineage is geographically isolated and restricted to the central Oregon Mountains.
Mole salamander
The mole salamanders are a group of salamanders endemic to North America, the only genus in the family Ambystomatidae...
in the family Ambystomatidae. This species, typically 4.1–8.9 cm (1 3/5–3½ in) long when mature, is characterized by its mottle
Mottle
Mottle or mottling is the appearance of uneven spots. It is commonly used to describe plants or the skin of animals. In plants, mottling usually consists of yellowish spots on plants, and is usually a sign of disease or malnutrition...
d black, brown and yellow pigmentation, and its long outer fourth toe on the hind limbs. Analysis of fossil records, genetics
Genetics
Genetics , a discipline of biology, is the science of genes, heredity, and variation in living organisms....
, and biogeography
Biogeography
Biogeography is the study of the distribution of species , organisms, and ecosystems in space and through geological time. Organisms and biological communities vary in a highly regular fashion along geographic gradients of latitude, elevation, isolation and habitat area...
suggest that A. macrodactylum and A. laterale are descended from a common ancestor that gained access to the western Cordillera with the loss of the mid-continental seaway
Western Interior Seaway
The Western Interior Seaway, also called the Cretaceous Seaway, the Niobraran Sea, and the North American Inland Sea, was a huge inland sea that split the continent of North America into two halves, Laramidia and Appalachia, during most of the mid- and late-Cretaceous Period...
toward the Paleocene
Paleocene
The Paleocene or Palaeocene, the "early recent", is a geologic epoch that lasted from about . It is the first epoch of the Palaeogene Period in the modern Cenozoic Era...
.
The distribution of the long-toed salamander is primarily in the Pacific Northwest
Pacific Northwest
The Pacific Northwest is a region in northwestern North America, bounded by the Pacific Ocean to the west and, loosely, by the Rocky Mountains on the east. Definitions of the region vary and there is no commonly agreed upon boundary, even among Pacific Northwesterners. A common concept of the...
, with an altitudinal range of up to 2800 metres (9,186.4 ft). It lives in a variety of habitats including temperate rainforests, coniferous forests, montane
Montane
In biogeography, montane is the highland area located below the subalpine zone. Montane regions generally have cooler temperatures and often have higher rainfall than the adjacent lowland regions, and are frequently home to distinct communities of plants and animals.The term "montane" means "of the...
riparian zones, sagebrush
Sagebrush (plant)
Sagebrush is the common name for Artemisia tridentata and a number of other species of shrubby plants in the genus Artemisia, native to the North American west and other parts of the world. It is sometimes confused with sage plants ....
plains, red fir
Red Fir
Abies magnifica, the Red Fir or Silvertip fir, is a western North American fir, native to the mountains of southwest Oregon and California in the United States. It is a high altitude tree, typically occurring at altitude, though only rarely reaching tree line...
forests, semi-arid sagebrush, cheatgrass plains, and alpine meadows along the rocky shores of mountain lakes. It lives in slow-moving streams, ponds and lakes during its aquatic breeding
Breeding in the wild
Breeding in the wild is the natural process of animal reproduction occurring in the natural habitat of a given species. This terminology is distinct from animal husbandry or breeding of species in captivity...
phase. The long-toed salamander hibernates during the cold winter months, surviving on protein
Protein
Proteins are biochemical compounds consisting of one or more polypeptides typically folded into a globular or fibrous form, facilitating a biological function. A polypeptide is a single linear polymer chain of amino acids bonded together by peptide bonds between the carboxyl and amino groups of...
energy reserves stored in the skin and tail.
There are five subspecies
Subspecies
Subspecies in biological classification, is either a taxonomic rank subordinate to species, ora taxonomic unit in that rank . A subspecies cannot be recognized in isolation: a species will either be recognized as having no subspecies at all or two or more, never just one...
having different genetic and ecological histories that are phenotypically
Phenotype
A phenotype is an organism's observable characteristics or traits: such as its morphology, development, biochemical or physiological properties, behavior, and products of behavior...
expressed in a range of color and skin patterns. Although the long-toed salamander is classified as a species of Least Concern
Least Concern
Least Concern is an IUCN category assigned to extant taxon or lower taxa which have been evaluated but do not qualify for any other category. As such they do not qualify as threatened, Near Threatened, or Conservation Dependent...
by the IUCN, many forms of land development threaten and negatively affect the salamander's habitat.
Taxonomy
Ambystoma macrodactylum is a member of the Ambystomatidae, also known as the mole salamanders. The Ambystomatidae originated approximately 81 million years ago (late CretaceousCretaceous
The Cretaceous , derived from the Latin "creta" , usually abbreviated K for its German translation Kreide , is a geologic period and system from circa to million years ago. In the geologic timescale, the Cretaceous follows the Jurassic period and is followed by the Paleogene period of the...
) from its sister
Cladistics
Cladistics is a method of classifying species of organisms into groups called clades, which consist of an ancestor organism and all its descendants . For example, birds, dinosaurs, crocodiles, and all descendants of their most recent common ancestor form a clade...
taxon Dicamptodontidae. The Ambystomatidae are also members of suborder Salamandroidea
Salamandroidea
Salamandroidea is a suborder of salamanders, referred to as advanced salamanders. The members of the suborder are found worldwide except for Antarctica, Southern Sahara, and Oceania. They differ from suborder Cryptobranchoidea as their angular and prearticular bones in their lower jaw are fused and...
, which includes all the salamanders capable of internal fertilization. The sister species to A. macrodactylum is A. laterale, distributed in eastern North America. However, the species-level phylogeny
Phylogenetics
In biology, phylogenetics is the study of evolutionary relatedness among groups of organisms , which is discovered through molecular sequencing data and morphological data matrices...
for Ambystomatidae is tentative and in need of further testing.
Description
The body of the long-toed salamander is dusky black with a dorsalDorsum (biology)
In anatomy, the dorsum is the upper side of animals that typically run, fly, or swim in a horizontal position, and the back side of animals that walk upright. In vertebrates the dorsum contains the backbone. The term dorsal refers to anatomical structures that are either situated toward or grow...
stripe of tan, yellow or olive-green. This stripe can also be broken up into a series of spots. The side of the body can have fine white or pale blue flecks. The belly is dark-brown or sooty in color with white flecks. Root tubercle
Tubercle
A tubercle is generally a wart-like projection, but it has slightly different meaning depending on which family of plants or animals it is used to refer to....
s are present, but they are not quite as developed as other species such as the Tiger Salamander
Tiger Salamander
The Tiger Salamander is a species of Mole Salamander. The proper common name is the Eastern Tiger Salamander, to differentiate from other closely related species.-Description:...
