S

SALAMANDERSSpela Goricki,* Matthew L. Niemiller,† and

Dante B. Fenolio‡

*University of Maryland, †University of Tennessee,‡Atlanta Botanical Garden

Salamanders are a diverse group of vertebrates, exploit-ing moist cool habitats in a variety of ways. Severallineages have colonized subterranean habitats, particu-larly in regions of climatic extremes. Salamanders associ-ated with karst exhibit differences in the amount of timethey spend in subterranean habitats, their dependenceon these resources, and morphological and behavioraladaptations to life underground (troglomorphisms).Differences are manifested within and across taxonomicgroups as well as between geographical regions. NorthAmerica and Europe host the greatest number of knowncave-dwelling species. Cave-dwelling salamanders mayinhabit subterranean environments for significant por-tions of their life cycle but not all of it, others migrate tothe surface periodically, and still others are exclusivelyfound underground. Sources of general information onsalamanders are Amphibia Web (2011), Grossenbacherand Thiesmeier (1999), and Lannoo (2005).

Salamanders are the only tetrapods that exhibit anexclusive subterranean existence. Such troglobitic sala-manders belong to the families Plethodontidae (in NorthAmerica) and Proteidae (in Europe). Troglomorphismsseen in troglobitic salamanders vary from species to spe-cies and even from locality to locality, but they frequentlyinclude reduced eyes and pigmentation, reduced numberof trunk vertebrae, elongated appendages, and modifiedhead shape with increased dentition. Salamanders areopportunistic predators, feeding on a variety of smallinvertebrates and will often also consume their own kind.There are records of notable dietary oddities in troglobiticsalamanders, including feeding on bat guano and silt.Troglobitic salamanders are usually found in caves wherefishes do not occur, and function as top predators inthose subterranean waters. Because of the constant water

temperatures in their habitat, they are likely active year-round. For orientation, feeding, and mating, they rely onmechano- and chemosensory cues, which corresponds toprogressive development of extraoptic sensory systems.Salamanders from subterranean environments usuallyhave lower metabolism, efficient energy (fat) storage, anda longer life span than their surface counterparts. Theyhave fewer, larger eggs and offspring compared torelated surface-dwelling species. The rate of developmentin amphibians strongly depends on environmental fac-tors, most notably ambient temperature. When comparedwith related epigean species that reproduce at the samewater temperature, troglobitic salamanders usuallydevelop more slowly. All begin their life inside a gelati-nous egg capsule, deposited in water. Eggs hatch into free-swimming aquatic larvae, with visible bushy gills and atailfin. Instead of metamorphosing into mature adults,however, most troglobitic salamanders attain sexual matu-rity while retaining these and other larval characteristics—a condition known as neoteny or paedomorphism.

We can only speculate about the origins and timerequired for the evolution of obligate subterranean exis-tence. While the ancestors of some troglobitic species mayhave colonized caves as early as in the Miocene, it is morelikely that subterranean colonization occurred much later,even as late as during the Pleistocene. Salamanderfossils are rare and the oldest found that may belong to acave-dwelling species date to the Pleistocene.

The following sections portray all ten currentlydescribed troglobitic salamanders. Accounts also areprovided for their close relatives that show affinities tosubterranean habitats.

OLMS AND WATERDOGS (PROTEIDAE)

The family includes six species of surface-dwellingmudpuppies or waterdogs (Necturus sp.) from easternand central North America and the troglobitic olm(Proteus anguinus) found in southeastern Europe. These

665Encyclopedia of Caves. © 2012 Elsevier Inc. All rights reserved.

salamanders are aquatic throughout their life, retainingexternal gills, but are also able to breathe air throughtheir skin and with their sac-like lungs. All representa-tives of this family are obligate paedomorphs; paedo-morphism in Proteus is thus seemingly not a result ofconditions particular to the subterranean environment.Thyroid glands, which control metamorphosis, arefunctional in all species of this family. Metamorphosiscannot be induced artificially, although changes in theskin structure toward a metamorphosed form havebeen observed in Proteus. Furthermore, it has beenshown that Necturus possesses functional thyroid hor-mone receptors and its tissues are not generally irre-sponsive to the hormone (Safi et al., 2006). Rather, theabsence of metamorphosis may be due to loss of func-tion of thyroid hormone-dependent genes required fortissue transformation.

Olm (Proteus anguinus)

The olm (Proteus anguinus) is the only European obli-gate cave-dwelling vertebrate. It has been found inover 250 springs and caves in the Dinaric karst on thewestern Balkan Peninsula, between the rivers Isonzo/Soca (northeastern Italy) and Trebisnjica (Bosnia andHerzegovina). Several populations, however, have beendestroyed or severely diminished by dam construction,earth fill, or pollution. The salamander inhabits karstwaters from close to the surface to deep in fissures.During flooding or at night it may be found in caveentrances or short distances away from springs.

This elongated salamander reaches 25 cm in totallength, although 40-cm-long individuals have alsobeen found. The salamander’s predominant mode oflocomotion is swimming with eel-like undulations ofthe body ending in a short, finned, laterally com-pressed tail (Fig. 1A). The very short limbs, with digitsreduced in number to three on the forelegs and two onthe hindlegs, are used for crawling on the water bot-tom and occasionally outside the water. Its muscularhead ends with a flattened, blunt snout.

The species is currently divided into two subspeciesbased on the extent of troglomorphism. Analyses ofmolecular data suggest, however, that P. anguinus maybe a complex of several species that independentlyevolved troglomorphic traits. Mitochondrial DNA datasuggest that P. anguinus is divided into six divergentlineages. These are about 5 to about 15 million yearsold, that is, they originated in the Pliocene or Miocene.Conversely, it has been hypothesized that troglo-morphism might have evolved in less than 500,000years (Trontelj et al., 2007).

Morphologically, the extremely rare subspeciesProteus anguinus parkelj, found only in the springs oftwo streams near Jelsevnik in Bela Krajina (southeast-ern Slovenia), is believed to resemble the supposedepigean ancestor of both forms. Despite having anentirely subterranean life, this salamander is darklypigmented (Fig. 1B). Its small but functional eyes arecovered with a transparent skin and have well-differ-entiated lens and retina. Conversely, the pineal gland,which in amphibians controls circadian rhythms, gam-ete development, and pigmentation changes, is greatlyreduced.

