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Locomotor, Chromatic, Postural, and Bioluminescent Behaviors of the Deep-Sea Squid Octopoteuthis Deletron Young 1972

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Locomotor, Chromatic, Postural, and Bioluminescent Behaviors of the Deep-Sea Squid Octopoteuthis Deletron Young 1972 Reference: Biol. Bull. 216: 7–22. (February 2009) © 2009 Marine Biological Laboratory Behaving in the Dark: Locomotor, Chromatic, Postural, and Bioluminescent Behaviors of the Deep-Sea Squid Octopoteuthis deletron Young 1972 STEPHANIE L. BUSH1,2,*, BRUCE H. ROBISON2, AND ROY L. CALDWELL1 1University of California, Berkeley, Department of Integrative Biology, Berkeley, California 94720; and 2Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd., Moss Landing, California 95039 Abstract. Visual behaviors are prominent components of tion (Packard and Sanders, 1971; Packard and Hochberg, intra- and interspecific communication in shallow-water 1977; Hanlon and Messenger, 1988, 1996). These cephalo- cephalopods. Meso- and bathypelagic cephalopods were be- pods assess their surroundings with well-developed vision, lieved to have limited visual communication, other than biolu- though in most species vision is monochromatic (Messen- minescence, due to the reduced illumination at depth. To ger, 1977; Kito et al., 1992; Shashar et al., 1998; Sweeney explore potential visual behaviors in mesopelagic squid, we et al., 2007). Individuals are capable of polyphenism con- used undersea vehicles to observe 76 individuals of Octopo- sisting of near instantaneous changes in appearance through teuthis deletron. In contrast to predictions, we found this spe- a broad range of camouflage and communication methods cies capable of a variety of visually linked behaviors not (Packard and Sanders, 1971; Packard and Hochberg, 1977; previously reported for a deep-ocean cephalopod. The resultant Hanlon and Messenger, 1988; Roper and Hochberg, 1988; ethogram describes numerous chromatic, postural, locomotor, Hanlon et al., 1999a; Barbato et al., 2007). An individual’s and bioluminescent behavioral components. A few common overall appearance, or body pattern, is composed of the body patterns—the whole appearance of the individual involv- following component types: chromatic, textural, postural, ing multiple components—are characterized. The behaviors and locomotor. Chromatic expression is achieved by pig- observed from individual squid were compared using a Non- mented chromatophores, underlying reflective leucophores metric Multi-Dimensional Scaling (NMDS) ordination, onto and iridophores, and polarizing elements (Mirow, 1972a, b; which hydrographic and observation parameters were mapped. Messenger, 1974; Packard and Hochberg, 1977; Cloney and Observation length, specimen collection, and contact with the Brocco, 1983; Packard, 1988; Mathger and Hanlon, 2007). vehicle affected which behaviors were performed. A separate Skin texturizing is accomplished with dermal muscles NMDS, analyzing the body patterns, indicated that these sets (Packard and Hochberg, 1977); this component type is of behavioral components could be visualized as groups within present in octopuses and cuttlefishes but absent from squids. the NMDS ordination. While the functional roles of the be- Postural components are the positions of muscular, flexible haviors described are not yet known, our findings of numerous limbs and body (Packard and Sanders, 1971). Locomotor behaviors in O. deletron clearly indicate that bioluminescence components and maneuvers are movements of the whole is not the sole method of visual communication by deep-sea body or its constituents (Roper and Hochberg, 1988). Vari- squid. ations of bioluminescence, or biologically derived light, expressed by an individual can also be considered a type of Introduction body patterning component (Herring, 2000). Body patterns used in inter-specific communication en- Shallow-water squids, octopuses, and cuttlefishes are re- able cephalopods to achieve search image impedance by nowned for their inter- and intraspecific visual communica- using polyphenism to hinder recognition (Hanlon et al., 1999a); perform deimatic behavior to startle potential pred- Received 21 May 2008; accepted 15 October 2008. ators (Edmunds, 1974); and implement effective preda- * To whom correspondence should be addressed. E-mail: [email protected] tion—for example, Sepia officinalis may use the dynamic Abbreviations: NMDS, Non-metric Multi-Dimensional Scaling ordination. Passing Cloud body pattern to distract prey prior to attack 7 8 S. L. BUSH ET AL. (Hanlon and Messenger, 1988). There are multiple ways in Camouflage by deep-sea animals centers almost exclusively which polyphenism is used to camouflage the individual. In on the few successful tactics presented above: transparency, background resemblance the individual approximates a ran- silvering, counter-illumination, and red coloration. There has dom sample