.
The egg
Egg (biology)
An egg is an organic vessel in which an embryo first begins to develop. In most birds, reptiles, insects, molluscs, fish, and monotremes, an egg is the zygote, resulting from fertilization of the ovum, which is expelled from the body and permitted to develop outside the body until the developing...
s of this species look similar to those of its cousins, the northwestern salamander (Ambystoma gracile) and the tiger salamander (Ambystoma tigrinum). Like many amphibians, the eggs of the long-toed salamander are surrounded by a gelatinous capsule. This capsule is transparent, making the embryo visible during development. Unlike A. gracile eggs, there are no visible signs of green algae
Green algae
The green algae are the large group of algae from which the embryophytes emerged. As such, they form a paraphyletic group, although the group including both green algae and embryophytes is monophyletic...
, which makes egg jellies green in color. When in its egg, the long-toed salamander embryo
Embryo
An embryo is a multicellular diploid eukaryote in its earliest stage of development, from the time of first cell division until birth, hatching, or germination...
is darker on top and whiter below compared to a tiger salamander embryo that is light brown to grey above and cream-colored on the bottom. The eggs are about 2 mm (0.078740157480315 in) or greater in diameter with a wide outer jelly layer. Prior to hatching—both in the egg and as newborn larva
Larva
A larva is a distinct juvenile form many animals undergo before metamorphosis into adults. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle...
e—they have balancers, which are thin skin protrusions sticking out the sides and supporting the head. The balancers eventually fall off and their external gills grow larger. Once the balancers are lost the larvae are distinguished by the sharply pointed flaring of the gills. As the larvae mature and metamorphose
Métamorphose
"Métamorphose" - a song by French singer Amanda Lear released in 1989 by Carrere Records.- Song information :"Métamorphose" was the first single from Amanda's French-Italian album Tant qu'il y aura des hommes. The album was actually a re-release of Uomini più uomini, and consisted mostly of down-...
, their limbs with digits become visible and the gills are absorbed.
The skin of a larva is mottled with black, brown, and yellow pigmentation. Skin color changes as the larvae develop and pigment cells migrate and concentrate in different regions of the body. The pigment cells are called chromatophore
Chromatophore
Chromatophores are pigment-containing and light-reflecting cells found in amphibians, fish, reptiles, crustaceans, and cephalopods. They are largely responsible for generating skin and eye colour in cold-blooded animals and are generated in the neural crest during embryonic development...
s, which are derived from the neural crest
Neural crest
Neural crest cells are a transient, multipotent, migratory cell population unique to vertebrates that gives rise to a diverse cell lineage including melanocytes, craniofacial cartilage and bone, smooth muscle, peripheral and enteric neurons and glia....
. There are three types of pigment chromatophores in salamanders, including yellow xanthophores, black melanophores, and silvery iridiophores (or guanophores). As the larvae mature the melanophores concentrate along the body and provide the darker background. The yellow xanthophores arrange along the spine and on top of the limbs. The rest of the body is flecked with reflective iridiophores along the sides and underneath.
As larvae metamorphose, they develop digits out of their limb bud protrusions. A fully metamorphosed long-toed salamander has four digits on the front hands and five digits on the rear feet. Its head is longer than it is wide, and the long outer fourth toe on the hind limb of mature larvae and adults distinguishes this species from others and is also the etymological
Etymology
Etymology is the study of the history of words, their origins, and how their form and meaning have changed over time.For languages with a long written history, etymologists make use of texts in these languages and texts about the languages to gather knowledge about how words were used during...
origin of its specific epithet: macrodactylum (Gr. makros = long and Gr. daktylos = toe). The adult skin has a dark brown, dark grey, to black background with a yellow, green, or dull red blotchy stripe with dots and spots along the sides. Underneath the limbs, head, and body the salamander is white, pinkish, to brown with larger flecks of white and smaller flecks of yellow. Adults are typically 3.8 – long.
Habitat and distribution
The long-toed salamander is an ecologically versatile species living in a variety of habitats, ranging from temperate rainforests, coniferous forests, montaneMontane
In biogeography, montane is the highland area located below the subalpine zone. Montane regions generally have cooler temperatures and often have higher rainfall than the adjacent lowland regions, and are frequently home to distinct communities of plants and animals.The term "montane" means "of the...
riparian, sagebrush
Sagebrush (plant)
Sagebrush is the common name for Artemisia tridentata and a number of other species of shrubby plants in the genus Artemisia, native to the North American west and other parts of the world. It is sometimes confused with sage plants ....
plains, red fir
Red Fir
Abies magnifica, the Red Fir or Silvertip fir, is a western North American fir, native to the mountains of southwest Oregon and California in the United States. It is a high altitude tree, typically occurring at altitude, though only rarely reaching tree line...
forest, semi-arid sagebrush, cheatgrass plains, to alpine meadows along the rocky shores of mountain lakes. Adults can be located in forested understory
Understory
Understory is the term for the area of a forest which grows at the lowest height level below the forest canopy. Plants in the understory consist of a mixture of seedlings and saplings of canopy trees together with understory shrubs and herbs...
, hiding under coarse woody debris
Coarse woody debris
Coarse woody debris is a term used in English-speaking countries for fallen dead trees and the remains of large branches on the ground in forests. Some prefer the term coarse woody habitat . A dead standing tree is known as a snag and provides many of the same functions as coarse woody debris...
, rocks, and in small mammal burrows. During the spring breeding season adults can be found under debris or the shoreline shallows of rivers, streams, lakes, and ponds. Ephemeral waters are often frequented.
This species
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
is one of the most widely distributed salamander
Salamander
Salamander is a common name of approximately 500 species of amphibians. They are typically characterized by a superficially lizard-like appearance, with their slender bodies, short noses, and long tails. All known fossils and extinct species fall under the order Caudata, while sometimes the extant...
s in North America, second only to the tiger salamander
Tiger Salamander
The Tiger Salamander is a species of Mole Salamander. The proper common name is the Eastern Tiger Salamander, to differentiate from other closely related species.-Description:...
