Comparative morphology of tube feet among the asteroidea: Phylogenetic implications

American Zoologist, Jun 2000 by Vickery, Minako S, McClintock, James B

SYNOPSIS. Tube-foot morphology has been included among a variety of taxonomic criteria for the Asteroidea over the past twenty-five years. Other than a few families belonging to the order Paxillosida, which are thought to have pointed, non-- suckered tube feet that are used for digging and burial in soft sediments, the presumption has been that asteroids have flat-tipped, suckered tube feet. This has become an accepted model despite the fact that the comparative morphology of asteroid tube feet has not been considered. In the present study we examine tube-- foot morphology of 45 species of Asteroidea representing 19 families. Our analysis confirms that members of the Luidiidae and Astropectinidae (order Paxillosida) lack suckers on the tips of their pointed tube feet. We demonstrate that there is considerable variation in tube-foot morphology among members of the Asteroidea including an entirely new type of flat-tipped, non-suckered tube foot in species belonging to the order Valvatida. The external morphology of tube feet in species belonging to the order Velatida could not be distinguished from "typical" flat-- tipped, suckered tube feet; nonetheless, histological sections revealed a distinctive internal morphology. Finally, we report the first observations of the tube-foot morphology of representatives of deep-sea asteroids belonging to the orders Notomy-- otida and Brisingida, a group that also lacks the typical flat-tipped, suckered tube-- foot morphology. The results of our study demonstrate that the current tube-foot morphology model needs to be reconsidered, as there is considerably greater variation than was previously believed to be the case. Moreover, we conclude that while tube-foot morphologies show consistent similarities within orders, tube-foot morphology is less appropriate as a taxonomic character below this level.

INTRODUCTION

Extant asteroids currently number approximately 1,600 species, occurring from the intertidal to the abyssal and from tropical to polar seas (Blake, 1989). Classifications of asteroids have been based primarily upon skeletal morphologies of adults (Spencer and Wright, 1966; Downey, 1973; Hayashi, 1973; Blake, 1987; Gale, 1987; Clark and Downey, 1992). Morphological differences or similarities of adult skeletons have been used to group asteroids into species, genera, families, and orders. Nonetheless, asteroid classifications have not gone without considerable debate among taxonomists. Species belonging to the families Astropectinidae and Luidiidae are a classic example of such a debate.

Both families were initially separated into two entirely different orders (Spencer and Wright, 1966; Downey, 1973; Hayashi 1973), only to be re-classified within Paxillosida (Blake, 1987; Gale; 1987; Clark and Downey, 1992). The question of whether paxillosidans are "primitive" or "advanced" members of the Asteroidea has been a matter of considerable discussion (Fell, 1963; Blake, 1987, 1988; Gale, 1987; Lafay et al., 1995; Wada et al., 1996; and Knott and Wray, 2000). Paxillosidans were originally positioned as a primitive group based upon a skeletal morphology that appeared to be similar to early fossil asteroid species (Blake, 1987). Moreover, Luidia spp. display similarities to the somasteroid Platasterias latiradiata, considered by Fell (1963) to be a "living fossil." Blake (1972, 1982) re-examined the skeleton of P. latiladiata and concluded it was an advanced asteroid belonging to the Luidiidae. This reclassification of the Paxillosida was based upon various characteristics including not only adult skeletal morphologies, but functional considerations such as developmental mode and, importantly, tube-foot morphology of both juveniles and adults (Blake, 1987). Oguro et al. (1976) reported that newly metamorphosed juveniles of the pax-- illosidan Astropecten scoparius possessed suckered tube feet, while adults lacked suckered tube feet.

Both histological and ultrastructural studies of asteroid tube feet have been conducted (Paine, 1926, 1929; Smith, 1937, 1947; Hyman, 1955; Souza Santos, 1966; Souza Santos and Silva Sasso, 1968, 1970, 1974; Engster and Brown, 1972; Hermans, 1983; Thomas and Hermans, 1985; Flammang et al., 1994; Flammang, 1995a, 1995b; McCurley and Kier, 1995). Nonetheless, none of these morphological studies have taken a broad comparative approach. Engster and Brown (1972) examined the (typical) pointed, non-suckered tube feet of Astropecten sp. (Fig. 1A). The tube foot was divided into a stem and a tip instead of a stem and a distal disc. The tip of the tube foot was tapered, the lumen was elongated into the tip, there was a thin layer of longitudinal muscle and an accumulation of mucopolysaccharide granules in the epithelial layer (providing capacity for adhesion), and there was no branching of connective tissue. Suckered tube feet (Fig. lB) were carefully examined in Asterias vulgaris by Paine (1929) who described the basic internal morphology. A longitudinal section of the tube foot revealed a distinct stem and a flat distal disc with an outer cuticle, underlaid by an epithelium, nervous and connective tissues, longitudinal muscle, endothelium (coelomic lining), and lumen. The connective tissues were branched in the disc area and extended toward the distal end of the tube foot. The basic internal morphology of the (typical) suckered tube feet described by Paine is similar to the internal morphology of the pointed, non-suckered tube feet described above.