In contrast, the widespread, troglomorphic Proteusanguinus anguinus is characterized by a yellowish topinkish-white skin, with few scattered melanophores(pigment cells) invisible to the naked eye (Fig. 1A).Melanin synthesis can be light-induced, and after aprolonged exposure to light, the animals turn dark.The skin is thinner than in the pigmented form,and contains fewer multicellular glands. The head andsnout of P. a. anguinus are elongated and flattened, and

FIGURE 1 The olm (Proteus anguinus). (A) Described in 1768, thisblind salamander was the first scientifically documented cave-dwell-ing animal, but its existence had already been known long before. Itsearliest representation may be a Venetian stone carving from thetenth or eleventh century. (B) A rare, pigmented individual witheyes, from southeastern Slovenia. This unique population was dis-covered toward the end of the twentieth century. (C) Female protect-ing her clutch of eggs from predation by conspecifics. Photos courtesyof G. Aljancic, Tular Cave Laboratory. Used with permission.

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the cranial bones are longer and the teeth more numer-ous than in the pigmented form. Cervical vertebrae areoften elongated as well. Compared to the pigmentedform, P. a. anguinus has a shorter trunk, but a propor-tionately longer tail and extremities. Morphometricvariability among genetically and hydrologically iso-lated populations can be quite high.

The eyes of this salamander are greatly reduced insize and structure, and lie embedded deep in thehypodermal tissue. While vision is lost, the eye is stillcapable of detecting light. The pineal gland is alsogreatly reduced, but may still be capable of light detec-tion and hormonal activity. As is common in salaman-ders, the skin and midbrain are also photosensitive.Extraoptic sensory systems, including the lateral line,inner ear, ampullary electroreceptors, olfactory epithe-lium, and taste buds, are well developed and believedto play a crucial role in prey detection and communi-cation among individuals. Furthermore, behavioralexperiments suggest that the animals may use theEarth’s magnetic field to orient themselves.

Because of its very low metabolic rate and efficientfat storage, predominantly in the liver and tail,P. anguinus can survive prolonged periods of fooddeprivation. When food in the form of small subterra-nean crustaceans, mollusks, or surface insect larvaeis abundant, it becomes a voracious and efficientpredator.

P. anguinus is a social animal, recognizing and com-municating with conspecifics through scent. Bothmales and females use water-borne chemical signals tolocate each other, but in order to recognize sex andreproductive state, they need to come into direct con-tact. Outside of the breeding period, aggressive behav-ior is reduced and the animals aggregate at communalresting places under stones and in cracks. Long peri-ods of inactivity are punctuated by sessions of foragingor exploratory behavior. The animals show no appar-ent daily rhythm of activity and resting.

Little is known about timing of reproduction. Afemale is thought to reproduce only every 12 years onaverage. Up to 70 eggs are attached under rocks, andare guarded by the female until hatching (Fig. 1C).Larvae hatch after 4 to 6 months. The newly hatchedlarvae are 2.5 cm long and have incompletely formedlimbs, but well-differentiated eyes and scattered, visi-ble melanophores in the skin. During early larvaldevelopment, the eyes only slightly increase in sizewithout further differentiation, and then graduallysink into the surrounding tissue. After four months,major degenerative changes appear which cannot beprevented by illumination. Sexual maturity is reachedat a size of about 20 cm, which is attained after about15 years. P. anguinus is thought to have the longest lifespan of all amphibians, living for 70 years or more.

LUNGLESS SALAMANDERS(PLETHODONTIDAE)

Salamanders of the family Plethodontidae are widelydistributed in North and Central America, with popula-tions also in South America, southern Europe, and onthe Korean Peninsula. Lacking lungs, these salamandersbreathe primarily through their skin (cutaneous respira-tion). Pheromones play an important role in communica-tion, and the characteristic nasolabial grooves present inmetamorphosed adults allow fine-tuning in chemorecep-tion. A great diversity of lifestyles has evolved in thisgroup, from terrestrial, arboreal, to semi-aquatic andaquatic; life histories range from biphasic and larvalreproduction to direct development and possibly evenvivipary. It is no surprise to find in this family speciesassociated with caves. The family includes ninedescribed troglobitic species, all found in central andeastern North America. They are grouped in the generaEurycea, Haideotriton, and Gyrinophilus. Formerly usedgenera Typhlotriton and Typhlomolge have been synony-mized with Eurycea.

Brook Salamanders (Eurycea)

This is a diverse genus of 26 recognized species, fiveof which are troglobites. Except for Eurycea spelaea, thetroglobitic species inhabit subterranean waters of theEdwards Plateau and Balcones Escarpment in centralTexas, in the United States. Many species of Eurycea inthis region are spring-dwelling troglophiles, and addi-tional troglophilic Eurycea are encountered in cavesoutside the region. Paedomorphism is common in bothcave- and spring-dwelling salamanders. Eurycea spelaeais the only metamorphosing troglobitic member of thegenus.

Texas Cave and Spring-Dwelling Eurycea

All species of Eurycea from the Edwards Plateau inTexas share a common ancestor. It has been hypothe-sized that about 15 million years ago a split into twolineages occurred, corresponding to the geographicdivide imposed by the Colorado River. The resultinglineage south of the divide later gave rise to a group ofextremely troglomorphic cave-dwelling species collec-tively called Typhlomolge and its sister lineage com-prised of less troglomorphic cave- and spring-dwellingspecies called Blepsimolge. For the spring-dwellingspecies north of the Colorado River the nameSeptentriomolge has been coined. Each troglobitic spe-cies has a surface counterpart inhabiting the springoutflows of the same watershed or geological forma-tion. The complex interspecies relationships along with

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their geographic and ecological segregation indicatethat an ancient speciation event giving rise to the sub-terranean and largely epigean species was followed bya rapid adaptive radiation and more recent coloniza-tion of subterranean habitats by still more species.Evidence of intermittent gene flow between speciesthat diverged millions of years ago has been detected.Conversely, in some of the species with relativelybroad ranges, there is generally very little migrationbetween geographically distant populations, with “dis-tant” sometimes referring to as little as a few hundredmeters (Chippindale et al., 2009; Lucas et al., 2009).

