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Functional Morphology and Evolution of Tail Autotomy in Salamanders

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Functional Morphology and Evolution of Tail Autotomy in Salamanders Functional Morphology and Evolution of Tail Autotomy in Salamanders DAVID B. WAKE AND IAN G. DRESNER Department of Anatomy, The University of Chicago, Chicago, lllinois ABSTRACT Basal tail constriction occurs in about two-thirds of the species of plethodontid salamanders. The constriction, which marks the site of tail autotomy, is a result of a reduction in length and diameter of the first caudal segment. Gross and microscopic anatomical studies reveal that many structural specializations are associated with basal constriction, and these are considered in detail. Areas of weak- ness in the skin at the posterior end of the first caudal segment, at the attachment of the musculature to the intermyotomal septum at the anterior end of the same segment, and between the last caudosacral and first caudal vertebrae precisely define the route of tail breakage. During autotomy the entire tail is shed, and a cylinder of skin one segment long closes over the wound at the end of the body. It is suggested that specializations described in this paper have evolved jndepend- ently in three different groups of salamanders. Experiments and field observations reveal that, contrary to expectations, frequency of tail breakage is less in species with apparent provisions for tail autotomy than in less specialized species. The tail is a very important, highly functional organ in salamanders and it is suggested that selection has been for behavioral and structural adaptations for control of tail loss, rather than for tail loss per se. Tail loss and subsequent regeneration is sent facts concerning anatomical details a well documented phenomenon among of the basal tail region, a functional inter- the lower vertebrates. Although much is pretation of the morphology of the region, known concerning regeneration, the litera- and a hypothesis concerning the evolution ture on tail breakage is scattered and of the observed morphological specializa- scanty. This is particularly true of sala- tions. manders, a group that contains a number of species reputed to practice tail autot- MATERIALS AND METHODS omy. The present study was undertaken Cleared and stained as well as skeleton- in an attempt to determine those anatom- ized specimens of adults of all genera and ical features that permit and facilitate tail most species of plethodontid salamanders breakage in salamanders. In addition, we have been available for the study (see wished to investigate morphological spe- Wake, '66, for complete list). In addition, cializations in those species reported to large numbers of x-rays have been exam- practice tail autotomy, and to attempt an ined to obtain osteological information. analysis of the evolution of such specializa- Histological investigations were made on tions. Our working hypothesis has been adults of the following species of the fam- that species which demonstrate specialized ily Plethodontidae : Desmognathus fuscus, behavioral patterns resulting in tail loss D. quadramaculatus, D. ochrophaeus, likely have evolved physiological and ana- Pseudotriton ruber, Gyrinophilus porphy- tomical specializations which facilitate the riticus, Eurycea bislineata, Hemidactylium phenomenon. These morphological fea- scutatum, Plethodon cinereus, P. jordani, tures might, in turn, provide insight into Aneides lugubris, Ensatina eschscholtzii, the processes leading to structural and Hydromantes brunus, Batrachoseps attenu- functional specialization. atus, B. pacificus, Bolitoglossa subpalmata, Our study has revealed that basal tail B. morio, B. rufescens, Chiropterotriton constriction in salamanders is an indica- chiropterus, C. abscondens, C. multidenta- tion of a series of interrelated morpholog- tus, Pseudoeunjcea leprosa, Oedipina uni- ical specializations. In this paper we pre- formis, Lineatriton lineola, and Thorius J. MORPII., 122: 265-306. 265 266 DAVID B. WAKE AND IAN G. DRESNER dubitus. Emphasis was placed on three all of the tail is lost. Many authors have genera, Hemidactylium, Ensatina, and reported tail autotomy in salamanders, liz- Bolitoglossa. ards, snakes, and mammals. The phenom- Material utilized in the study was fixed enon is most prevalent and most thor- in neutral buffered formalin, Bouin's or oughly understood in lizards (Quattrini, Zenker's fluid, decalcified in dilute HC1 or '52a,b, '54; Etheridge, '67) where breakage buffered EDTA, embedded in paraffin or is intravertebral. The breakage plane fol- parlodion, and sectioned serially in frontal, lows an unossified area that extends trans- sagittal, or transverse planes at 5 to 10 P. versely through from one to many Stains were chosen to best demonstrate vertebrae, along the caudal side of the connective