Flight of the Vampire: Ontogenetic Gait-Transition in Vampyroteuthis Infernalis (Cephalopoda: Vampyromorpha) Brad A
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University of Rhode Island DigitalCommons@URI Biological Sciences Faculty Publications Biological Sciences 1998 Flight of the Vampire: Ontogenetic Gait-Transition in Vampyroteuthis Infernalis (Cephalopoda: Vampyromorpha) Brad A. Seibel University of Rhode Island, [email protected] Erik V. Thuesen See next page for additional authors Follow this and additional works at: https://digitalcommons.uri.edu/bio_facpubs Terms of Use All rights reserved under copyright. Citation/Publisher Attribution Seibel, B.A.; Thuesen, E.V.; Childress, J.J.; 1998. Flight of the vampire: ontogenetic gait-transition in Vampyroteuthis infernalis (Cephalopoda: Vampyromorpha). The Journal of Experimental Biology. 201, 2413–2424. Available at: http://jeb.biologists.org/content/201/16/2413 This Article is brought to you for free and open access by the Biological Sciences at DigitalCommons@URI. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of DigitalCommons@URI. For more information, please contact [email protected]. Authors Brad A. Seibel, Erik V. Thuesen, and James J. Childress This article is available at DigitalCommons@URI: https://digitalcommons.uri.edu/bio_facpubs/14 The Journal of Experimental Biology 201, 2413–2424 (1998) 2413 Printed in Great Britain © The Company of Biologists Limited 1998 JEB1479 FLIGHT OF THE VAMPIRE: ONTOGENETIC GAIT-TRANSITION IN VAMPYROTEUTHIS INFERNALIS (CEPHALOPODA: VAMPYROMORPHA) BRAD A. SEIBEL*, ERIK V. THUESEN† AND JAMES J. CHILDRESS Oceanic Biology Group, Marine Science Institute, University of California, Santa Barbara, CA 93106, USA *e-mail: [email protected] †Present address: The Evergreen State College, Olympia, WA 98505, USA Accepted 3 June; published on WWW 27 July 1998 Summary Vampyroteuthis infernalis is a cosmopolitan cephalopod increased use of the fins for lift-based propulsion. Fin that lives in the oxygen minimum layer between 600 and swimming appears to be the primary means of propulsion 800 m depth. Morphometric and physiological studies have at all adult sizes. The negative allometry of CS activity in indicated that V. infernalis has little capacity for jet mantle and arm muscle is consistent with the scaling of propulsion and has the lowest metabolic rate ever oxygen consumption previously measured for V. infernalis measured for a cephalopod. Because fin swimming is and with the scaling of aerobic metabolism observed in inherently more efficient than jet propulsion, some of the most animals. The unusual positive allometry of fin muscle reduction in energy usage relative to other cephalopods CS activity suggests that the use of fins is either relatively may result from the use of fins as the primary means of more important or more costly in larger animals. Positive propulsion. V. infernalis undergoes a rapid metamorphosis scaling of ODH activity in all tissues suggests that fin which consists of changes in the position, size and shape of propulsion, jet propulsion and medusoid ‘bell-swimming’ the fins. This suggests that there are changes in the selective are all important for burst escape responses. Enzyme factors affecting locomotion through ontogeny. The present activities in Cirrothauma murrayi are consistent with fin- study describes these changes in relation to models for swimming observed from submersibles, while those in underwater ‘flight’. Citrate synthase (CS) and octopine Opisthoteuthis californiana suggest a strong reliance on dehydrogenase (ODH) activities, indicative of aerobic and medusoid swimming using the arms. The transition from anaerobic metabolism, respectively, were measured in fin, jet propulsion to paired-fin ‘flight’ with increasing body mantle and arm tissue across a range of body size of four size in Vampyroteuthis infernalis appears functionally to be orders of magnitude. The low enzymatic activities in both an ontogenetic ‘gait-transition’. posterior and anterior fin tissue and the relatively high activity in mantle muscle prior to metamorphosis indicate Key words: metabolism, scaling, metamorphosis, locomotion, flight, that jet propulsion using mantle contraction is the primary deep-sea, Cephalopoda, Vampyromorpha, Vampyroteuthis infernalis, means of propulsion in juvenile V. infernalis. The increase Cirrata, Opisthoteuthis californiana, Cirrothauma murrayi, in CS activity with size after metamorphosis suggests an Coleoidea. Introduction Vampyroteuthis infernalis Chun, 1903 is a bathypelagic animal. Anatomical studies led Pickford (1949) to suggest that cephalopod which inhabits the oxygen minimum layer V. infernalis spends the majority of its time ‘floating, rather (600–800 m) throughout the world’s temperate and tropical than in active progression’. Young (1964) supported this view, oceans. It shares many characteristics with both squids (Order saying that V. infernalis ‘has no more control over its location Teuthoidea) and the octopods (Pickford, 1949), but was placed in the water than that exercised by the common jellyfish’. in its own order (Vampyromorpha; Pickford, 1936) primarily Seibel et al. (1997) showed that V. infernalis has the lowest on the basis of the presence of sensory filaments (Young, metabolic rate of any cephalopod ever measured, comparable 1967). It was named for its jet-black skin, the caped appearance with that of many medusae (Thuesen and Childress, 1994). of the webbing between the arms, and eyes that appear red However, in situ and laboratory observations (Hunt, 1996) of under some light conditions. Beebe (1926) describes V. Vampyroteuthis infernalis reveal fairly active fin swimming. infernalis as ‘a very small but terrible octopus, black as night, Broad fins with a well-developed muscular band in the anterior with ivory white jaws and blood red eyes’. In contrast to this margin attached to the broad gladius (chitinous support horrific description, V. infernalis appears to be a rather docile structure) appear to be the main means of propulsion (Clarke, 2414 B. A. SEIBEL, E. V. THUESEN AND J. J. CHILDRESS 1988), and the fin muscles, while relatively weak, are the turbulence and skin abrasion of specimens in the net. strongest muscles in the animal (Young, 1964). Fin shape (see Specimens were weighed on a motion-compensated ship-board Lauder and Jayne, 1996) and motion and the surprisingly high precision balance system (Childress and Mickel, 1980). swimming speeds observed (Hunt, 1996) in adult vampire squid The one specimen of Opisthoteuthis californiana (Berry, are consistent with models for underwater ‘flight’ reported for a 1949) was captured in a benthic otter trawl at 500 m depth in the variety of taxa (Satterlie et al. 1985; Bannasch, 1994; Davenport Santa Barbara Basin (34°17′N, 120°2′W). Our single rare et al. 1984; Vogel, 1994; Feldkamp, 1987). The unique specimen of Cirrothauma murrayi (Chun, 1913) was captured ‘metamorphosis’ observed for V. infernalis, which consists of in midwater at a depth of 2200 m. Animals were generally changes in the position, size and shape of the fins (Pickford, transferred to chilled sea water and dissected within 24 h of 1949), suggests that fin locomotion is important but that the reaching the surface. All animals, with the exception of selective factors influencing locomotion change with ontogeny Cirrothauma murrayi, were able to swim actively on board ship. or size. The nature and cause of ontogenetic- (or at least size-) C. murrayi appeared freshly dead and was probably killed by related changes in metabolism and locomotion of all animals, either pressure or temperature shock (the animal was too large including cephalopods, have been the subject of intense study to fit in the cod-end) within the few minutes prior to reaching and debate (Preuss et al. 1997; West et al. 1997; Seibel et al. the surface. It is not known to what extent the enzymatic 1997; Villanueva et al. 1995; Hoar et al. 1994; Webb, 1994; activities may have degraded in this specimen. Voucher Childress and Somero, 1990; Somero and Childress, 1980, 1985; specimens are housed in the Department of Invertebrate Zoology for a review, see Schmidt-Nielsen, 1984). at the Santa Barbara Museum of Natural History. Shallow-living squids have extremely high metabolic rates (O’Dor and Webber, 1986) and are known to achieve Live animal observations remarkable speeds from jet propulsion using mantle Immediately following capture, some specimens were contraction (Cole and Gilbert, 1970). Deeper-living placed in ship-board plankton kreisels connected to a chilled cephalopods, however, have lower metabolic rates than their seawater system (Monterey Bay Aquarium) for photography shallow-living counterparts resulting from reduced selection and observation. The small size of the aquaria (0.5 m in for strong locomotory abilities for predator–prey interactions diameter) limited the motion of the animals and so locomotory in the light-limited deep sea (Seibel et al. 1997). Where high observations are reported in the text only to augment reports speed is not a priority, fin propulsion, being more economical of in situ observations (Hunt, 1996; deGruy and Brown, 1995). than jet propulsion, may be more prevalent. To test this Drawings published here are based on personal in situ hypothesis and to assess the role of body size and development observations (by J. J. Childress from the DSRV Alvin), ship- on metabolism and locomotion, we measured enzymatic board observations (video and photography; B. A. Seibel; activities in fin, mantle and arm tissue of Vampyroteuthis David Wrobel, Monterey Bay Aquarium), in situ