. Its altitudinal range runs from sea level up to 2800 metres (9,186.4 ft) spanning a wide variety of vegetational zones. The range includes isolated endemic populations in Monterey Bay
Monterey Bay
Monterey Bay is a bay of the Pacific Ocean, along the central coast of California. The bay is south of San Francisco and San Jose, between the cities of Santa Cruz and Monterey....
and Santa Cruz, California
Santa Cruz, California
Santa Cruz is the county seat and largest city of Santa Cruz County, California in the US. As of the 2010 U.S. Census, Santa Cruz had a total population of 59,946...
. The distribution reconnects in northeastern Sierra Nevada, California running continuously along the Pacific Coast
Pacific Coast
A country's Pacific coast is the part of its coast bordering the Pacific Ocean.-The Americas:Countries on the western side of the Americas have a Pacific coast as their western border.* Geography of Canada* Geography of Chile* Geography of Colombia...
to Juneau, Alaska
Juneau, Alaska
The City and Borough of Juneau is a unified municipality located on the Gastineau Channel in the panhandle of the U.S. state of Alaska. It has been the capital of Alaska since 1906, when the government of the then-District of Alaska was moved from Sitka as dictated by the U.S. Congress in 1900...
, with populations dotted along the Taku
Taku River
The Taku River is a river running from British Columbia, Canada, to the northwestern coast of North America, at Juneau, Alaska. Its mouth coincides with the Alaska-British Columbia border...
and Stikine River
Stikine River
The Stikine River is a river, historically also the Stickeen River, approximately 610 km long, in northwestern British Columbia in Canada and southeastern Alaska in the United States...
valleys. From the Pacific coast the range extends longitudinally
Longitude
Longitude is a geographic coordinate that specifies the east-west position of a point on the Earth's surface. It is an angular measurement, usually expressed in degrees, minutes and seconds, and denoted by the Greek letter lambda ....
to the eastern foothills of the Rocky Mountains
Rocky Mountains
The Rocky Mountains are a major mountain range in western North America. The Rocky Mountains stretch more than from the northernmost part of British Columbia, in western Canada, to New Mexico, in the southwestern United States...
in Montana
Montana
Montana is a state in the Western United States. The western third of Montana contains numerous mountain ranges. Smaller, "island ranges" are found in the central third of the state, for a total of 77 named ranges of the Rocky Mountains. This geographical fact is reflected in the state's name,...
and Alberta
Alberta
Alberta is a province of Canada. It had an estimated population of 3.7 million in 2010 making it the most populous of Canada's three prairie provinces...
.
Ecology and life cycle
Eggs
Like all amphibians, the life of a long-toed salamander begins as an egg. In the northern extent of its range, the eggs are laid in lumpy masses along grass, sticks, rocks, or the mucky substrateSubstrate (biology)
In biology a substrate is the surface a plant or animal lives upon and grows on. A substrate can include biotic or abiotic materials and animals. For example, encrusting algae that lives on a rock can be substrate for another animal that lives on top of the algae. See also substrate .-External...
of a calm pond. The number of eggs in a single mass ranges in size, possibly up to 110 eggs per cluster. Females invest a significant amount of resources into egg production, with the ovaries accounting for over 50% of the body mass in the pre-breeding season. A maximum of 264 eggs have been found in a single female—a large number considering each egg is approximately 0.5 millimetre (0.0196850393700787 in) in diameter. The egg mass is held together by a gelatinous outer layer protecting the outer capsule of individual eggs. The eggs are sometimes laid singly, especially in warmer climates south of the Canada and US border. The egg jellies contribute a yearly supply of biological material that supports the chemistry and nutrient dynamics of shallow-water aquatic ecosystem
Aquatic ecosystem
An aquatic ecosystem is an ecosystem in a body of water. Communities of organisms that are dependent on each other and on their environment live in aquatic ecosystems. The two main types of aquatic ecosystems are marine ecosystems and freshwater ecosystems....
s and adjacent forest ecosystems. The eggs also provide habitat for water molds, also known as oomycetes.
Larvae
LarvaLarva
A larva is a distinct juvenile form many animals undergo before metamorphosis into adults. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle...
e hatch from their egg casing in two to six weeks. They are born carnivores, feeding instinct
Instinct
Instinct or innate behavior is the inherent inclination of a living organism toward a particular behavior.The simplest example of an instinctive behavior is a fixed action pattern, in which a very short to medium length sequence of actions, without variation, are carried out in response to a...
ively on small invertebrate
Invertebrate
An invertebrate is an animal without a backbone. The group includes 97% of all animal species – all animals except those in the chordate subphylum Vertebrata .Invertebrates form a paraphyletic group...
s that move in their field of vision. Food items include small aquatic crustacean
Crustacean
Crustaceans form a very large group of arthropods, usually treated as a subphylum, which includes such familiar animals as crabs, lobsters, crayfish, shrimp, krill and barnacles. The 50,000 described species range in size from Stygotantulus stocki at , to the Japanese spider crab with a leg span...
s (cladocera
Cladocera
Cladocera is an order of small crustaceans commonly called water fleas. Around 620 species have been recognised so far, with many more undescribed. They are ubiquitous in inland aquatic habitats, but rare in the oceans. Most are long, with a down-turned head, and a carapace covering the apparently...
ns, copepod
Copepod
Copepods are a group of small crustaceans found in the sea and nearly every freshwater habitat. Some species are planktonic , some are benthic , and some continental species may live in limno-terrestrial habitats and other wet terrestrial places, such as swamps, under leaf fall in wet forests,...
s and ostracod
Ostracod
Ostracoda is a class of the Crustacea, sometimes known as the seed shrimp because of their appearance. Some 65,000 species have been identified, grouped into several orders....
s), aquatic diptera
Diptera
Diptera , or true flies, is the order of insects possessing only a single pair of wings on the mesothorax; the metathorax bears a pair of drumstick like structures called the halteres, the remnants of the hind wings. It is a large order, containing an estimated 240,000 species, although under half...
ns and tadpole
Tadpole
A tadpole or polliwog is the wholly aquatic larval stage in the life cycle of an amphibian, particularly that of a frog or toad.- Appellation :...
s. As they develop, they naturally feed upon larger prey. To increase their chances for survival, some individuals grow bigger heads and become cannibals
Cannibalism (zoology)
In zoology, cannibalism is the act of one individual of a species consuming all or part of another individual of the same species as food. Cannibalism is a common ecological interaction in the animal kingdom and has been recorded for more than 1500 species...
, and feed upon their own brood mates.