Typhlomolge (Blind Salamanders)

All species are neotenic troglobites with very longand thin limbs, short trunk, broad and flattened snout,and a virtually pigmentless and translucent skin(Fig. 2A). They have a shimmering white appearancedue to the reflective connective tissue that lies

beneath the skin. The rudimentary eyes may be visi-ble as tiny dark spots under the skin, and possiblystill detect light. These salamanders are moderatelysmall with the total length of adults ranging from7�14 cm. Their diet consists of a variety of smallaquatic subterranean invertebrates, including crusta-ceans and snails. When feeding, the salamanders usu-ally probe the bottom using lateral movements oftheir spatulate head.

The Texas blind salamander (Eurycea rathbuni) hasbeen found in caves, wells, and pipes that intersect theSan Marcos Pool of the Edwards Aquifer, although itmay have a wider geographic range than previouslythought. Molecular analyses revealed high levels ofgenetic variation and the possibility that two distinctspecies occur within E. rathbuni. In springs immedi-ately above the subterranean waters occupied byE. rathbuni, E. nana (see below) is locally abundant.A captive breeding program has been established forboth species.

FIGURE 2 Brook salamanders (Eurycea). TroglobiticE. rathbuni (A) and (B), E. waterlooensis (C), andE. tridentifera (D) from the Edwards Plateau havedegenerate eyes and reduced pigmentation comparedto spring-dwelling populations of E. sosorum (E)and E. latitans (F). Adult (G) and larva (H) of Euryceaspelaea from the Ozark Plateau. This species is the onlytroglobitic brook salamander to readily undergo meta-morphosis in nature. Photos by D. Fenolio.

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Artificial induction of transformation in E. rathbuniresulted in only partial metamorphosis, with some tissues(e.g., skin) continuing to show only larval features. Thissalamander has an extremely depressed and broad ante-rior part of the head (Fig. 2B), with elongated anteriorcranial bones, and the longest limbs of all troglomorphicEurycea. The eyespots are barely visible. Juveniles havedarker pigmentation and proportionally larger eyes.

In contrast, the olfactory system is well developedand plays a very important role in the social behaviorof this salamander (Epp et al., 2010). Nothing is knownabout social interactions or breeding of this species innature; however, they have been observed in captivity.These salamanders rarely show aggressive or socialbehavior. The male of E. rathbuni lacks mental (chin)and caudal hedonic glands used during courtship inother Eurycea salamanders. Nevertheless, the specieshas an elaborate tail-straddling walk similar to thatwhich has been observed in other plethodontid sala-manders, albeit somewhat simplified. In captivity,these salamanders can live for over 10 years.

The Blanco blind salamander (Eurycea robusta) wasdescribed based on a single specimen collected from awell drilled in the bed of the Blanco River east of SanMarcos. More specimens had been collected at the time,but birds consumed two individuals while they were ina bucket and one preserved specimen has vanished.Molecular data are not available for this species, but thegeological formation in which it occurs is hydrologicallyisolated from that in which the geographically proximalE. rathbuni is found. The epigean salamander found inthe springs of the Blanco River drainage is E. pterophila(see below). Compared to E. rathbuni, the body ofE. robusta is stockier, with longer trunk, and shorter, rel-atively robust limbs. The head also is wider posteriorlyand more massive. The eyes are extremely reduced andinvisible through the skin.

The Austin blind salamander (Eurycea waterlooensis) isknown only from the outflows of Barton Springs inAustin, where individuals presumably are washed outfrom the Barton Springs segment of the EdwardsAquifer. This species is much more rarely encounteredthan the sympatric surface-dwelling E. sosorum (seebelow), both of which are included in a captive breedingprogram. This species is similar to E. rathbuni, but has awider head (Fig. 2C). The eyespots are visible and super-ficially resemble those of E. rathbuni. The limbs areshorter and the skin is slightly more pigmented than inE. rathbuni and E. robusta. The tail fin is weakly developed.

Blepsimolge (Sighted Salamanders)

A large majority of these salamanders are neotenicand completely aquatic. Besides those listed below, the

group includes several populations of yet undescribedspecies. The salamanders of this group are primarilysurface-dwelling, found in the immediate vicinity ofspring outflows, but they also inhabit caves, fissures,and sinkholes. Various species have independentlyevolved cave-associated morphological traits, whichhas become more apparent as new populations are dis-covered and genetically analyzed (Bendik et al., 2009).

These small salamanders (6�10 cm long) usuallyhave a dark, finely patterned dorsal coloration andtranslucent ventral parts (Figs. 2E,F). The intensity andpattern of dorsal coloration may vary due to an irregu-lar pattern of melanophores and reflective white irido-phores. Single or double dorsolateral rows of lightspots extend along the body. The species differ in eyesize, head shape, tail fin shape, and color pattern onthe tail and flanks. Certain cave-dwelling populationsexhibit marked reduction of eyes and pigmentation.The skin of the troglomorphic animals has a lightyellowish color, with diffuse gray or brown spots dor-sally and lighter spots laterally (Fig. 2D). Juveniles aredarker than adults. The snout is flattened but trun-cated. The eyes are regressed, sometimes lacking alens, but are usually still visible through the skin asdark spots; they are larger than the rudimentary eyesof E. rathbuni and other members of the Typhlomolgegroup. The trunk is short, containing fewer vertebrae,and the limbs are somewhat elongated.

The life history of most species is poorly known andbased predominantly on observations of E. nana andE. sosorum in captive breeding programs (e.g., Najvaret al., 2007). The spring-dwelling Eurycea are fairly sed-entary, although they may seasonally move betweensurface and cave habitats. On the surface, these secre-tive salamanders usually hide under rocks, in gravelsubstrate, or among aquatic plants. They can survivetemporary drying of ephemeral springs, presumablyby retreating to subsurface refugia. They are activethroughout the year and appear to reproduce duringall seasons. Up to 70 eggs are laid singly and do notreceive parental care. In captivity, the salamandersusually live for about 4 years, but an individual ofE. sosorum survived to at least 12 years.

