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Appendicular Skeletal Morphology in Minute Salamanders

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Appendicular Skeletal Morphology in Minute Salamanders JOURNAL OF MORPHOLOGY 17457-77 (1982) Append icuI ar Skeletal Mor pho I og y in Mi nut e Salamanders, Genus Thorius (Amphibia: Plethodontidae): Growth Regulation, Adult Size Determination, and Natural Variation JAMES HANKEN Museum of Vertebrate Zoology and Department of Zoology, University of California. Berkeley, California 94720 ABSTRACT Patterns of growth and variation of the appendicular skeleton were examined in Thorius, a speciose genus of minute terrestrial plethodontid sal- amanders from southern Mexico. Observations were based primarily on ontoge- netic series of each of five species that collectively span the range of adult body size in the genus; samples of adults of each of seven additional species provided supplemental estimates of the full range of variation of limb skeletal morphology. Limbs are generally reduced, i.e., pedomorphic, in both overall size and develop- ment, and they are characterized by a pattern of extreme variation in the composi- tion of the limb skeleton, especially mesopodial elements, both within and between species. Fifteen different combinations of fused carpal or tarsal elements are vari- ably present in the genus, producing at least 18 different overall carpal or tarsal ar- rangements, many of which occur in no other plethodontid genus. As many as four carpal or tarsal arrangements were observed in single population samples of each of several species; five tarsal arrangements were observed in one population of T. minutissimus. Left-right asymmetry of mesopodial arrangement in a given speci- men is also common. In contrast, several unique, nonpedomorphic features of the limb skeleton, in- cluding ossification of the typically cartilaginous adult mesopodial elements and ontogenetic increase in the degree of ossification of long bones, are characteristic of all species and distinguish Thorius from most related genera. They form part of a mechanism of determinate skeletal growth that restricts skeletal growth after sexual maturity. Interspecific differences in the timing of the processes of appen- dicular skeletal maturation relative to body size are well correlated with interspe- cific differences in mean adult size and size at sexual maturity, suggesting that shifts in the timing of skeletal maturation provide a mechanism of achieving adult size differentiation among species. Processes of skeletal maturation that confer determinate skeletal growth in Thorius are analogous to those typical of most amniotes - both groups exhibit on- togenetic reduction and eventual disappearance of the complex of stratified layers of proliferating and maturing cartilage in long bone epiphyses - but, unlike most amniotes, Thorius lacks secondary ossification centers. Thus, the presence of sec- ondary ossification centers cannot be used as a criterion for establishing determi- nate skeletal growth in all vertebrates. Phyletic size change is a conspicuous feature opment of the skeleton - particularly the ap- of evolution, and the phenomenon of size in- pendicular skeleton - have figured prominently crease or decrease is well documented for many in attempts to explain growth regulation over- taxa (Stanley, '80). Less is known of the physi- all. Early development of the appendicular ological mechanisms of growth regulation by skeleton is remarkably similar in all Recent which size are achieved' In tetra- Dr. Hanken's current address is Department of Biology, Dalhousie pod vertebrates, patterns of growth and devel- University, HaMax B3H 4Jl.Nova Scotia, Canada 0362-2525/82/1741-0057$06.000 1982 ALAN B. LISS, INC. 58 J. HANKEN tetrapods; many differences among groups be- brates, the variation and distribution of these come apparent only at later stages (Hinchliffe mechanisms among different taxa, and the and Johnson, ’80). A typical long bone initially consequences of size change in particular forms as a mesodermal condensation that sub- groups. sequently differentiates into a cartilaginous The genus Thorius (Amphibia: Plethodonti- model, or precursor, of the later bony element. dae) comprises a complex of at least 15 species All tetrapods, as well as bony fishes, develop a of terrestrial lungless salamanders that live in single ossification center, or diaphysis, in the the montane forests of southern Mexico. Rep- midsection (shaft)of each long bone between resenting a specialized component of the ex- the two cartilaginous ends, or epiphyses tensive radiation of plethodontid salamanders (Haines, ’42). This single, or primary, ossifica- in the New World tropics, Thorius is highly de- tion center is typical of amphibians, turtles, rived in many respects, particularly in mor- and crocodilians, whereas mammals, birds, and