of the visual background (Endler, 1981). The been no a priori reason to expect deep-sea cephalopods to be juxtaposition of colored areas in disruptive coloration at- different, despite the multitude of capabilities known for shal- tract a predator’s attention away from the animal’s outline low-dwelling cephalopods (Moynihan and Rodaniche, 1982; (Cott, 1940; Chiao et al., 2007). Counter-shading is used to Hanlon and Messenger, 1996). Consistent with this reasoning, cancel shadows on a body surface caused by uneven illu- most deep-sea cephalopods have been found to possess sil- mination (Cott, 1940). Finally, in masquerade the animal vered eyes and digestive glands that are counter-illuminated, resembles an inedible or non-prey entity (Endler, 1981; and bodies that are transparent or of dark, usually red, colora- Hanlon et al., 1999a). tion (Chun, 1910; Voss, 1967; Herring, 1988). Body patterning may be used in intraspecific communi- Octopoteuthis deletron Young 1972 is a solitary meso- cation to attract and court mates, repel or deceive sexual pelagic squid that is found in the eastern North Pacific from competitors, coordinate movements within a shoal, and Alaska to Baja California, off Peru, and perhaps off Japan warn conspecifics of predators (Moynihan and Rodaniche, (Young, 1972). Individuals attain a mantle length of 17 cm; 1982; Hanlon and Messenger, 1996; Hunt et al., 2000). possess large, elliptical fins; and have long arms with hooks Species that experience diverse environmental encounters in place of suckers along most of the length (Young, 1972). may benefit from a varied communication repertoire. Body Members of the family Octopoteuthidae lose the tentacles at patterning diversity in cephalopods is thought to be influenced an early life-stage, leaving just the eight arms to function in by activity patterns (diel vs. nocturnal), social behavior, habitat prey capture (Young, 1972). Individual O. deletron possess complexity, predators, and reproductive mode (Hanlon and a variety of photophores, the most conspicuous of which are Messenger, 1988). Cephalopods that are either asocial or noc- single organs that occupy the terminus of each arm (Young, turnally active, use simple reproductive modes, or dwell in 1972; Vecchione et al., 2002). This species also has a homogeneous environments may display fewer body patterns number of ventrally directed photophores: a series along the than other cephalopods (Hanlon and Messenger, 1988). In the core of the four ventral arms; an arm base organ on arm deep ocean, most species are asocial, the water is a nearly pairs II, III, and IV; a pair of small medial head organs; a homogenous visual substrate, and both intra- and interspecific photophore posterior to each eye; a pair of visceral photo- interactions are infrequent due to low animal densities (Chil- phores situated ventral to the ink sac; and a single posterior dress, 1995; Herring, 2000). In addition, below 200 m, more “tail” organ (Young, 1972). Counter-illumination by ventral than 99% of surface illumination has been attenuated, and this photophores has been observed from the congener Octopo- “twilight” environment makes visual communication less via- teuthis neilseni (Young and Vecchione, 2006). ble than in well-lit habitats (McFall-Ngai, 1990). Conse- quently, limited body patterning has been predicted for deep- Materials and Methods ocean cephalopods (Hanlon and Messenger, 1996; Nixon and Young, 2003). Observations were made during dives of two remotely The characteristic distribution of light in the deep sea has operated vehicles (ROVs) operated by the Monterey Bay led to convergence in camouflage tactics across taxa Aquarium Research Institute (MBARI). The ROV Ventana, (Johnsen, 2001; Marshall, 1979; Johnsen, 2001, 2005; War- a 40-hp electro-hydraulic vehicle, ranges to 1500 m. Illu- rant and Locket, 2004). In the relatively well-lit euphotic mination is provided by six 400-W DSPL HID Daylight and upper mesopelagic zones, individuals are often counter- lamps. The ROV Tiburon is an electric vehicle that ranges shaded, transparent, have highly reflective silvered sides, to 4000 m; it has four 400-W DSPL HMI lights for illumi- and/or have laterally flattened bodies to minimize their nation. Both of these arrays produce illumination in the silhouette (Johnsen, 2001). Below 30 m depth, red wave- daylight range (5500–5600 °K). One important difference lengths are completely absent from ambient light. At these between these vehicles is that hydraulic power produces depths, non-transparent individuals often have red, purple, more noise than electric power; the ROV Tiburon is quieter brown, or black body coloration, which appears black in the in the water. Each ROV dive is recorded on Panasonic D5 absence of red light (McFall-Ngai, 1990). In the meso- high definition videocassettes or Sony Digital Betacam stan- pelagic (200–1000 m), light down-welling from the surface
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