Metamorphosis and juveniles
After the larvae grow and mature, for at least one season (the larval period lasts about four months on the Pacific coastPacific Coast
A country's Pacific coast is the part of its coast bordering the Pacific Ocean.-The Americas:Countries on the western side of the Americas have a Pacific coast as their western border.* Geography of Canada* Geography of Chile* Geography of Colombia...
), they absorb their gills and metamorphose
Métamorphose
"Métamorphose" - a song by French singer Amanda Lear released in 1989 by Carrere Records.- Song information :"Métamorphose" was the first single from Amanda's French-Italian album Tant qu'il y aura des hommes. The album was actually a re-release of Uomini più uomini, and consisted mostly of down-...
into terrestrial juveniles that roam the forest undergrowth
Undergrowth
Undergrowth usually refers to the vegetation in a forest, which can obstruct passage through the forest. The height of undergrowth is usually considered to be 0.3 – 3 m . Undergrowth can also refer all vegetation in a forest, which isn't in the canopy....
. Metamorphosis has been reported as early as July at sea level, for A. m. croceum in October to November and even January. At higher elevations the larvae may overwinter
Overwinter
To overwinter is to pass through or wait out the winter season, or to pass through that period of the year when “winter” conditions make normal activity or even survival difficult or near impossible...
, develop, and grow for an extra season before metamorphosing. In lakes at higher elevations, the larvae can reach sizes of 47 millimetres (1.9 in) snout to vent length (SVL) at metamorphosis, but at lower elevations they develop faster and metamorphose when they reach 35 – SVL.
Adults
As adults, long-toed salamanders often go unnoticed because they live a subterranean life-style digging, migrating, and feeding on the invertebrates in forest soils, decaying logs, small rodentRodent
Rodentia is an order of mammals also known as rodents, characterised by two continuously growing incisors in the upper and lower jaws which must be kept short by gnawing....
burrow
Burrow
A burrow is a hole or tunnel dug into the ground by an animal to create a space suitable for habitation, temporary refuge, or as a byproduct of locomotion. Burrows provide a form of shelter against predation and exposure to the elements, so the burrowing way of life is quite popular among the...
s or rock fissure
Fissure
In anatomy, a fissure is a groove, natural division, deep furrow, elongated cleft, or tear in various parts of the body.-Brain:...
s. The adult diet consists of insects, tadpoles, worms, beetles and small fish. Salamanders are preyed upon by garter snakes, small mammals, birds, and fish. An adult may live 6–10 years, with the largest individuals weighing approximately 7.5 gram (0.26455471578834 oz), snout to vent lengths reaching 8 cm (3.1 in), and total lengths reaching 14 cm (5.5 in).
Seasonal
The life historyBiological life cycle
A life cycle is a period involving all different generations of a species succeeding each other through means of reproduction, whether through asexual reproduction or sexual reproduction...
of the long-toed salamander varies greatly with elevation and climate. Seasonal dates of migration to and from the breeding ponds can be correlated with bouts of sustained rainfall, ice thaw, or snow melt sufficient to replenish the (often) seasonal ponds. Eggs may be spawned
Spawn (biology)
Spawn refers to the eggs and sperm released or deposited, usually into water, by aquatic animals. As a verb, spawn refers to the process of releasing the eggs and sperm, also called spawning...
at low elevations as early as mid-February in southern Oregon
Oregon
Oregon is a state in the Pacific Northwest region of the United States. It is located on the Pacific coast, with Washington to the north, California to the south, Nevada on the southeast and Idaho to the east. The Columbia and Snake rivers delineate much of Oregon's northern and eastern...
, from early January to July in northwestern Washington, from January to March in southeastern Washington, and from mid-April to early May in Waterton Lakes National Park
Waterton Lakes National Park
Waterton Lakes National Park is a national park located in the southwest corner of Alberta, Canada, and borders Glacier National Park in Montana, USA. Waterton was Canada's fourth national park, formed in 1895 and named after Waterton Lake, in turn after the Victorian naturalist and conservationist...
, Alberta. The timing of breeding can be highly variable; of notable mention, several egg masses in early stages of development were found on July 8, 1999 along the British Columbia
British Columbia
British Columbia is the westernmost of Canada's provinces and is known for its natural beauty, as reflected in its Latin motto, Splendor sine occasu . Its name was chosen by Queen Victoria in 1858...
provincial border outside Jasper, Alberta
Jasper, Alberta
Jasper is a specialized municipality in western Alberta, Canada. It is the commercial centre of Jasper National Park, located in the Canadian Rockies in the Athabasca River valley....
. Adults migrate seasonally to return to their natal
Birth
Birth is the act or process of bearing or bringing forth offspring. The offspring is brought forth from the mother. The time of human birth is defined as the time at which the fetus comes out of the mother's womb into the world...
breeding ponds, with males arriving earlier and staying longer than females, and some individuals have been seen migrating along snow banks on warm spring days. Gender differences (or sexual dimorphism
Sexual dimorphism
Sexual dimorphism is a phenotypic difference between males and females of the same species. Examples of such differences include differences in morphology, ornamentation, and behavior.-Examples:-Ornamentation / coloration:...
) in this species are only apparent during the breeding season, when mature males display an enlarged or bulbous vent area.
Breeding
Adults aggregate in large numbers (>20 individuals) under rocks and logs along the immediate edge of the breeding sites and breed explosively over a few days. Suitable breeding sites include small fish-free ponds, marshes, shallow lakes and other still-water wetlands. Like other ambystomatid salamanders, they have evolved a characteristic courtship dance where they rub bodies and release pheromones from their chin gland prior to assuming a copulatory mating
Mating
In biology, mating is the pairing of opposite-sex or hermaphroditic organisms for copulation. In social animals, it also includes the raising of their offspring. Copulation is the union of the sex organs of two sexually reproducing animals for insemination and subsequent internal fertilization...
position. Once in position, the male deposits a spermatophore
Spermatophore
A spermatophore or sperm ampulla is a capsule or mass created by males of various animal species, containing spermatozoa and transferred in entirety to the female's ovipore during copulation...
, which is a gooey stalk tipped with a packet of sperm, and walks the female forward to be inseminate
Insemination
Insemination is the deliberate introduction of sperm into the uterus of a mammal or the oviduct of an oviparous animal for the objective of impregnating a female for reproduction...
d. Males may mate more than once and may deposit as many as 15 spermatophores over the course of a five hour period. The courtship dance for the long-toed salamander is similar to other species of Ambystoma and very similar to A. jeffersonianum. In the long-toed salamander, there is no rubbing or head-butting; the males directly approach females and grab on, while the females try to rapidly swim away. The males clasp the female from behind the forelimbs and shake, a behavior called amplexus
Amplexus
Amplexus is a form of pseudocopulation in which a male amphibian grasps a female with his front legs as part of the mating process...