Historically, many spring-dwelling populations fromthroughout the Edwards Plateau were assigned to theTexas salamander (Eurycea neotenes) based on morpho-logical similarity, but they were found to differ geneti-cally. This species is now restricted to the springs in thevicinity of Helotes, near San Antonio. A disjunct andgenetically divergent population inhabits the area ofComal Springs in New Braunfels.

One salamander that has been elevated to speciesfrom E. neotenes is the Barton Springs salamander(Eurycea sosorum), known from the Barton Springs pooland adjacent springs in Austin. This species is

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primarily surface-dwelling, but appears to reproducein subterranean conduits. Skin pigmentation inE. sosorum varies considerably, but all individuals havevery small eyes and somewhat elongated limbs. Theflattened, slightly elongated head ends with a trun-cated snout (Fig. 2E). The subterranean portion of theBarton Springs Aquifer is inhabited by the troglobiticE. waterlooensis (see above).

The San Marcos salamander (Eurycea nana) is abun-dant in the Spring Lake pool at the source of San MarcosRiver, the only site where it occurs. Metamorphosis hasbeen induced artificially in this species.

The Fern Bank salamander (Eurycea pterophila) inha-bits springs and caves of the Blanco and GuadalupeRiver drainages. Most populations are morphologicallysimilar to E. neotenes, to which they were formerlyassigned, but cave-dwelling individuals with reducedeyes and pigmentation have also been identified. Thisspecies is genetically different from E. neotenes, butsimilar to, perhaps even conspecific with, E. latitansand/or E. tridentifera (see below).

The Cascade Caverns salamander (Eurycea latitans)is possibly a complex of several species found in cavesand springs of the Cibolo Creek basin and south of theGuadalupe River in the southeastern part of theEdwards Plateau. For some time before initial molecu-lar analyses were completed, most populations wereregarded as E. neotenes, and the population at thetype locality (Cascade Caverns) was considered to behybrid between E. neotenes and E. tridentifera (seebelow). This population includes individuals with aspectrum of morphological features, ranging fromhighly troglomorphic, most similar to those ofE. tridentifera, to surface-like (Fig. 2F), most similar towhat was historically considered E. neotenes. Recentmolecular analyses suggest that at least part ofE. latitans, including the Cascade Caverns population,is conspecific with E. tridentifera. Furthermore, a fewcave populations were determined genetically to behybrids between E. latitans and E. neotenes, and in twocases individuals of both species were located withinthe same cave.

As currently recognized, the Comal blind salaman-der (Eurycea tridentifera) is a troglobitic species. It exhi-bits morphological modifications similar to the blindsalamanders of the Typhlomolge group, although gen-erally not to the same extreme extent (Fig. 2D). The sal-amander is found in caves of the Cibolo Creek basinand south of the Guadalupe River, in the southeasternpart of the Edwards Plateau. These populations mayactually be cave populations of E. latitans that havebecome troglomorphic. At the entrance to the typelocality (Honey Creek Cave), individuals intermediatein morphology between E. tridentifera and the surfacespecies have been found.

The Valdina Farms salamander (Eurycea troglodytes)is likely a complex of several species found in thesouthwestern part of the Edwards Plateau. Most popu-lations in this species complex are neotenic. However,natural metamorphosis has been observed in popula-tions from several springs and caves. Two groups ofpopulations within this complex are troglomorphic,with enlarged head, and reduced eyes and pigmenta-tion. The morphologically variable population fromthe type locality (Valdina Farms Sinkhole) was forsome time considered a hybrid between E. neotenesand E. tridentifera. This population is now extinct,but analyses of others have revealed that E. troglodytesis genetically distinct from both E. neotenes andE. tridentifera.

Septentriomolge (Northern Salamanders)

Most populations of these spring-dwelling speciesfrom north of the Colorado River were discovered after1995. The few known prior to 2000, when these specieswere formally described, had been considered periph-eral isolates of E. neotenes. Morphologically they resem-ble spring-dwelling species south of the Colorado River(Blepsimolge), described above. They can be seen year-round, most easily during the spring and summermonths, but small juveniles are rarely observed.

The San Gabriel Springs salamander (Eurycea naufra-gia) is known from springs and caves in the drainageof the San Gabriel River, in the vicinity of Georgetown.The adults have prominent eyes with melanophoresconcentrated around them. The range of the JollyvillePlateau salamander (Eurycea tonkawae) is limited toa few drainages on the Jollyville Plateau segmentof the Edwards Aquifer. This species makesextensive use of subterranean aquatic habitat, espe-cially when surface spring flow decreases. Adults havewell-developed eyes, broad jaws, and blunt snouts.The rare Chisholm Trail salamander (Eurycea chishol-mensis) is known only from springs at Salado.Compared to E. tonkawae and E. naufragia, the eyes ofthis salamander are reduced, and the head is flattenedand elongated.

Other Troglobitic and Troglophilic Eurycea

Several species of Eurycea with overlapping rangesoccur syntopically in caves and spring-fed headwaterswithin the Ozark and Appalachian Highlands and theInterior Lowlands of North America. These includeE. tynerensis, E. lucifuga, E. longicauda, and the troglobi-tic E. spelaea.

The grotto salamander (Eurycea spelaea) is restrictedto the Springfield and Salem Plateaus in the Ozark

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region of southern Missouri, extreme southeasternKansas, and adjacent areas in Arkansas and Oklahoma(U.S.A.). DNA sequence divergence within E. spelaea isrelatively large, and some of the populations may rep-resent distinct species. This is the only known troglobi-tic member of the genus that undergoes completemetamorphosis. Adults are known only from caves,but a large fraction of the larval population developsin surface springs and streams. Here they displace thelarvae of sympatric Eurycea species to more ephemeralparts of the stream and where predatory fishes andcrayfish are present. Both adults and larvae are sensi-tive to floods, which can extirpate a significant propor-tion of a population.

