NORTH AMERICAN SALAMANDERS FOUND ONLY IN CAVES

There are ten species of Plethodontidae found only in caves.These species seem to be glacial relicts. The majority of North American troglophilic Plethodontidae are members of the Boletoglossinae. In Europe, subterranean plethodontidsare represented only by

Hydromantes

(see the followingsection).

Eurycea

Several stygobitic

Eurycea

are restricted to Edward’s Plateau,TX. They are characterized by small size, elongated shape, along tail, a mobile lower mandible, the absence of lungs,a nasolabial furrow, and internal fertilization. There is amorphological continuum from the neotenic epigean forms(

E. pterophila

and

E. nana

) to the troglophilic forms (

E.neotenes

), then troglobitic forms (

E. latitans, E. troglodytes, E.tridentifera

) to the most highly evolved,

E. rathbuni

(Fig. 1).All

Eurycea

seem to have a common

Proeurycea

ancestor(Wake, 1966). The existing continuum between various

Eurycea

of Edward’s Plateau is related to their morphological,physiological, and behavioral preadaptations and adaptationsto aphotic underground life.

Eurycea latitans

, the Cascade Cavern salamander, is theleast specialized of the stygobitic species observed in fourcaves in Kendall County, Texas (Cascade Cavern, CascadeSinkhole, Dead Man’s Cave, and Century Cavern). Itscharacteristics include a length of 64–105 mm, a groovedtrunk with short legs, four fingers and five toes, and it is fourto five times longer than it is wide. This species of salamanderhas clear coloring with delimited pigmented patches. Thehead is less globulous than that of

E. neotenes

, with aflattened snout and a truncated brow followed by a markedexpansion of the face, 14–15 costal grooves, and 17–18presacral vertebrae. There are three gills on each side of thehead; with the reduction in size of the eyes, the orbital

Salamanders

Jacques Pierre Durand

Laboratoire Souterrain, France

everal lineages of salamanders have evolved to becomeobligate inhabitants of caves. These independently evolvedlineages possess characteristics similar to those of otheranimals that have become adapted for life inside cavesor within underground waterways. For example, cavesalamanders lack or have much reduced pigmentation, havereduced or absent eyes and associated structures, possesselongated and flattened bodies with longer and more gracilelimbs, and possess several physiological and reproductivespecializations — all related to a subterranean lifestyle. Theseobservations underscore that salamanders are excellentmodels for studying common morphological andphysiological specializations for underground life.There are several different life cycles that are played out insubterranean ecosystems. Those animals that spend theirentire lives within caves are referred to as troglobionts ortroglobites. There are also animals that spend only a part of their lives in caves, either intentionally or accidentally, andthese organisms are called troglophiles or troglophilic. Thepreﬁx troglo- refers to the Greek “troglodytes” — one whocreeps in holes. There are also organisms that live in under-ground waterways (some of these waterways are not caves)called stygobionts or stygobites. The preﬁx stygo- refers tothe mythological River Styx, which must be crossed to reachthe world of the dead.Not all of the eight common families of salamandersinclude underground-adapted taxa. Salamanders restricted tocaves, i.e., those that live their entire lives in caves, belong tothe Plethodontidae and Proteidae families. Salamanders thatspend only part of their lives in caves are plethodontids, butthere are also some Salamandridae.

485

depression becomes increasingly visible. The eyes are underthe skin but are not more than 1 mm in diameter.

Eurycea troglodytes

, Valdinia Farm salamander populations,are isolated in the deep wells and the brooks of an under-ground water system of the Edward’s Plateau. Their charac-teristics include an average body length of 78 mm andreduced eyes (0.7–0.9 mm) covered by skin. They have abroader head with head-body limits more clearly deﬁnedthan in

E. tridentifera

and

E. rathbuni

, 13–14 rib grooves,and 18 presacral vertebrae. Their legs measure 5 –11 timesmore in length than in width with almost white coloring andtranslucent skin on the belly. These animals live in cave poolswhose banks are rich in guano and invertebrates, submergedat the time of high waters of the underground streams.

Typhlomolge

is a species synonymous with

Euryceatridentifera

Eurycea tridentifera

lives in caves of the Edward’sPlateau, such as Honey Creek Cave in the Comal Countiesof Texas. Its characteristics include depigmentation andblindness, persistent red external gills, and fused premaxillae.Nasals and prefrontals are absent. It has 11–12 costal groovesand 13–14 vertebrae.

Eurycea tridentifera

has a ﬁnned tailwith basal constriction. Its limbs are 8–13 times longer thanwide. Its eyes are small (0.6 mm) but visible. The head iswider than the body (40%), but not as much as in

E.rathbuni

. The muzzle is abrupt and truncated at the level of the nostrils. The body is white with a little gray and orangepigment.

Eurycea rathbuni

(Fig. 2), the Texas blind salamander, livesin underground brooks and phreatic groundwater. Some-times ejected from artesian wells, populations are isolated inthe aquifers and the underground rivers (artesian well in SanMarcos, Ezell’s Cave, Frank Johnson’s well, and Wonder Cavein Edward’s Plateau, TX). They live in water where foodis scarce. Their characteristics include a longer body, a very depressed orbit, and a more angular head than in other

Eurycea

. The adults are blind, unpigmented, and neotenic,with long thin members. The skin-covered eye is vestigial.The lens, the vitreous body, and the ocular muscles are absentand the retina is disorganized. They are 30–120 mm long.Sexual maturity for these oviparous animals is reachedaround 40–50 mm. Their metamorphosis obtained inexperiments is partial. The females have 17–22 eggs perovary. The larvae and the young (10–30 mm length) show gray dorsal pigmentation. The apparent eyes are black andcovered by a transparent cornea (Fig. 3).