. Males sometimes clasp other amphibian species during breeding and shake them as well. The male only grabs with the front limbs and never uses his hind limbs during the courtship dance as he rubs his chin side to side pressing down on the female's head. The female struggles but later becomes subdued. Males increase the tempo and motions, rubbing over the female's nostrils, sides, and sometimes the vent. When the female becomes quite docile the male moves forward with his tail positioned over her head, raised, and waving at the tip. If the female accepts the males courtship, the male directs her snout toward his vent region while both move forward stiffly with pelvic undulations. As the female follows, the male stops and deposits a spermatophore, and the female will move forward with the male to raise her tail and receive the sperm packet. The full courtship dance is rarely accomplished in the first attempt. Females deposit their eggs a few days after mating.
Energy storage and defense mechanisms
Aposematism
Aposematism , perhaps most commonly known in the context of warning colouration, describes a family of antipredator adaptations where a warning signal is associated with the unprofitability of a prey item to potential predators...
) that it will taste bad. Its skin colors and patterns are diverse, ranging from a dark black to reddish brown background that is spotted or blotched by a pale-reddish-brown, pale-green, to a bright yellow stripe. An adult may also drop part of its tail and slink away while the tail bit acts as a squirmy decoy; this is called autotomy
Autotomy
Autotomy or self amputation is the act whereby an animal severs one or more of its own appendages, usually as a self-defense mechanism designed to elude a predator's grasp...
. The regeneration
Regeneration (biology)
In biology, regeneration is the process of renewal, restoration, and growth that makes genomes, cells, organs, organisms, and ecosystems resilient to natural fluctuations or events that cause disturbance or damage. Every species is capable of regeneration, from bacteria to humans. At its most...
and regrowth of the tail is one example of the developmental physiology
Physiology
Physiology is the science of the function of living systems. This includes how organisms, organ systems, organs, cells, and bio-molecules carry out the chemical or physical functions that exist in a living system. The highest honor awarded in physiology is the Nobel Prize in Physiology or...
of amphibians that is of great interest to the medical profession.
Conservation status
While the long-toed salamander is classified as least concern by the IUCN, many forms of land development negatively affect the salamander's habitat and have put new perspectives and priorities into its conservation biologyConservation biology
Conservation biology is the scientific study of the nature and status of Earth's biodiversity with the aim of protecting species, their habitats, and ecosystems from excessive rates of extinction...
. Conservation priorities focus at the population level of diversity, which is declining at rates ten times that of species extinction. Population level diversity is what provides ecosystem services
Ecosystem services
Humankind benefits from a multitude of resources and processes that are supplied by natural ecosystems. Collectively, these benefits are known as ecosystem services and include products like clean drinking water and processes such as the decomposition of wastes...
, such as the keystone role that salamanders play in the soil ecosystems, including the nutrient cycling that supports wetland and forested ecosystems.
Two life-history features of amphibians are often cited as a reason why amphibians are good indicators of environmental health or 'canaries in the coal mine'. Like all amphibians, the long-toed salamander has both an aquatic and terrestrial life transition and semi-permeable skin. Since they serve different ecological functions in the water than they do in land, the loss of one amphibian species is equivalent to the loss of two ecological species. The second notion is that amphibians, such as long-toed salamanders, are more susceptible to the absorption of pollutants because they naturally absorb water and oxygen through their skin. The validity of this special sensitivity to environmental pollutants, however, has been called into question. The problem is more complex, because not all amphibians are equally susceptible to environmental damage because there is such a diverse array of life histories among species.
Long-toed salamander populations are threatened by fragmentation
Habitat fragmentation
Habitat fragmentation as the name implies, describes the emergence of discontinuities in an organism's preferred environment , causing population fragmentation...
, introduced species
Introduced species
An introduced species — or neozoon, alien, exotic, non-indigenous, or non-native species, or simply an introduction, is a species living outside its indigenous or native distributional range, and has arrived in an ecosystem or plant community by human activity, either deliberate or accidental...
, and UV radiation. Forestry, roads, and other land developments have altered the environments that amphibians migrate to, and have increased mortality
Mortality rate
Mortality rate is a measure of the number of deaths in a population, scaled to the size of that population, per unit time...
. Places such as Waterton Lakes National Park
Waterton Lakes National Park
Waterton Lakes National Park is a national park located in the southwest corner of Alberta, Canada, and borders Glacier National Park in Montana, USA. Waterton was Canada's fourth national park, formed in 1895 and named after Waterton Lake, in turn after the Victorian naturalist and conservationist...
have installed a road tunnel underpass to allow safe passage and to sustain the migration ecology of the species.http://www.pc.gc.ca/eng/pn-np/ab/waterton/natcul/natcul1/w/1.aspx The distribution of the long-toed salamander overlaps extensively with the forestry industry, a dominant resource supporting the economy of British Columbia and the western United States. Long-toed salamanders will alter migration behaviour and are affected negatively by forestry practices not offering sizable management buffers
Riparian buffer
A riparian buffer is a vegetated area near a stream, usually forested, which helps shade and partially protect a stream from the impact of adjacent land uses...
and protections for the smaller wetlands where salamanders breed. Populations near the Peace River Valley
Peace River (Canada)
The Peace River is a river in Canada that originates in the Rocky Mountains of northern British Columbia and flows to the northeast through northern Alberta. The Peace River flows into the Slave River, a tributary of the Mackenzie River. The Mackenzie is the 12th longest river in the world,...
, Alberta, have been lost to the clearing and draining of wetlands for agriculture. Trout
Trout
Trout is the name for a number of species of freshwater and saltwater fish belonging to the Salmoninae subfamily of the family Salmonidae. Salmon belong to the same family as trout. Most salmon species spend almost all their lives in salt water...
introduced for the sport fisheries into once fishless lakes are also destroying long-toed salamander populations. Introduced goldfish predate upon the eggs and larvae of long-toed salamanders. Increased exposure to UVB radiation is another factor being implicated in the global decline of amphibians and the long-toed salamander is also susceptible to this threat, which increases the incidence of deformities and reduces their survival and growth rates.