tissue relationships. These in- associated intermyotomal septum and cluded routine Ehrlich's hematoxylin and through the skin. An unsegmented cartila- eosin, orcein (Mallory, '38), aldehyde fuch- ginous rod and rather atypical musculature sin (Gomori, '50), Heidenhain's azan (Lil- and skin is regenerated (Moffat and Bel- lie, '54), Van Gieson's connective tissue lairs, '64). Breakage is between vertebrae stain (Lillie, '54), and Bodian's Protargol in the other groups, but only in salaman- method of silver staining (Bodian, '36). ders is there any apparent morphological Living examples of many species of sal- specialization and only salamanders regen- amanders have been studied in the field erate a virtually normal tail. and laboratory, including Hemidactylium Salamanders may be placed in three scutatum, Ensatina eschscholtzii, Bolito- very general groups based on the structure glossa subpalmata, B. yucatana, Pseudo- of the tail and the pattern of tail breakage eurycea leprosa, Chiropterotriton multiden- (Wake, '66). These groups are not phy- tatus, C. chiropterus, Thorius dubitus, Ietic, but rather represent grades of mor- Batrachoseps attentuatus, B. pacificus, and phological and functional specialization. Plethodon cinereus. Large numbers of pre- Because this classification is convenient served animals have been studied in the and facilitates communication we have Field Museum of Natural History and the adopted it in the present report. University of Michigan Museum of No obvious specializations are associ- Zoology. ated with the breakage of tails in the more The classification scheme adopted here primitive families of salamanders. Break- for the salamander family Plethodontidae age is the result of traumatic events, such is that proposed by Wake ('66). Because as attacks by predators, rock falls, entrap- this classification is as yet relatively un- ment, and similar accidents. These ani- familiar, it is briefly summarized below mals usually have tails that are not sharply (genera in parentheses) : differentiated from the body and hence are Subfamily Desmognathinae (Desmognathus, of large diameter basally. Breakage is usu- Leurognathus, Phaeognathus). ally limited to posterior parts of the tail. Subfamily Plethodontinae Tribe Hemidactyliini ( Gyrinophilus, Pseudo- These animals are said to have thich-based triton, Stereochilus, Typhlotriton, Eurycea, tails in this study. Species characteristic Typhlomolge, Haideotriton, of this group included in our study are Hemidactylium). Pseudotriton Tuber, Desmognathus fuscus, Tribe Plethodontini (Plethodon, Aneides, Ensatina). and Eurycea bislineata. Tribe Bolitoglossini Some members of the family Salaman- Supergenus Hydromantes (Hydromantes). dridae (e.g. Chwglossa lusitanica) and Supergenus Batrachoseps (Batrachoseps). many members of the family Plethodon- Supergenus Bolitoglossa (Bolitoglossa, Oedipina, Pseudoeulycea, Chiropterotriton, tidae (e.g. Batrachoseps pacificus, Pletho- Lineatriton, Parvimolge, Thorius). don cinereus) have what we call slender- based tails. In these species breakage may Patterns of tail morphology occur at any point in the tail, but the route The term tail autotomy has been used of breakage is specialized in that the skin freely in the literature and it is impossible break occurs one segment posterior to the to determine exactly what various authors muscle break. The result is that, following mean by it. Nevertheless, the end result of breakage, the skin covers the open wound tail autotomy is always the same - part or and facilitates healing. This pattern, first TAIL AUTOTOMY IN SALAMANDERS 267 mentioned by Piersol ('lo), is called the sines) species. The amount of constriction wound-healing specialization by us. and details of structure differ considerably A final group that includes almost two- among the species. Constriction is pro- thirds of the species of the family Pletho- nounced in most, but is barely evident in dontidae has constricted-based tails. A dis- Oedipina, Lineatriton, and some species of tinct tail constriction is found at the base other genera. A universal feature of the of the tail and breakage, when it occurs, group is the presence of a first caudal seg- is ordinarily at this point. Members of the ment that is short relative to the segments group have been reported to practice tail that immediately precede and follow it. autotomy by many authors. We have stud- This segment is immediately posterior to ied this group more intensively than the the cloaca1 slit and is the first to entirely others, especially the following species : surround the vertebral column. Shortening Hemidactylium scutatum, Ensatina esch- of the segment is most pronounced in those scholtzii, and Bolitoglossa subpalmata. species with obvious basal constriction, With the exception of some brief and gen- such as members of the genus Bolitoglossa.
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