Adults grow to 7�14 cm in length and are white,pinkish white, or light brown in color (Fig. 2G). Theeyes are reduced in size and structure, visible as raiseddark spots through the fused eyelids. The larvae aretan dorsally, often spotted or mottled; those develop-ing inside caves can be pale to pink (Fig. 2H). Theyhave relatively small but functional eyes, which degen-erate in old larvae or during metamorphosis. Theextent of retinal degeneration in adults is related topostmetamorphic age but there is variability in eachage group. In its terminal stage, reduction encom-passes the entire area of the retina and vision is lost.Individuals raised in light maintain some pigmentationor become pigmented. The larvae may retain visionlonger than those kept in darkness and the eyelids inadults do not fuse.

Adults congregate in the main caverns where colonialbats roost, most likely for the purposes of feeding andbreeding. They are most active during spring and sum-mer, when moisture levels are high and food is abun-dant. They may be found climbing moist vertical rockwalls outside water, but commonly return to the waterto hunt aquatic invertebrates. Besides aquatic and terres-trial invertebrates they also feed on bat guano (Fenolioet al., 2006). In caves where colonial bats have declined,emaciated individuals have been observed. Mating inlate spring is followed by oviposition through summerand fall. Larvae metamorphose 2�3 years after hatching,at the size of 5�12 cm, and mature soon afterward.

The sister species of E. spelaea, the troglophilicOklahoma salamander (Eurycea tynerensis), is alsofound on the Ozark Plateau. The species comprisesboth strictly aquatic neotenic populations and moreterrestrial metamorphic populations. Neotenic animalsthat inhabit caves are often pale, whereas those on thesurface retain normal larval pigment patterns. Themetamorphs rarely venture far away from water.Usually they inhabit cool, moist habitats both on thesurface and in the twilight zone of caves. Larvae mayuse the karst cavities to move within or betweenstreams.

The troglophilic cave salamander (Eurycea lucifuga)occurs in the broad region between southern Indiana,northwestern Virginia, northern Alabama, and north-eastern Oklahoma (U.S.A.); this includes the karstareas of the Ozarks, Interior Low Plateau, and theAppalachians. The twilight zone of caves is the pre-ferred habitat of this species, although it can also befound deeper into caves and, despite its name, outsideof caves in forested limestone ravines, springs, andspring-fed streams. The species is broadly sympatricwith the long-tailed salamander (Eurycea longicauda),which is distributed throughout a similar area. Thisspecies is also frequently associated with caves andmines. These slender salamanders have very long tailsand grow to 18�19 cm. They are very conspicuous,colored yellow or orange, and covered withblack spots (Figs. 3A,B). E. lucifuga has long limbs anda prehensile tail used in climbing rock walls andledges. The eyes of this salamander are large and capa-ble of twilight vision. Adults can be found in cavesyear-round, but their numbers fluctuate seasonally.They aggregate there between spring and fall, whensurface temperatures are high. During this time thefemales deposit their eggs in subterranean waters.Larvae hatch after rains, when water flow increasesand more food becomes available (Ringia and Lips,2007).

Georgia Blind Salamander (Haideotritonwallacei)

The geographically isolated troglobitic Georgia blindsalamander (Haideotriton wallacei) has been found in afew caves pertaining to the Floridan Aquifer belowGeorgia, Florida, and Alabama (U.S.A.). At least twohistoric localities have been destroyed by human activi-ties, but cave divers have since spotted this species inthe corresponding portion of the aquifer. This species issometimes included in the genus Eurycea.

Adults of this neotenic salamander measure 5�8 cmin length and have little pigmentation, being mostlypink or whitish with scattered melanophores on theback and sides. The head is broad and the snout islong, but not flattened. The limbs are slender and theeyes are almost invisible, embedded in a mass of adi-pose tissue below the skin. Juveniles are slightly morepigmented and the eyespots are visible.

Haideotriton wallacei can be seen in cave pools andstreams especially in caves where bats defecate over ornear the water. Salamanders move about slowly, rest-ing on bottom sediments or climbing on submergedlimestone sidewalls and ledges. Deeper in subterraneantunnels the salamanders are much less common, pre-sumably because their food (benthic invertebrates) is

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scarce. Cave stream sediments have been found in thedigestive tracts of H. wallacei. One hypothesis attemptingto explain silt feeding holds that Haideotriton inten-tionally ingests the material to digest biofilm and micro-organisms in the sediments (the same has beenobserved in young Proteus anguinus). Another hypothe-sis posits that the silt represents failed feeding attempts.

Spring Salamanders (Gyrinophilus)

Four North American species are currently recog-nized. Three species are troglobites, found in caves ofsouthern and central Appalachian Highlands (U.S.A.).In Gyrinophilus, paedomorphosis is not universal andhas appeared after colonization of caves, although themetamorphosing nontroglobitic species already has anextremely long larval period.

The troglophilic spring salamander (Gyrinophilusporphyriticus) is common in and around small streams and

springs in eastern North America. Next to Eurycea lucifugathis is the most frequently encountered salamander incaves. Both larvae and adults can be found in cavesthroughout the Appalachian Highlands, even considerabledistances from the entrance. These large salamanders,which can grow over 20 cm in total length, are notoriousfor supplementing their invertebrate diet with conspecificsand other salamanders. Metamorphosed animals are usu-ally orangish-red to salmon and turn darker with age(Fig. 4B), but some individuals of cave populations arepale. The eyes of cave-dwelling individuals do not differfrom those from surface populations. A much higheroccurrence of ingested debris found in cave-dwellingindividuals compared to individuals from surfacestreams may indicate a lower feeding efficiency in thedark. Larvae, which are also often pale in color, cangrow up to 16 cm. They metamorphose after 3�5 yearsin surface populations but perhaps after 10 years ormore in cave populations.

FIGURE 3 A few salamanders frequently found incaves. In eastern North America, Eurycea lucifuga (A)and E. longicauda (B) frequently inhabit the same cave.(C) Plethodon petraeus is associated with karst andcaves on Pigeon Mountain in Georgia. (D) Pseudotritonruber also frequently uses caves for reproduction(Miller et al., 2008). (E) This undescribed species ofParamesotriton inhabits pools in the twilight zone ofcaves in China. Photos (A)�(C) by D. Fenolio; (D)�(E)by M. Niemiller.

