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Circadian Rhythms of Crawling and Swimming in the Nudibranch Mollusc Melibe Leonina

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Circadian Rhythms of Crawling and Swimming in the Nudibranch Mollusc Melibe Leonina University of New Hampshire University of New Hampshire Scholars' Repository Institute for the Study of Earth, Oceans, and Jackson Estuarine Laboratory Space (EOS) 12-1-2014 Circadian Rhythms of Crawling and Swimming in the Nudibranch Mollusc Melibe leonina Winsor H. Watson III University of New Hampshire, Durham, [email protected] James M. Newcomb University of New Hampshire, Durham Lauren E. Kirouac New England College Amanda A. Naimie New England College Follow this and additional works at: https://scholars.unh.edu/jel Recommended Citation Newcomb, J. M., L. E. Kirouac, A. A. Naimie, K. A. Bixby, C. Lee, S. Malanga, M. Raubach and W. H. Watson III. 2014. Circadian rhythms of crawling and swimming in the nudibranch mollusk Melibe leonina. Biol. Bull. 227: 263-273. https://doi.org/10.1086/BBLv227n3p263 This Article is brought to you for free and open access by the Institute for the Study of Earth, Oceans, and Space (EOS) at University of New Hampshire Scholars' Repository. It has been accepted for inclusion in Jackson Estuarine Laboratory by an authorized administrator of University of New Hampshire Scholars' Repository. For more information, please contact [email protected]. Reference: Biol. Bull. 227: 263–273. (December 2014) © 2014 Marine Biological Laboratory Circadian Rhythms of Crawling and Swimming in the Nudibranch Mollusc Melibe leonina JAMES M. NEWCOMB1,*, LAUREN E. KIROUAC1,†, AMANDA A. NAIMIE1,‡, KIMBERLY A. BIXBY2,§, COLIN LEE2, STEPHANIE MALANGA2,¶, MAUREEN RAUBACH2, AND WINSOR H. WATSON III2 1Department of Biology and Health Science, New England College, Henniker, New Hampshire 03242; 2Department of Biological Sciences, University of New Hampshire, Durham, New Hampshire 03824 Abstract. Daily rhythms of activity driven by circadian located in, or near, the eyes. Thus, locomotion in Melibe clocks are expressed by many organisms, including mol- appears to be influenced by both ocular and extraocular luscs. We initiated this study, with the nudibranch Melibe photoreceptors, although the former appear to have a greater leonina, with four goals in mind: (1) determine which influence on the expression of circadian rhythms. behaviors are expressed with a daily rhythm; (2) investigate which of these rhythmic behaviors are controlled by a Introduction circadian clock; (3) determine if a circadian clock is asso- ciated with the eyes or optic ganglia of Melibe,asitisin Most organisms are typically more active at certain times several other gastropods; and (4) test the hypothesis that of the day or night, and this tendency is controlled, in part, Melibe can use extraocular photoreceptors to synchronize by endogenous circadian clocks. When these organisms are its daily rhythms to natural light-dark cycles. To address placed in constant light, or constant darkness, they no longer these goals, we analyzed the behavior of 55 animals ex- receive light cues about the time of day, but they continue posed to either artificial or natural light-dark cycles, fol- to express daily rhythms of behavior that have a period of lowed by constant darkness. We also repeated this experi- “about a day” and thus they are referred to as “circadian” ment using 10 animals that had their eyes removed. rhythms. Circadian rhythms of behavior, along with the Individuals did not express daily rhythms of feeding, but molecular clocks underlying these rhythms, have been stud- they swam and crawled more at night. This pattern of ied in a wide array of animals (Takahashi, 1991, 1995; locomotion persisted in constant darkness, indicating the Dunlap, 1999; Hastings et al., 2007; Allada and Chung, presence of a circadian clock. Eyeless animals also ex- 2010). However, the neural mechanisms by which these pressed a daily rhythm of locomotion, with more locomo- well-understood molecular clocks ultimately influence the tion at night. The fact that eyeless animals synchronized expression of circadian behaviors have not been fully elu- their locomotion to the light-dark cycle suggests that they cidated. To bridge this gap, it would be advantageous to can detect light using extraocular photoreceptors. However, study an animal with clearly defined and easily accessible in constant darkness, these rhythms deteriorated, suggesting neural circuitry underlying a specific behavior that is ex- that the clock neurons that influence locomotion may be pressed with a circadian rhythm. Gastropods have been very useful