Batoid Wing Skeletal Structure: Novel Morphologies, Mechanical Implications, and Phylogenetic Patterns

JOURNAL OF MORPHOLOGY 264:298–313 (2005) Batoid Wing Skeletal Structure: Novel Morphologies, Mechanical Implications, and Phylogenetic Patterns Justin T. Schaefer* and Adam P. Summers University of California, Irvine, Department of Ecology and Evolutionary Biology, Irvine, California 92697-2525 ABSTRACT The skeleton of the “wings” of skates and oscillatory locomotion. These swimming strategies rays consists of a series of radially oriented cartilaginous can be described by the number of waves (f) moving fin rays emanating from a modified pectoral girdle. Each across the wing during steady swimming (Rosen- fin ray consists of small, laterally oriented skeletal ele- berger, 2001). Oscillators appear to fly through the ments, radials, traditionally represented as simple cylin- water, flapping their wings such that f is less than drical building blocks. High-resolution radiography re- 0.5 at any given time (Heine, 1992). In contrast, veals the pattern of calcification in batoid wing elements, Ͼ and their organization within the fin ray, to be consider- undulators often have many waves (f 1) moving ably more complex and phylogenetically variable than along the wing. Fish that swim with f between 0.5 previously thought. Calcification patterns of radials var- and 1 have been categorized as “semi-oscillatory”. ied between families, as well as within individual pectoral The wing skeleton upon which these locomotor fins. Oscillatory swimmers show structural interconnec- waves are propagated consists of an array of serially tions between fin rays in central areas of the wing. Mor- repeating cartilaginous elements (Fig. 1). The carti- phological variation was strongly predictive of locomotor laginous skeleton of batoids is mineralized to vary- strategy, which we attribute to oscillatory swimmers ing degrees, usually taking the form of a thin layer needing different areas of the wing stiffened than do un- of tiles, tesserae, arranged on the surface of an undulatory swimmers. Contributions of various forms of cal- mineralized core (Applegate, 1967; Kemp and We- cification to radial stiffness were calculated theoretically. Results indicate that radials completely covered by min- strin, 1979; Clement, 1992; Summers et al., 2003; De eralized tissue (“crustal calcification”) were stiffer than Carvalho et al., 2004). The wing skeleton originates those that were calcified in chain-like patterns (“catenated on the craniocaudally expanded pectoral girdle and calcification”). Mapping this functionally important vari- is formed by many long, tapering fin rays (Mivart, ation onto a phylogeny reveals a more complicated pattern 1878; Compagno, 1999). Each fin ray is composed of than the literature suggests for the evolution of locomotor cylindrical skeletal elements, radials, stacked end- mode. Therefore, further investigation into the phyloge- to-end, much like carpals. The fin rays of most ba- netic distribution of swimming mode is warranted. J. Mor- toids bifurcate once or twice before reaching the phol. 264:298–313, 2005. © 2005 Wiley-Liss, Inc. edge of the wing (Fig. 1). This complicated skeleton is actuated by long thin KEY WORDS: cartilage; calcification; tesserae; swimming; undulation; oscillation; flapping; robotics muscles that run from the craniocaudally expanded pectoral girdle along each of the fin rays, inserting on every radial (Liem and Summers, 1999). During locomotion, the radials are flexed dorsally by dorsal Batoid fishes (stingrays, skates, sawfishes, and adductor muscles and ventrally flexed by less mas- guitarfishes), are cartilaginous fishes (Chondrich- sive ventral abductors. Although the range of motion thyes) characterized by dorsoventrally compressed between any two adjacent radials in a fin ray is bodies ranging in shape from circular to rhomboidal small (ϳ15°) (Schaefer, pers. obs.), there are enough (Compagno, 1977). They inhabit all the oceans of the radials, and therefore interradial joints, that the world and have invaded freshwater systems on five wingtips of rapidly swimming oscillatory rays often continents (Lovejoy, 1996; Compagno, 2001). Their pectoral fins are greatly enlarged and fused to the cranium, forming large, wing-like structures. These highly modified pectoral fins are usually used as the Contract grant sponsor: National Science Foundation (NSF); Con- tract grant number: IBN-0317155 (to A.P.S.); Contract grant spon- primary locomotor propulsors (Klausewitz, 1964; sors: Teledyne Corp.; Mr. and Mrs. R. Schaefer. Heine, 1992). Some basal batoids, such as sawfish and electric *Correspondence to: Justin Schaefer, 321 Steinhaus Hall, Univer- rays, do not use their pectoral fins to swim, instead sity of California, Irvine, Irvine, CA 92697-2525. relying on the plesiomorphic caudal fin-based