The subspecies Ambystoma macrodactylum croceum (Santa Cruz Long-toed Salamander
Santa Cruz Long-toed Salamander
The Santa Cruz long-toed salamander is an endangered subspecies of the long-toed salamander, which is found only close to a few isolated ponds in Santa Cruz County and Monterey County, California. It has a black body, broken yellow or orange irregular striping along its spine, and a tail fin well...
) is of particular concern and it was afforded protections in 1967 under the US Endangered Species Act
Endangered Species Act
The Endangered Species Act of 1973 is one of the dozens of United States environmental laws passed in the 1970s. Signed into law by President Richard Nixon on December 28, 1973, it was designed to protect critically imperiled species from extinction as a "consequence of economic growth and...
. This sub-species lives in a narrow range of habitat in Santa Cruz County
Santa Cruz County, California
Santa Cruz County is a county located on the Pacific coast of the U.S. state of California, on the California Central Coast. The county forms the northern coast of the Monterey Bay. . As of the 2010 U.S. Census, its population was 262,382. The county seat is Santa Cruz...
and Monterey County, California. Prior to receiving protections, some few remaining populations were threatened by development. The sub-species is ecologically unique, having unique and irregular skin patterns on its back, a unique moisture tolerance, and it is also an endemic that is geographically isolated from the rest of the species range. Other subspecies include A. m. columbianum, A. m. krausei, A. m. macrodactylum and A. m. sigillatum.
Evolutionary origins
The ancestral origins for this species stem from eastern North AmericaNorth America
North America is a continent wholly within the Northern Hemisphere and almost wholly within the Western Hemisphere. It is also considered a northern subcontinent of the Americas...
, where species richness
Species richness
Species richness is the number of different species in a given area. It is represented in equation form as S.Species richness is the fundamental unit in which to assess the homogeneity of an environment. Typically, species richness is used in conservation studies to determine the sensitivity of...
of ambystomatids are highest. The following biogeographic
Biogeography
Biogeography is the study of the distribution of species , organisms, and ecosystems in space and through geological time. Organisms and biological communities vary in a highly regular fashion along geographic gradients of latitude, elevation, isolation and habitat area...
interpretation on the origins of A. macrodactylum into western North America is based on a descriptive account of fossils, genetics, and biogeography. The long-toed salamander's closest living sister species is A. laterale, a native to northeastern North America. Ambystomatidae was isolated to the southeast of the mid-Continental or Western Interior Seaway
Western Interior Seaway
The Western Interior Seaway, also called the Cretaceous Seaway, the Niobraran Sea, and the North American Inland Sea, was a huge inland sea that split the continent of North America into two halves, Laramidia and Appalachia, during most of the mid- and late-Cretaceous Period...
during the Cretaceous
Cretaceous
The Cretaceous , derived from the Latin "creta" , usually abbreviated K for its German translation Kreide , is a geologic period and system from circa to million years ago. In the geologic timescale, the Cretaceous follows the Jurassic period and is followed by the Paleogene period of the...
(~145.5–65.5 Ma). While three other species of the Ambystomatidae (A. tigrinum, A. californiense, and A. gracile) have overlapping ranges in western North America, the long-toed salamander's closest living sister species is A. laterale, a native to northeastern North America. It has been suggested that A. macrodactylum speciated
Speciation
Speciation is the evolutionary process by which new biological species arise. The biologist Orator F. Cook seems to have been the first to coin the term 'speciation' for the splitting of lineages or 'cladogenesis,' as opposed to 'anagenesis' or 'phyletic evolution' occurring within lineages...
from A. laterale after the Paleocene
Paleocene
The Paleocene or Palaeocene, the "early recent", is a geologic epoch that lasted from about . It is the first epoch of the Palaeogene Period in the modern Cenozoic Era...
(~65.5–55.8 Ma) with the loss of the Western Interior Seaway
Western Interior Seaway
The Western Interior Seaway, also called the Cretaceous Seaway, the Niobraran Sea, and the North American Inland Sea, was a huge inland sea that split the continent of North America into two halves, Laramidia and Appalachia, during most of the mid- and late-Cretaceous Period...
opening an access route for a common ancestor into the Western Cordillera. Once situated in the montane regions of western North America, species had to contend with a dynamic spatial and compositional ecology responding to the changes in altitude, as mountains grew and the climate changed. For example, the Pacific Northwest
Pacific Northwest
The Pacific Northwest is a region in northwestern North America, bounded by the Pacific Ocean to the west and, loosely, by the Rocky Mountains on the east. Definitions of the region vary and there is no commonly agreed upon boundary, even among Pacific Northwesterners. A common concept of the...
became cooler in the Paleocene
Paleocene
The Paleocene or Palaeocene, the "early recent", is a geologic epoch that lasted from about . It is the first epoch of the Palaeogene Period in the modern Cenozoic Era...
, paving the way for temperate forest
Temperate forest
Temperate forests correspond to forest concentrations formed in the northern hemisphere. Main characteristics include: wide leaves, big and tall trees and non seasonal vegetation...
to replace the warmer tropical forest of the Cretaceous
Cretaceous
The Cretaceous , derived from the Latin "creta" , usually abbreviated K for its German translation Kreide , is a geologic period and system from circa to million years ago. In the geologic timescale, the Cretaceous follows the Jurassic period and is followed by the Paleogene period of the...
. A scenario for the splitting of A. macrodacylum and other western temperate species from their eastern counterparts involves Rocky Mountain uplift in the late Oligocene
Oligocene
The Oligocene is a geologic epoch of the Paleogene Period and extends from about 34 million to 23 million years before the present . As with other older geologic periods, the rock beds that define the period are well identified but the exact dates of the start and end of the period are slightly...
into the Miocene
Miocene
The Miocene is a geological epoch of the Neogene Period and extends from about . The Miocene was named by Sir Charles Lyell. Its name comes from the Greek words and and means "less recent" because it has 18% fewer modern sea invertebrates than the Pliocene. The Miocene follows the Oligocene...
. The orogeny
Orogeny
Orogeny refers to forces and events leading to a severe structural deformation of the Earth's crust due to the engagement of tectonic plates. Response to such engagement results in the formation of long tracts of highly deformed rock called orogens or orogenic belts...
created a climatic barrier by removing moisture from the westerly air stream and dried the midcontinental area, from southern Alberta to the Gulf of Mexico.