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The three troglobitic species are believed to have arisenindependently from a single epigean ancestor similar toG. porphyriticus as early as 2.5 million (Pliocene) to asrecently as 60,000 years ago (Pleistocene), but precise phy-logenetic relationships are obscured due to recent specia-tion (Niemiller et al., 2008, 2009). Nonetheless, otherevidence supports their independent origins and DNAdata indicate that divergence has occurred in the presenceof continuous or periodic gene flow between subterra-nean populations and their surface-dwelling progenitor.

The Tennessee cave salamander (Gyrinophilus palleu-cus) is found in caves in the Central Basin, Highland Rim,and Cumberland Plateau of central Tennessee, northernAlabama, and extreme northwestern Georgia. Its range ison the periphery of that of G. porphyriticus. Two subspe-cies of G. palleucus are recognized: the pale salamander(Gyrinophilus palleucus palleucus; Fig. 4D), which inhabitscaves in the Lower Tennessee River watershed inAlabama and Tennessee, and the big mouth cave sala-mander (Gyrinophilus palleucus necturoides), found in the

Collins, Duck, Elk, and Stones River drainages inTennessee. This form is tan with dark spots dorsally andlaterally (Fig. 4E). The subspecies also differ slightly inhead width, leg length, eye size, and the number of trunkvertebrae. Except for the lost ability for eye accommoda-tion (focusing), vision is not greatly impaired in G. palleu-cus (Besharse and Brandon, 1973). Exposure to light hasno effect on eye development and does not induce anychange in skin pigmentation.

G. palleucus inhabits sinkhole-type caves that arerich in nutrients, which support its invertebrate preybase. Besides cave streams, where it is easily observed,the salamander is believed to inhabit subterraneanwaters inaccessible to humans. It has occasionally beenfound in springs outside caves. Little is known aboutthe life history of this species. Breeding is most likelyseasonal, occurring in late autumn or early winter.This salamander is typically paedomorphic, althoughmetamorphosed individuals have been encounteredin at least four caves. Metamorphosed individuals of

FIGURE 4 Spring salamanders (Gyrinophilus).Metamorphosed adults of G. palleucus (A) and left in (B)are pale and have smaller, degenerate eyes compared tothe troglophile G. porphyriticus (right in (B)). The larvaeof G. subterraneus (C), G. palleucus palleucus (D), G. palleu-cus necturoides (E), and G. gulolineatus (F) have small butfunctional eyes. In addition, the numerous neuromastmechanoreceptors on the head and flanks enable themto detect vibrations in the water. Photos (A)�(B) and(D)�(F) by M. Niemiller; photo (C) by D. Fenolio.

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G. palleucus differ from adult G. porphyriticus in theirpale skin, gaunt appearance, longer and narrowersnout and smaller eyes (Fig. 4A,B) and in retaining thelarval characteristic of an undivided premaxillary bone.

The Berry Cave salamander (Gyrinophilus gulolineatus)is known from caves in the Ridge and Valley of easternTennessee. Its range is entirely contained within the rangeof G. porphyriticus and the two species sometimes occur inthe same cave (Miller and Niemiller, 2008). Like G. palleu-cus, G. gulolineatus is usually paedomorphic and generallyresembles the former (Fig. 4F), but can be distinguishedfrom it by having a darker pigmentation, wider head,more spatulate snout, and by attaining a greater adultsize. The eyes are small and degenerate, comparable insize to the eyes of G. palleucus. Unlike G. palleucus, how-ever, transformed individuals have fully divided premax-illae, in which they resemble G. porphyriticus.

The West Virginia spring salamander (Gyrinophilussubterraneus) is known only from General DavisCave in West Virginia where it co-occurs withG. porphyriticus. Unlike G. palleucus and G. gulolineatus,G. subterraneus regularly metamorphoses, although atan exceedingly large size (up to 18 cm). Large larvaehave fully developed, mature gonads. Both larvae andadults have a light brownish-pink skin color, overlaiddorsally and laterally by a darker reticulate pattern(Fig. 4C). The head of larval G. subterraneus is broaderthan the heads of either G. porphyriticus or G. palleucus,but does not have the spatulate snout typical ofG. gulolineatus. Metamorphosed adults retain fusedpremaxillae (as in G. palleucus). Both larvae and adultshave smaller eyes than G. porphyriticus and, unlikeG. palleucus, only weak visual perception.

Although G. porphyriticus also occurs in GeneralDavis Cave, only adults of this species have been found(Niemiller et al., 2010). G. subterraneus has been observedas far as 2 km into the cave; however, in the first 300 mof the stream passage, predominantly larvae have beenencountered, suggesting that its main habitat may belocated deeper into the cave. The larvae prefer shallow,calm pools and are found in water depths of 1�20 cm.Adults can be found in shallow water as well, whereasG. porphyriticus almost never enters the water. Thebanks of the cave stream contain thick deposits ofdecaying leaf litter, washed into the cave by floods. Thisleaf litter is the source of nutrients for cave invertebratesthat adults of both species putatively prey on.

DIVERSITY PATTERNS OFSALAMANDERS FOUND IN CAVES

Including the salamanders described above, over 90species (approximately 15% of all known salamanderspecies) belonging to five families have been reported

from natural or manmade subterranean environments.Their dependence on the cave environment varies notonly between species, but also among populations ofthe same species.

Over half of all species found in caves are reportedfrom eastern North America. Several woodland sala-manders (Plethodon sp.), especially Plethodon albagula,P. glutinosus, P. dorsalis, and P. petraeus (Fig. 3C) are fre-quently associated with caves. Also reliant on caves arethe red salamander (Pseudotriton ruber; Fig. 3D), a fewdusky salamander species (Desmognathus sp.), and thegreen salamander (Aneides aeneus). To the south, inthe Mexican Sierra del Madre Oriental and Sierra Madredel Sur, two splayfoot salamanders (Chiropterotriton sp.)and two false brook salamanders (Pseudoeurycea sp.)occur in caves. Of the salamanders that occur in westernNorth America, the web-toed salamanders (Hydromantessp.) in California, especially the shasta salamander(Hydromantes shastae), are often found in caves.Apart from the plethodontids, the mole salamanders(Ambystoma sp.) of the family Ambystomatidae are reg-ularly encountered in caves, particularly in the regionfrom Arizona to Alabama and Tennessee. Neoteniccave-dwelling populations of the barred tiger salaman-der (Ambystoma mavortium) have been reported fromNew Mexico and in gypsum caves of northeasternOklahoma.