phology, compared to related genera (Wake, the remaining Recent, limbed reptiles - liz- ’66). The most conspicuous attribute of Thor- ards and Sphenodon (thetuatara) - frequently ius is small size - as adults, body size ranges form additional, secondary ossification centers from as little as 14 mm SVL (snout to posterior in the cartilaginous epiphyses after the appear- end of vent)in the smallest species, tojust over ance of the primary center. During ontogeny in 30 mm SVL in the largest species. Associated these latter groups, primary and secondary os- with reduced size are several extreme modifica- sification centers increase in size relative to the tions of the appendicular skeleton. The limbs overall length of the bone and gradually erode are relatively small and the digits (especially the intervening cartilaginous plates that sepa- the terminal phalanges) are poorly developed; rate them. Because this cartilage is the only in these aspects, skeletal development is trun- tissue capable of longitudinal expansion (via cated precociously relative to that of more gen- cell proliferation and interstitial growth), lon- eralized plethodontid salamanders, conform- gitudinal bone growth is no longer possible ing to an overall pattern of pedomorphosis when primary and secondary centers meet and exhibited by much of the skeleton, including fuse. Consequently, secondary ossification the skull. In contrast, the appendicular skele- centers are often presumed to be related inti- ton possesses several novel features whose mately to a mechanism of growth regulation presence cannot be attributed simply to trun- that confers a pattern of “determinate”growth cated development. Mesopodial elements, to those amniotes that possess them (Haines, which typically are cartilaginous throughout ’38, ’41, ’42, ’69; Romer, ’56, ’70).Tetrapods that life in plethodontid salamanders, are ossified in lack secondary centers are considered to have adult Thorius. Furthermore, long bones, which “indeterminate” growth (Goin and Goin, ’71; retain relatively large and well-developedcarti- Goss, ‘74, ’80; Romer, ’66). laginous epiphyses in adults of most other The dichotomy between determinate and in- plethodontid genera, show increased ossifica- determinate growth is well entrenched in the tion in Thorius. Yet despite the identification literature on skeletal development and has of these “derived features of the appendicular played a central role in arguments concerning skeleton more than a century ago (Cope, 1869a), the origin of particular vertebrate groups, such their role in limb function and skeletal matura- as lizards (Carroll, ’77).In many instances, the tion has remained unclear. In this paper, I pre- presence or absence of secondary ossification sent the results of an examination of skeletal centers is used as a sufficient criterion for iden- growth and variation in Thorius that was con- tifying which mode of growth prevails in a par- ducted as part of a larger study of the mecha- ticular taxon (for example, see Andrew and nisms and morphological consequences of ex- Hickman, ’74). Yet thorough studies of pat- treme size reduction in salamanders (Hanken, terns of skeletal growth on which the dichot- ’80). This allows consideration of both the omy is based include surprisingly few taxa; mechanism by which size reduction was furthermore, empirical data gathered from lon- achieved during the evolution of Thorius from gitudinal studies of growth of many natural larger ancestors and the means by which size populations of fish and amphibians suggest differentiation is effected among species with- that growth patterns in these groups may be in the genus. quite “determinate,” regardless of the absence Analysis of size and skeletal growth regula- of secondary ossification centers. Thus, much tion was based primarily on observations of remains to be learned concerning the mecha- five species that collectively span the range of nisms of growth and size regulation in verte- adult body size found in Thorius. Supplemen- SKELETAL GROWTH AND VARIATION IN SALAMANDERS 59 tary observations of seven additional species Abbreviations provided estimates of the range of skeletal var- b, compact bone fibula iation in the genus. I focused particularly on C, centrale in termedium the appendicular skeleton for two reasons: 1) cl, centrale 1 hypertrophied cartilage d, diaphysis marrow cavity the presence of several unique, or derived, fea- dl-2, distal carpal 1-2 mature cartilage tures not seen in larger plethodontid salaman- d3, distal carpal 3 carpus metatarsal 3 ders, with the presumption that the occurrence d4, distal carpal 4 proliferating cartilage of these features is related to the process of dl-2, distal tarsal 1-2 radiale d3. distal tarsal 3 tarsus resting cartilage size and growth regulation; and 2) the promi- d4-5, distal tarsal 4-5 tibiale
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