Ancestors of contemporary salamanders were likely able to disperse and migrate into habitats of the Rocky Mountains
Rocky Mountains
The Rocky Mountains are a major mountain range in western North America. The Rocky Mountains stretch more than from the northernmost part of British Columbia, in western Canada, to New Mexico, in the southwestern United States...
and surrounding areas by the Eocene
Eocene
The Eocene Epoch, lasting from about 56 to 34 million years ago , is a major division of the geologic timescale and the second epoch of the Paleogene Period in the Cenozoic Era. The Eocene spans the time from the end of the Palaeocene Epoch to the beginning of the Oligocene Epoch. The start of the...
. Mesic forests were established in western North America by the mid Eocene
Eocene
The Eocene Epoch, lasting from about 56 to 34 million years ago , is a major division of the geologic timescale and the second epoch of the Paleogene Period in the Cenozoic Era. The Eocene spans the time from the end of the Palaeocene Epoch to the beginning of the Oligocene Epoch. The start of the...
and attained their contemporary range distributions by the early Pliocene
Pliocene
The Pliocene Epoch is the period in the geologic timescale that extends from 5.332 million to 2.588 million years before present. It is the second and youngest epoch of the Neogene Period in the Cenozoic Era. The Pliocene follows the Miocene Epoch and is followed by the Pleistocene Epoch...
. The temperate forest valleys and montane
Montane
In biogeography, montane is the highland area located below the subalpine zone. Montane regions generally have cooler temperatures and often have higher rainfall than the adjacent lowland regions, and are frequently home to distinct communities of plants and animals.The term "montane" means "of the...
environments of these time periods (Paleogene
Paleogene
The Paleogene is a geologic period and system that began 65.5 ± 0.3 and ended 23.03 ± 0.05 million years ago and comprises the first part of the Cenozoic Era...
to Neogene
Neogene
The Neogene is a geologic period and system in the International Commission on Stratigraphy Geologic Timescale starting 23.03 ± 0.05 million years ago and ending 2.588 million years ago...
) would have provided the physiographic and ecological features supporting analogs of contemporary Ambystoma macrodactylum habitats. The Cascade Range
Cascade Range
The Cascade Range is a major mountain range of western North America, extending from southern British Columbia through Washington and Oregon to Northern California. It includes both non-volcanic mountains, such as the North Cascades, and the notable volcanoes known as the High Cascades...
rose during the mid Pliocene
Pliocene
The Pliocene Epoch is the period in the geologic timescale that extends from 5.332 million to 2.588 million years before present. It is the second and youngest epoch of the Neogene Period in the Cenozoic Era. The Pliocene follows the Miocene Epoch and is followed by the Pleistocene Epoch...
and created a rain shadow effect causing the xerification of the Columbia Basin
Columbia Basin
The Columbia Basin, the drainage basin of the Columbia River, occupies a large area–about —of the Pacific Northwest region of North America. In common usage, the term often refers to a smaller area, generally the portion of the drainage basin that lies within eastern Washington.Usage of the term...
and also altered ranges of temperate mesic ecosystems at higher elevations. The rise of the Cascades causing the xerification of the Columbia Basin is a major biogeographic feature of western North America that divided many species, including A. macrodactylum, into coastal and inland lineages.
Subspecies
There are five subspeciesSubspecies
Subspecies in biological classification, is either a taxonomic rank subordinate to species, ora taxonomic unit in that rank . A subspecies cannot be recognized in isolation: a species will either be recognized as having no subspecies at all or two or more, never just one...
of long-toed salamander. The subspecies are discerned by their geographic location and patterns in their dorsal stripe pattern; Denzel Ferguson gives a biogeographic account of skin patterns, morphology, and based on this analysis he introduced two new sub-species, A. macrodactylum columbianum and A. m. sigillatum. The ranges of sub-species are illustrated in Robert Stebbin's amphibian field guides.
Physical appearance (phenotypes)
Summary of distinguishing skin patterns and morphological features for the subspecies include:A. m. croceum: Orange dorsal color on tail breaking into patches along black body and into tiny dots on head, often absent anterior to eyes. Sides have whitish flecks. Number of costal groove
Costal groove
The Costal groove is a groove between the ridge of the internal surface of the rib and the inferior border. It contains the intercostal vessels and intercostal nerve....
s equals 13.
A. m. columbianum: Yellow to tan dorsal stripe on black body continuous blotches to spots along body ending in narrowed blotches with spot patterns distributed on the head. White flecks along sides and underside remaining as separate small flecks. Number of vomerine teeth greater than 35.
A. m. krausei: Yellow to tan dorsal stripe continuous blotches to spots along body ending in widened blotches with spot patterns distributed on the head. White flecks along sides and underside remaining as separate small flecks. Number of vomerine teeth equaling 32. Number of costal grooves equals 12.
A. m. sigillatum: Wax yellow to tan dorsal stripe forming spotty to irregular shaped blotches along body ending in dots or specks of dorsal color on head. Number of vomerine teeth equals 44. Number of costal grooves equals 13.
A. m. macrodactylum: Citrine, dull citrine, to tan dorsal stripe that is diffuse and continuous along grayish body. Pattern ending in diffuse specks of stripe color or absent on head and snout. White flecks on sides sometimes coming together to form larger flecks. Number of vomerine teeth equaling 33, forming a distinguished transverse arc. Number of costal grooves equals 13.
Biogeography and genetics
Mitochondrial DNAMitochondrial DNA
Mitochondrial DNA is the DNA located in organelles called mitochondria, structures within eukaryotic cells that convert the chemical energy from food into a form that cells can use, adenosine triphosphate...
analysis identifies somewhat different ranges for the subspecies lineages. The genetic analysis, for example, identifies an additional pattern of deep divergence in the eastern part of the range. The spatial distribution of populations and genetics of this species links spatially and historically through the interconnecting mountain and temperate valley systems of western North America. The breeding fidelity of long-toed salamanders (philopatry
Philopatry
Broadly, philopatry is the behaviour of remaining in, or returning to, an individual's birthplace. More specifically, in ecology philopatry is the behaviour of elder offspring sharing the parental burden in the upbringing of their siblings, a classic example of kin selection...
) and other migratory behaviours reduce rates of dispersal among regions, such as within mountain basins. This aspect of their behavior restricts gene flow
Gene flow
In population genetics, gene flow is the transfer of alleles of genes from one population to another.Migration into or out of a population may be responsible for a marked change in allele frequencies...
and increases the degree and rates of genetic differentiation. Genetic differentiation among regions is higher in the long-toed salamander than measured in most other vertebrate
Vertebrate
Vertebrates are animals that are members of the subphylum Vertebrata . Vertebrates are the largest group of chordates, with currently about 58,000 species described. Vertebrates include the jawless fishes, bony fishes, sharks and rays, amphibians, reptiles, mammals, and birds...
groups. Natural breaks in the range of dispersal and migration occur where ecosystems grade into drier xeric low-lands (such as prairie
Prairie
Prairies are considered part of the temperate grasslands, savannas, and shrublands biome by ecologists, based on similar temperate climates, moderate rainfall, and grasses, herbs, and shrubs, rather than trees, as the dominant vegetation type...
climates) and at frozen or harsher terrain at high elevation extremes (2200 metres (7,217.8 ft)).
