Mar Biodiv (2017) 47:735–753 DOI 10.1007/s12526-017-0649-8 RECENT ADVANCES IN KNOWLEDGE OF CEPHALOPOD BIODIVERSITY A catalog of the chromatic, postural, and locomotor behaviors of the pharaoh cuttlefish (Sepia pharaonis) from Okinawa Island, Japan Ryuta Nakajima1 & Yuzuru Ikeda2 Received: 25 March 2016 /Revised: 1 December 2016 /Accepted: 26 January 2017 /Published online: 6 February 2017 # Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017 Abstract Coleoid cephalopods such as cuttlefishes, squids, Keywords Body patterns . Cephalopods . Cuttlefish . and octopods are able to produce a diverse array of visual Catalog . Sepia pharaonis expressions that are used for mimesis and inter- and intraspe- cific communication. They achieve this by intricately combin- ing several neurally controlled behaviors, which include chro- Introduction matic, textural, postural, and locomotor components. To un- derstand this diverse range of body patterns, it is necessary to In many animal species, body color and/or texture play an develop an accurate and extensive catalog of them, which can important role in predator/prey interactions, such as crypsis then be used as a tool for future behavioral monitoring and (Endler 1978) and disruption (Cott 1940). Most animals have quantitative analyses, as well as for the identification of mor- fixed or slightly changeable appearances (Cott 1940). phologically identical sub-species. In this study, a catalog of However, coleoid cephalopods such as cuttlefishes, squids, the chromatic, postural, and locomotor behaviors was pro- and octopods are not only able to able to change their body duced for the pharaoh cuttlefish (Sepia pharaonis)fromcoast- color and texture rapidly, but also to exhibit a variety of visu- al waters of Okinawa Island, Japan. Data were collected from ally complex appearances. These appearances comprise a aquacultured animals using egg masses sampled from around combination of chromatic, textural, postural, and locomotor the island and hatched in aquaria during 2010, 2011, 2012, components for both camouflage and communication. The and 2014. In total, 53 chromatic, four supplementary chromat- total appearance of the animal is defined specifically as its ic conditions, three textural, 11 postural, and nine locomotor body pattern while components are the individual parts that components were identified and described in detail. Many of make up the body pattern (Packard 1972; Packard and the described components are similar to previously described Hochberg 1977; Moynihan 1985; Hanlon and Messenger body patterns of Sepia officinalis.However,therearenotable 1988, 1996). differences between the two species, which may indicate that The chromatic component of the body pattern is changed they use body patterns in different ways for cryptic behavior by neuromuscular control of the size of many pigment-filled and inter- and intraspecific communication. organs called chromatophores (Messenger 2001). A chro- matophore is connected to a set of radial muscles that contract and relax to change its effective surface area (Hanlon 1982). In Communicated by M. Vecchione addition, two types of light-reflective cells–iridophores and leucophores contribute to the overall color palette of the ani- * Ryuta Nakajima mal. Iridophores selectively reflect light producing iridescent [email protected] blue, green, and pink colors, and are also neurally controlled (Messenger 2001; Wardill et al. 2012). Leucophores also re- 1 Department of Art and Design, University of Minnesota Duluth, flect light, creating high-contrast white appearance 1201 Ordean Ct., Duluth, MN 55812, USA (Messenger 2001). Octopods and cuttlefishes are also able to 2 Department of Chemistry, Biology and Marine Sciences, University alter the physical texture of their skin from smooth to three- of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan dimensional by using dermal muscles to produce erectile 736 Mar Biodiv (2017) 47:735–753 papillae (Holmes 1940; Packard and Hochberg 1977). The has been used as a less subjective and repeatable cataloging postural component is changed by altering the positional ori- approach (Thomas and MacDonald 2016). entation of the flexible, muscular arms, tentacles, mantle, The pharaoh cuttlefish, Sepia pharaonis (Ehrenberg 1831), head, and fins (Packard and Sanders 1971). Finally, the loco- lives in tropical coastal waters in the Indo-Pacific region from motor component involves the movement of the entire body of 35°N to 30°S and 30°E to 140°E down to 100 m depth the individual (Roper and Hochberg 1988). Each of these (Norman and Reid 2000; Nabhitabhata and Nilaphat 1999). components can appear for seconds (acute) or for hours This species is divided into three sub-types depending