Eurycea rathbuni

has a developed lateral line, long thin legs, an extremely flat muzzle, and white body, except for the gills, which arecolored by blood. The tail attains 50% of the total length andthe head 16%.

Eurycea robusta

, the Blanco blind salamander, lives in theBalcones aquifer north and east of the Blanco River in HaysCounty, TX.

Typhlotriton

The Grotto salamander or Ozark blind salamander, lives inthe caves of the Southwestern Ozark Plateau (Rock HouseCave and Marble Cave), Missouri, Kansas, Oklahoma, andArkansas where it is rather common. Some larvae occur

486

Salamanders

FIGURE 1

The

Eurycea

salamander series. Note the progressive widening of the head, the lengthening of the body and limbs, and the sinking of the orbitrelated to the reduction in size of the eyes. These modifications areprogressive from species living on the surface to the most specializedstygobiont, and finally to neotenic or perennibranchiate forms. Thisadaptive pattern is convergent with that of troglobionts from very differentfamilies such as the Proteidae (Modified from Mitchell and Reddel, (1965)).

FIGURE 2

Eurycea rathbuni

. This North American stygobiont is one of themost specialized. Note the angular head, the orbit and the eyes, which havedisappeared, the permanent gills reddened by blood, and very elongated thinlimbs. (Photo by R. W. Mitchell. Magniﬁcation

2.5.)

in springs.

Typhlotriton braggi

and

T. nereus

are synonyms for

T. spelaeus

. Only one species,

T. spelaeus,

is blind andunpigmented.

Typhlotriton spelaeus

differs from

Eurycea

inthat it metamorphoses. Characteristics include 18–19 costalfurrows instead of 14–15 and 17–20 vertebrae instead of 15–16. The tongue is attached to the oral floor. Its lengthis 72–120 mm with a broad head and tail 42–47% of itstotal length. The adult (Fig. 4) is pale yellow; the belly skin is lighter. Like all plethodontids lungs are absent. Thissalamander is terrestrial and is able to use cutaneous andbuccal respiration only in very wet environments. Conse-quently, it is observed only inside cavities where moisture andfood are abundant.Typhlotriton reproduction takes place between March andAugust. The females isolate themselves, and the whole cycletakes place in caves where guano is present and whereamphipods and flatworms are abundant. Generally theyoung larvae (17 mm) migrate toward the twilight of thecave entrance or outside where food is more abundant. Insprings, the larvae are pigmented (Fig. 5). In the old larvae(from 80 to 110 mm length) the dorsal and side pigmenta-tion varies from light gray to dark gray with yellow spotson the base of the back and the tail. The branchiae arecolored pink by blood. The functional eyes measure 3 mm indiameter; the head is 25% wider than the trunk. The tailcomprises 50% of body length with a corrugated caudalmembrane. After 3–5 years of aquatic life, the animalsmetamorphose and gills regress

. Typhlotriton spelaeus

becomesaerial and enters caves. The upper eyelid covers the lowereyelid and an ocular cyst is inserted. In

Typhlotriton

as in

Proteus

, the ocular degeneration is genetic. It is one of therare examples where an animal, during its existence, passesfrom surface life to cavernicolous life, and from aquatic lifeto air-breathing life, a process related to the thyroxinianclimax, which is accompanied by morphological, physiolo-gical, behavioral, and sensory transformations. The rarity of food accompanied by underground darkness result in anincrease of the larval life span and an increase in the size of the larvae. So the penetration to the moist underground isobligatory for the adult for respiratory and reproductivereasons.

Haideotriton

For a long time only one specimen of

Haideotriton wallacei

,the Georgia blind salamander, had been collected — anoviparous female, ejected from a water pump in Albany,in south Georgia. Now specimens have also been found inseveral caves and the groundwater in Jackson County innorthern Florida.This salamander is a Plethodontidae perennibranch(28–76 mm, from the nose to the cloaca).

Haideotriton

has external gills and, like all plethodontids, no lungs. The

Salamanders

487

FIGURE 3

Larva of

E. rathbuni

, length 17 mm. Note the existence (as in

Proteus

larva) of some dorsal pigmentation and eyes whose pigmentary epithelium of the retina is black. Above the eye, the cutaneocornealepithelium is semitransparent. In troglobionts, ocular decay is irreversible.(Photo by Maruska. Magniﬁcation

6.5.)

FIGURE 4

Adult

T. spelaeus,

at the time when it metamorphoses, comes outof water and loses its gills. No lungs are present; respiration occurs throughthe skin and within the buccal cavity, which must remain wet. To make thispossible,

T. spelaeus

seeks moisture, entering caves and becoming a truetroglobiont whose eyes and pigmentation degenerate. This is a uniqueexample of morphological and physiological adaptive modiﬁcationsoccurring during the life of one individual. This has been correlated with thepresence of thyroxin in the blood. (Photo by J. Durand. Magniﬁcation

2.5)

FIGURE 5

Larva of

T. spelaeus

. Before metamorphosis (from 3 to 7 years)the larva of

Typhlotriton

is often observed in springs, exposed to light whereit forages. Its eyes are large and functional at this time. (Photo by J. Durand.Magniﬁcation