A. m. columbianum:Genetic evidence for the 'central' subspecies (A. m. columbianum) suggests that it does not extend north into British Columbia, but is restricted to the Blue
Blue Mountains (Oregon)
The Blue Mountains are a mountain range in the western United States, located largely in northeastern Oregon and stretching into southeastern Washington...
and Wallowa Mountains
Wallowa Mountains
The Wallowa Mountains are a mountain range located in the Columbia Plateau of northeastern Oregon in the United States. The range runs approximately 40 mi northwest to southeast in southwestern Wallowa County between the Blue Mountains to the west and the Snake River to the east. The range is...
of central to northeastern sections of Oregon. Populations are restricted to these areas by the Snake River Canyon (Idaho)
Snake River Canyon (Idaho)
Snake River Canyon is a large canyon formed by the Snake River in the Magic Valley region of southern Idaho. It is well known as the site of an unsuccessful 1974 attempt by Evel Knievel to jump it in the Skycycle X-2....
to the east and low dry or xeric lands in the Madras basin
Madras, Oregon
Madras is a city in Jefferson County, Oregon, United States. Originally called The Basin after the circular valley the city is located in, it is unclear as to whether Madras was named in 1903 for the cotton fabric called "Madras" that originated in the Madras area in India, or from the city of...
to the west.
A. m. macrodactylum:The 'coastal' or 'western' subspecies (A. m. macrodactylum) lineage extends north from northeastern California, across the Klamath Siskiyou Range, through the Willamette Valley
Willamette Valley
The Willamette Valley is the most populated region in the state of Oregon of the United States. Located in the state's northwest, the region is surrounded by tall mountain ranges to the east, west and south and the valley's floor is broad, flat and fertile because of Ice Age conditions...
, along the coastal mountain ranges, including the Cascade Mountains, and continuing north through British Columbia and up into Alaska.
A. m. croceum:The Santa Cruz salamander (A. m. croceum) is most closely related to the 'coastal' or 'western' subspecies. This conclusion is the most parsimonious biogeographic explanation
Explanation
An explanation is a set of statements constructed to describe a set of facts which clarifies the causes, context, and consequencesof those facts....
with nearest populations of A. m. macrodactylum separated by approximately 300 km across the Sacramento-San Joaquin River Delta, California. The isolated endemic populations in California, the Santa Cruz Long-toed Salamander
Santa Cruz Long-toed Salamander
The Santa Cruz long-toed salamander is an endangered subspecies of the long-toed salamander, which is found only close to a few isolated ponds in Santa Cruz County and Monterey County, California. It has a black body, broken yellow or orange irregular striping along its spine, and a tail fin well...
(Ambystoma macrodactlylum croceum), are listed as an endangered sub-species. Based on the biogeography and molecular clock calibrations, this sub-species may have been separated from the remainder of the distribution since the Miocene, molecular clock
Molecular clock
The molecular clock is a technique in molecular evolution that uses fossil constraints and rates of molecular change to deduce the time in geologic history when two species or other taxa diverged. It is used to estimate the time of occurrence of events called speciation or radiation...
calibrations estimating 13.9 million years of separation.
A. m. krausei:The 'eastern' subspecies (A. m. krausei) range is distributed throughout the interior mountains, with the western extent of its range encroaching into the low-land areas of the central interior plateau of Washington and British Columbia and the eastern extent of its range pushing through Rocky Mountain valleys into the low-land foothills and prairies of Montana and Alberta.
A. m. sigillatum:The traditional 'southern' sub-species (A. m. sigillatum) does not register a mitochondrial genetic identity. This sub-species was identified by Ferguson as forming an integrade with A. m. columbianum in south central Oregon.
Thompson and Russell found another evolutionary lineage that originates in a glacially restricted area of the Salmon River
Salmon River (Idaho)
The Salmon River is located in Idaho in the northwestern United States. The Salmon is also known as The River of No Return. It flows for through central Idaho, draining and dropping more than between its headwaters, near Galena Summit above the Sawtooth Valley in the Sawtooth National...
Mountains, Idaho. With the arrival of the Holocene
Holocene
The Holocene is a geological epoch which began at the end of the Pleistocene and continues to the present. The Holocene is part of the Quaternary period. Its name comes from the Greek words and , meaning "entirely recent"...
interglacial
Interglacial
An Interglacial period is a geological interval of warmer global average temperature lasting thousands of years that separates consecutive glacial periods within an ice age...
, approximately 10,000 years ago, the Pleistocene glaciers receded and opened a migratory path linking these southern populations to northern areas where they currently overlap with A. m. krausei and co-migrated north into the Peace River (Canada)
Peace River (Canada)
The Peace River is a river in Canada that originates in the Rocky Mountains of northern British Columbia and flows to the northeast through northern Alberta. The Peace River flows into the Slave River, a tributary of the Mackenzie River. The Mackenzie is the 12th longest river in the world,...
Valley. Ferguson also noted an intergradation
Intergradation
In zoology, intergradation is the way in which two distinct subspecies are connected via areas where populations are found that have the characteristics of both...
in the same geographic area, but between the morphological sub-species A. m. columbianum and A. m. kraisei that run parallel to the Bitteroot
Bitterroot Range
The Bitterroot Range runs along the border of Montana and Idaho in the northwestern United States. The range spans an area of 62,736 square kilometers and is named after the bitterroot , a small pink flower that is the state flower of Montana.- History :In 1805, the Corps of Discovery,...
and Selkirk ranges
Selkirk Mountains
The Selkirk Mountains are a mountain range spanning the northern portion of the Idaho Panhandle, eastern Washington, and southeastern British Columbia. They begin at Mica Peak near Coeur d'Alene, Idaho and extend approximately 320 km north from the border. The range is bounded on its west,...
. Thompson and Russell suggest that this contact zone is between two different sub-species lineages, because the A. m. columbianum lineage is geographically isolated and restricted to the central Oregon Mountains.