Europe’s salamander fauna is dominated by thefamily Salamandridae, but seven species of the pletho-dontids also occur here. The European cave salaman-ders (Speleomantes sp. and Atylodes sp.) of Sardinia,northwestern mainland Italy, and southern France areclosely related to the Californian Hydromantes andshare many life history features with them. They arestrongly associated with caves, and will aggregate inthe twilight zone. Although they have prominent eyes,they can also detect prey in darkness using olfactoryinformation. Several surface species of the familySalamandridae frequent natural or manmade subterra-nean refugia in Europe, especially in the arid circum-Mediterranean region. The widespread fire salamander(Salamandra salamandra) not only seeks refuge in cavesbut also frequently favors them as reproduction siteseven when surface water is available nearby. ThePyrenean mountain newt (Calotriton asper) inhabitsstreams, lakes, and ponds along the Pyrenees Mountainsof France and Spain, but is also found in subterraneanwaters, especially on the periphery of its range. Exceptfor one pale-colored cave population, no morphologicalmodifications have been described in this species.Instead, modifications related to cave life involve thereproductive cycle and its periodicity, including pro-longed or continuous gamete production, slower eggdeposition, and delayed metamorphosis. Neotenic indi-viduals have also been found.

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Despite extensive karst areas in Central Americaand Asia, and great salamander diversity (especially inCentral America), the number of salamanders thatinhabit caves and other subterranean habitats is low.The caves on the Yucatan Peninsula in Mexico andadjacent Guatemala are the temporal habitat of theplethodontid Yucatan salamander (Bolitoglossa yucata-na), (perhaps) the nimble long-limbed salamander(Nyctanolis penix), and potentially two more species.In western Asia, only one species, of the familyHynobiidae, has been found in a cave. The almost fullyaquatic Gorgan mountain salamander (Paradactylodongorganensis) is known from two localities in the AlborzMountains of northern Iran, one of which is a cave. Ineastern Asia, another hynobiid species, the oki salaman-der (Hynobius okiensis) from the Dogo Island of Japan, isbelieved to reproduce in hypogean waters. The salaman-drid wart newts (Paramesotriton sp.) have been observedin the twilight zone of caves in Guizhou Province, China.

CONCLUSION

Very few salamanders are obligate cave-dwellers,which is in contrast to the great number of species thattemporarily inhabit caves. Ranges of troglobitic salaman-ders are usually small, limited by hydrological or geo-logical barriers. Due to the limitations such asinaccessibility or rarity, only the more common specieshave been studied in detail. A fair amount of attentionhas been given to their phylogenetic relationships, obser-vations on regressive morphological modifications asso-ciated with cave life, development, and behavior, butlimited knowledge exists of their life histories and ecol-ogy. Continuing research in these areas is essential forgaining insight into the origins and processes involvedin evolution of obligate subterranean existence.

Because of suspected small population sizes, limiteddistribution, and high specialization, troglobitic sala-manders are threatened by habitat and water qualitydegradation, caused mainly by urbanization, agricul-ture, and deforestation. Their position in the food weband the tendency to accumulate energy reserves intheir bodies make them particularly vulnerable tothe effects of toxic chemicals in contaminated water.Most troglobitic salamanders are legally protected.However, in the face of increasing demands forgroundwater, pollution, and alterations to the land-scape above cave systems, their numbers continue todecline. Not only troglobitic species but also all sala-manders that use caves during part of their life history,are important components of subterranean ecosystemsand greatly depend on the preservation of thesespecial habitats.

Bibliography

AmphibiaWeb: Information on amphibian biology and conservation(2011). Berkeley, CA: AmphibiaWeb. Available: ,http://amphi-biaweb.org>.

Bendik, N. F., Gluesenkamp, A. G., & Chippindale, P. T. (2009). Thebiogeography and rapid radiation of central Texas neotenic sala-manders. Proceedings of the 15th International Congress of Speleology,1, 219�225.

Besharse, J. C., & Brandon, R. A. (1973). Optomotor response and eyestructure of the troglobitic salamander Gyrinophilus palleucus.American Midland Naturalist, 89, 463�467.

Chippindale, P. T., Gluesenkamp, A. G., & Bendik, N. F. (2009).Texas cave and spring salamanders (Eurycea): New discoveriesand new surprises. Proceedings of the 15th International Congress ofSpeleology, 1, 227.

Epp, K. J., Gonzales, R., Jr., & Gabor, C. R. (2010). The role of water-borne chemical cues in mediating social interactions of the Texasblind salamander, Eurycea rathbuni. Amphibia-Reptilia, 31(2),294�298.

Fenolio, D. B., Graening, G. O., & Stout, J. F. (2006). Coprophagy in acave-adapted salamander; the importance of bat guano examinedthrough stable isotope and nutritional analyses. Proceedings of theRoyal Society B, 273(1585), 439�443.

Grossenbacher, K., & Thiesmeier, B. (Eds.), (1999). Handbuch derReptilien und Amphibien Europas. Band 4/I: Schwanzlurche (Urodela)I. Wiesbaden: AULA (in German).

Lannoo, M. (Ed.), (2005). Amphibian declines: The conservation status ofUnited States species. Berkeley: University of California Press.

Lucas, L. K., Gompert, Z., Ott, J. R., & Nice, C. C. (2009). Geographicand genetic isolation in spring-associated Eurycea salamandersendemic to the Edwards Plateau region of Texas. ConservationGenetics, 10, 1309�1319.

Miller, B. T., & Niemiller, M. L. (2008). Distribution and relativeabundance of Tennessee cave salamanders (Gyrinophilus palleucusand G. gulolineatus) with an emphasis on Tennessee populations.Herpetology Conservation and Biology, 3(1), 1�20.