loco- E-mail: [email protected] motor mode of their shark relatives. However, the Published online 18 April 2005 in majority of batoid fishes use their pectoral fins to Wiley InterScience (www.interscience.wiley.com) swim and fall on a continuum from undulatory to DOI: 10.1002/jmor.10331 © 2005 WILEY-LISS, INC. NOVEL MORPHOLOGIES IN BATOID WING SKELETONS 299 radial is independent of total wing flexibility, as changes in one can be counteracted by changes in the other. If we assume that the mineralized cartilage is materially the same among species and is far stiffer and stronger than unmineralized cartilage, then the flexural stiffness of the wing skeleton should be de- pendent primarily on the amount and arrangement of the mineralized tissue. In this study we investi- gate the pattern of mineralization in the wing skeleton of 12 families of batoid fishes. Our goals were to: 1) describe previously unknown mineralization patterns in radials; 2) qualitatively compare mineralization patterns; 3) describe functionally signifi- cant variation in the distribution of joints between radials; and 4) place this variation in a functional and phylogenetic context. MATERIALS AND METHODS Dorsoventral radiographs of adult specimens of 56 batoid species from 12 families and three orders were obtained from various museum collections, supplemented by specimens from the first author’s personal collection (Appendix). Additional radiographs were performed with a cabinet radiograph (Hewlett Packard, Faxitron series) using Kodak Bio-Max MR film. Voltage and exposure times for radiographs varied depending on the thick- ness of the specimen. Specimens for clearing and staining were obtained by beach seine at Seal Beach, California (California Dept. of Fish and Game permit #801060-02) and stored in a –30°C freezer prior to Fig. 1. Cleared and stained embryo of Gymnura marmorata. preparation. Tissue was dissected from the skeleton prior to Dorsal view of left side of animal is shown. Red areas indicate clearing and staining. Specimens were cleared and stained using calcification, blue is cartilage. From these images and those of a standard staining procedure which allowed for visualization of other cleared and stained embryos, we can infer that the calcifi- all mineralized portions of the skeleton (Dingerkus and Uhler, cation in batoids increases in intensity medially to laterally with 1977). Specimens were stored in glycerin and photographed in a age. glycerin bath to minimize glare. Dorsal and cross-sectional images were taken with a Nikon Coolpix 950 digital camera fitted to a Zeiss dissection scope. Digitized radiographs (1200 DPI resolution) and images of cleared and stained samples (Appendix) were touch behind their back (Rosenberger, 2001). This optimized for visual clarity in Adobe PhotoShop 7 (San Jose, CA), implies a morphological constraint: the interradial and anatomical drawings were created in Adobe Illustrator 10. joints must be mobile to give the wing flexibility, yet Phylogenetic analysis was based on the phylogeny presented by the radials must be stiff to transmit the force of the McEachran and Aschliman (2004), a strict consensus tree of 10 most parsimonious trees generated from 82 characters and 39 wing musculature. taxa. We collapsed the operational taxonomic units into families During locomotion individual radials function as based on the tentative classification presented in the same arti- end-loaded cantilevered beams. The deflection cle. We used Mesquite (Maddison and Maddison, 2004) to trace (Y ) of a cantilevered beam is: the most parsimonious evolution of the morphological characters max described here as well as the swimming modes described in 3 Rosenberger and Westneat (1999). FL It is important to keep in mind that for the majority of speci- Y ϭ (1) max 3EI mens examined for this study, radiographs were the primary source of information. For this reason, only those structures that were mineralized were evident. This does not mean that other, where F is the force of the muscle, L is the length of soft tissue structures serving the same purpose as calcified struc- the radial, E is the material stiffness and I is the tures were not present in some specimens. Another caveat to second moment of area, a measure of the distribu- these data is that the ages of the specimens are not known. In cases where morphology varies among specimens of the same tion of material around an object’s neutral axis (Vo- species, (e.g., Pteroplatytrygon violacea) or morphological varia- gel, 2003). Deflection of a loaded beam can be de- tion is exhibited by a single species in a family (e.g., Urotrygon creased in several ways: by making it shorter, micropthalmum), this variation might be due to the age of the increasing its material stiffness, or increasing the specimen, which

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