on the (chronic) and can be displayed in a wide variety of combina- body pattern and geographical distribution: Type I in the tions to create the overall appearance of the animal (Packard Arabian Gulf, western Indian Ocean, and Red Sea; Type II and Hochberg 1977; Hanlon and Messenger 1996). Therefore, from Japan to the Gulf of Thailand, the Philippines, and north- each component of the body pattern of a species needs to be ern Australia; and Type III from the Andaman Sea to the cataloged and described to allow quantitative analysis of its Maldives. These three types differ in size, growth rate and in behaviors and for species identification. color patterns of mating animals. Type I and Type II males More than 100 species of cuttlefishes have been described have zebra stripes on their third arms, while Type III males to date (Jereb and Roper 2005), of which one species—the have spots on their third arms (Norman 2000). Previous stud- benthic, shallow-water common cuttlefish (Sepia ies on the body patterns of this species have particularly fo- officinalis)—is the most extensively studied for its body pat- cused on camouflage and its visual cues. These studies have tern. These studies have shown that S. officinalis can create a found that S. pharaonis’s disruptive coloration is affected wide range of body patterns allowing it to either blend into its largely by area rather than the shape or aspect ratio of a light visually rich and complex natural habitat or to stand out star- colored object on a substrate (Chiao and Hanlon 2001)and tlingly, with 87 components (42 chromatic, eight textural, 13 that visual orientation of substrate pattern has little effect on its postural, and 24 locomotor) identified and described to date body pattern selection (Shohet et al. 2006). However, aside (Holmes 1940;Boycott1958; Neill 1971;Hanlonand from 34 chromatic components assumed based on Messenger 1988). Although recent study suggests that S. officinalis (Shohet et al. 2007), there has been no extensive cuttlefishes are able to detect colors by chromatic aberration catalog of their body pattern diversity that includes chromatic, (Stubbs and Stubbs 2016), they possess one visual pigment textural, postural, and locomotor components. Hence, the aim and are color blind (Marshall and Messenger 1996;Mäthger of this study was to document the range of body pattern com- et al. 2006). Hence, their visual behavior has been directly ponents exhibited by S. pharaonis. We hope that these find- correlated with multiple visual cues, such as the scale of a ings will provide a useful foundation for the identification of light object, the edge detection, the relative tonal differences Sepia species and sub-species and for future quantitative be- between the foreground and background, and the two- and havioral analyses. three-dimensional visual depths. Visual information is gath- ered by highly developed eyes, processed by a hierarchically organized set of lobes in their brain, and then converted into an Materials and methods appropriate pattern as a motor output (Muntz and Johnson 1978;Messenger2001;Zylinskietal.2009). Egg cases of Type II S. pharaonis were collected from the In addition to S. officinalis, over 20 extensive body pattern Sunabe beach area (depth ranging from 10 to 12 m, water catalogs have been produced for other cephalopod species temperature ranging from 23 °C to 25 °C) in Okinawa including the flamboyant cuttlefish, Metasepia pfefferi Island on April of 2010, 2011, and 2012. Egg cases were (Thomas and MacDonald 2016; Roper and Hochberg 1988); immediately transported to the laboratory of the Department slender inshore squid, Doryteuthis plei (Postuma and Gasalla of Chemistry, Biology, and Marine Sciences at the University 2015); longfinned inshore squid, Doryteuthis pealeii (Hanlon of the Ryukyus, where they were reared and cultured in three et al. 1999); Large Pacific striped octopus (Caldwell et al. 20 L (300 mm diameter x 170 mm depth) cylindrical, acrylic, 2015); Humboldt squid, Dosidicus gigas (Trueblood et al. closed-system tanks (Multi-hydense®, Aqua Co., Ltd Japan). 2015); northern shortfin squid, Illex illecebrosus (Harrop All tanks were filled with artificial seawater (Tetra Marine Salt et al. 2014); deep sea squid, Octopoteuthis deletron (Bush Pro, Tetra Japan Inc., Japan), and 2 L of seawater was ex- et al. 2009); Cape Hope squid, Loligo reynaudii (Hanlon changed in each tank every few days. In addition, fresh water et al. 1994);andcommonoctopus,Octopus vulgaris was added to the tanks as required to compensate for evapo- (Packard and Sanders 1971) (reviewed by Borrelli et al. ration. The water quality (temperature, salinity, pH, and con- 2006; Hanlon and Messenger 1996). Many of these reports centration