Miller, B. T., Niemiller, M. L., & Reynolds, R. G. (2008). Observationson egg-laying behavior and interactions among attending femalered salamanders (Pseudotriton ruber) with comments on the use ofcaves by this species. Herpetological Conservation and Biology, 3(2),203�210.

Najvar, P. A., Fries, J. N., & Baccus, J. T. (2007). Fecundity of SanMarcos salamanders in captivity. Southwestern Naturalist, 52(1),145�147.

Niemiller, M. L., Fitzpatrick, B. M., & Miller, B. T. (2008). Recentdivergence-with-gene-flow in Tennessee cave salamanders(Plethodontidae: Gyrinophilus) inferred from gene genealogies.Molecular Ecology, 17(9), 2258�2275.

Niemiller, M. L., Miller, B. T., & Fitzpatrick, B. M. (2009). Systematicsand evolutionary history of subterranean Gyrinophilus salaman-ders. Proceedings of the 15th International Congress of Speleology, 1,242�248.

Niemiller, M. L., Osbourn, M. S., Fenolio, D. B., Pauley, T. K.,Miller, B. T., & Holsinger, J. R. (2010). Conservation status andhabitat use of the West Virginia spring salamander (Gyrinophilussubterraneus) and spring salamander (G. porphyriticus) in GeneralDavis Cave, Greenbrier Co., West Virginia. HerpetologicalConservation and Biology, 5(1), 32�43.

Ringia, A. M., & Lips, K. R. (2007). Oviposition, early developmentand growth of the cave salamander, Eurycea lucifuga: Surface andsubterranean influences on a troglophilic species. Herpetologica, 63(3), 258�268.

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Pedomorphosis revisited: Thyroid hormone receptors are functionalin Necturus maculosus. Evolution and Development, 8(3), 284�292.

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SALTPETRE MININGDavid A. Hubbard Jr.

Virginia Speleological Survey and Virginia Department ofMines, Minerals and Energy

DEFINITIONS AND IMPORTANCE

Historically, saltpetre is one of the most strategic of com-modities. It occurs naturally in caves and rockshelters,but it is rare. A suite of related nitrates occurs in manycaves. The mining and processing of cave nitrate-enriched sediments is a relatively simple endeavor,although labor intensive. The tendency of these sedi-ments to contain a suite of nitrates rather than just potas-sium nitrate is one reason the archaic spelling saltpetre isused in reference to the mining of cave nitrates and thecaves in which they occur. This convention is followedthroughout this article.

The invention of gunpowder revolutionized weap-onry and warfare. Gunpowder, also referred to as blackpowder, consisted of a mixture of saltpetre, sulfur, andcharcoal. Although saltpetre was used in the preserva-tion of meats, the greatest historic demand for saltpetrewas during times of insurrection and war. Nowherehas the quest for saltpetre contributed to historic eventsmore than in the United States, where this commoditycontributed to both the formation of a country andalmost its destruction.

The mineral niter (synonym, saltpeter) is potassiumnitrate (KNO3). Like many other nitrate compounds,niter is deliquescent; that is, it has a natural tendencyto draw water to itself and dissolve into a solution.Although deliquescent minerals can absorb moisturefrom humid air, they occur naturally in sheltered loca-tions under conditions of low humidity or during peri-ods of reduced humidity. The deliquescent nature ofsaltpeter is the reason for the old warning of soldiersand frontiersmen, who depended on their firearms forsurvival, to “keep your powder dry!”

Caves and rockshelters, also termed rockcastles, arelocations where nitrates may accumulate. Analyses ofcave sediments, which were mined historically for salt-petre, commonly reveal no nitrate minerals. The reasonis that most of the classical saltpetre caves are in regionswhere the humidity typically is too high for niter andthe even more deliquescent minerals nitromagnesite,

Mg(NO3)2 � 6H2O, and nitrocalcite, Ca(NO3)2 � 4H2O, tocrystallize into their solid mineral forms. Instead, thesaltpetre-rich sediments, historically termed petre dirt,contain concentrated viscose nitrate solutions in theform of sediment moisture.

Because nitrate minerals rarely crystallize in most ofthe known saltpetre caves, other clues to the accumula-tion of nitrates in cave sediments are important. In theabsence of niter, the foremost evidence of significantnitrate concentrations in cave sediment is the presenceof efflorescent crusts. These white or light-colored pow-dery crusts commonly are composed of a mixture ofsoluble salts and minerals, such as gypsum and calcite,that accumulate on cave sediment and rock surfaces asa result of evaporation. Efflorescent incrustations sig-nify locations where periodic atmospheric conditionsallow evaporation and the concentration of the minuteamounts of dissolved solids in interstitial soil and rockmoisture. Precipitation and concentration drive thewicking action of the dissolved solids through soil androck pores from their respective remote sources. Thesources of most saltpetre cave nitrates are the surfaceecosystems overlying saltpetre caves.

Recent microbiological work in caves and karst hasshown that bacteria are important in cave development(speleogenesis) and in the development of the secondarycave mineral forms (speleothems) that were thought tobe the result of physiochemical reactions (Taylor,1999). The importance of nitrifying and other bacteriain the accumulation of efflorescent crusts and nitrateaccumulations in sediments (petre dirt) is unknownbut probably is not trivial.

SALTPETRE MINING

The mineral niter (KNO3) is rarely found in caves,but when observed it occurs as clear to white lint-likefibers, acicular (needle-like) crystals, powder, crusts,coralloid, or flowstone forms. The most extensive formobserved in saltpetre caves is the lint-like fibers thatoccur in dense carpets on bedrock walls (Fig. 1) andsediment-covered walls and floors. These niter fiberoccurrences can be harvested with the use of a thinwooden spatula or paddle-like scraper, leaving little orno evidence of extraction. Such a wooden scraperwas observed high on a Virginia saltpetre cave ledgebefore this author had observed an efflorescent niteroccurrence.

The majority of the documented saltpetre cavesdoes not normally contain crystalline niter. At thehumidities typically found in these caves, the deliques-cent nitrate accumulations occur as viscose nitratesolutions in efflorescent crusts on rock and sediment

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Encyclopedia of Caves. © 2012 Elsevier Inc. All rights reserved.