Metabolic Rate of Embryonic Little Skate, Raja erinacea (Chondrichthyes: Batoidea): The Cost of Active Pumping

Near-hatching embryonic little skates, Raja erinacea, are highly active within their egg capsules, displaying a characteristic tail beating, which pumps water through the capsule. We measured the metabolic rate of late-stage embryos to determine whether oxygen sufficient for the embryo’s needs will diffuse through the egg capsule, and to assess the energetic cost of tail beating. Metabolic rate was inferred from oxygen consumption rates while embryos were in the capsules, unencapsulated, and anesthetized and unencapsulated. Anesthesia inhibited voluntary movements, including tail wagging, allowing an estimate of the standard metabolic rate (SMR). Averaged over five embryos, the SMR was 0.032 ± 0.004 ml O2 g–1 hr–1. There was no significant difference in metabolic rate between encapsulated (0.058 ± 0.009 ml O2 g–1 hr–1) and unencapsulated (0.049 ± 0.009 ml O2 g–1 hr–1) skates. Tail beating was found to be energetically expensive, requiring a 53%–81% increase over the SMR. From literature values for the oxygen permeability of the egg capsule we conclude that tail beating is required to supply sufficient oxygen to the embryonic skate. This observation is consistent with the proposal that actively pumping water through the capsule, by tail beating, has played an evolutionary role in the shape of the capsule. J. Exp. Zool. 283:13–18, 1999. © 1999 Wiley-Liss, Inc. Skates are dorsoventrally flattened chondrichthian fishes inhabiting shallow and deep water of all the oceans. The little skate (Raja erinacea) is a common member of the Northwestern Atlantic marine ecosystem. Like many elasmobranchs, populations of this fish have come under increasing fishing pressure off the coast of New England, primarily because of the decrease in groundfish in the area (Hutchings and Meyers, ’94; Meyers et al., ’96). There is a growing targeted fishery for elasmobranchs in the region, including skates. Reproduction in elasmobranchs is generally characterized by low fecundity and consequently they are at risk of over-exploitation (Cailliet, ’90). Currently, there is little known about hatching success and the survival of skate offspring in the wild, particularly because the spawning grounds have not been identified for this species. An increased understanding of the reproduction and early development of elasmobranchs is crucial to developing responsible management regimes for these fishes. All skates are oviparous, laying rectangular egg capsules that usually contain a single embryo (Fig. 1). A distinctive feature of most of these capsules is the horns that emanate from the corners, two pointing posteriorly and two anteriorly. Each horn has a slit that, although plugged with albumen early in development, allows sea water to enter the case during the latter two thirds of the embryonic period (Clark, ’22; Luer and Gilbert, ’85). Skate embryos remain in the egg capsule for several months (e.g., Raja eglanteria) to a year or longer (e.g., Raja erinacea) prior to hatching. While in the egg case, skate embryos demonstrate a characteristic tail-beating behavior. This *Correspondence to: Adam Summers, Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003. E-mail: [email protected] Received 3 February 1998; Accepted 1 May 1998 14 J.B.K. LEONARD ET AL. movement is rhythmic and rapid and has also been observed in several other oviparous elasmobranch species (e.g., Raja eglanteria, Luer and Gilbert, ’85; Scyliorhinus canicula, Diez and Davenport, ’87). Luer and Gilbert (’85) reported that the embryonic activity increased within the egg case after the albumen plugs were removed from the horns. The embryonic skate tail is equipped with a thin appendage which is visible during the last few weeks before hatching (Libby, ’59; Long and Koob, ’97) and which appears to be lost after hatching in most skate species (Clark, ’23; Bigelow and Schroeder, ’53). This appendage is frequently inserted into a horn of the egg case where it is rapidly oscillated (Fig. 1) (Clark, ’22). This rhythmic action pumps water through the capsule (Long and Koob, ’97). While the purpose of the pumping is not entirely clear, it has been observed that blocking the horns with sediment causes 100% mortality in the embryos (Richards et al., ’63). The assumption is, that though the capsule is permeable to many metabolites (Foulley and Mellinger, ’80; Evans, ’81), as the embryo grows diffusion will not suffice, and water must be pumped through the capsule to obtain oxygen and/or remove metabolic waste. In addition to this active pumping mechanism it has been shown experimentally that water flows through the capsule in the presence of an external current (Koob and Summers, ’96). Such a method of ventilating the capsule comes with no metabolic cost to the embryo since it relies only on the shape of the capsule and the speed of the external current. The purpose of this study was twofold: (1) to determine the standard metabolic rate of an embryonic batoid fish; and (2) to quantify the cost to the embryo of actively pumping water through the capsule.