model organisms for neuroethological investigations during the last several decades, and using gastropod model * To whom correspondence should be addressed. E-mail: jnewcomb@ nec.edu systems may help elucidate the connection between clocks † Current address: Massachusetts College of Pharmacy and Health Sci- and certain behaviors. ence University, Manchester, NH 03101. Circadian rhythms of locomotion have been demon- ‡ Current address: Department of Microbiology and Immunology, strated in six gastropods—Aplysia californica (Kupfer- Geisel School of Medicine, Dartmouth College, Hanover, NH 03755. mann, 1968; Jacklet, 1972; Lickey et al., 1977), Bulla § Current address: Alzheimer’s Disease and Memory Disorders Center, Rhode Island Hospital, Providence, RI 02903. gouldiana (Block and Davenport, 1982), Bursatella leachi ¶ Current address: Brigham and Women’s Hospital, Boston, MA 02115. plei (Block and Roberts, 1981), Helisoma trivolvis (Kava- Abbreviations: DD, constant darkness; LD, light-dark. liers, 1981), Limax maximus (Sokolove et al., 1977), and 263 This content downloaded from 132.177.229.130 on May 17, 2017 11:39:47 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 264 J. M. NEWCOMB ET AL. Melanoides tuberculata (Beeston and Morgan, 1979). Ap- cuitry underlying a behavior that is expressed with a circa- lysia and Bursatella exhibit diurnal activity in light-dark dian rhythm. regimes (Kupfermann, 1968; Jacklet, 1972; Kupfermann and Carew, 1974; Lickey et al., 1977; Block and Roberts, Materials and Methods 1981), whereas Bulla, Helisoma, and Limax are nocturnal (Sokolove et al., 1977; Kavaliers, 1981; Block and Daven- Animal collection and housing port, 1982), and Melanoides exhibits crepuscular patterns of Specimens of Melibe were obtained during 2011–2013 locomotor activity (Beeston and Morgan, 1979). In Aplysia, from two areas. Some animals were collected in southern Bursatella, and Bulla, circadian pacemakers have been lo- California by Marinus Scientific (Newport Beach, CA) and calized to the eyes, which, when isolated in vitro, exhibit the Monterey Abalone Company (Monterey, CA), while circadian rhythms of electrical activity in constant darkness others were obtained from the waters surrounding San Juan (Jacklet, 1969; Block and Roberts, 1981; Block and Wal- Island and Shaw Island, Washington. Animals used in lace, 1982). However, further studies have indicated that the 2011–2012 were shipped to New England College (NEC) eyes are not the only circadian pacemakers in Aplysia and and the University of New Hampshire (UNH) within 24 h of Bulla (Lickey et al., 1977, 1983; Roberts and Xie, 1996). collection and housed in tanks filled with either artificial While the aforementioned investigations into the circa- seawater (Carolina Biological) or natural seawater from the dian rhythms of locomotion in gastropods have revealed a UNH Coastal Marine Laboratory (New Castle, NH). The great deal about the location and nature of the underlying seawater was maintained at temperatures between 10 and circadian clocks, the link between these clocks and the 15 °C and salinities of 29–32 ppt. Animals were typically neural networks controlling locomotion has yet to be deter- fed Artemia nauplii 2–3 times per week prior to experi- mined. Thus, we have turned our attention to another spe- ments. Lighting conditions matched those used during sub- cies, Melibe leonina (Gould, 1852), because the central sequent LD experiments—either 10 h of light and 14 h of pattern generator underlying at least one form of locomotion darkness (10:14 LD) or 12:12 LD. Light was provided with in this nudibranch is well understood. Melibe exhibits two 40–60-W compact fluorescent bulbs, which typically re- modes of locomotion—crawling, like most other gastro- sulted in daytime light levels of 215–290 lux. pods, and swimming, via lateral body flexions (Watson et The animals collected and used in the winter and spring al., 2001; Lawrence and Watson, 2002). Melibe swims as an of 2013 (n ϭ 18) were housed in outdoor flow-through escape mechanism (Lawrence and Watson, 2002), sponta- seawater tanks at the Friday Harbor Laboratories (FHL; neously for reasons that are currently poorly understood, Friday Harbor, WA), less than 2 km from where they were and perhaps as a form of population dispersal (Mills, 1994). collected. At this time of year, the ambient water tempera- Both crawling and swimming are exhibited with greater ture ranged from 8–10 °C. These animals fed ad libitum on frequency at night, and preliminary evidence from animals prey carried into their tanks via the flow-through seawater in 36–48 h of constant darkness suggests that these forms of system, and they were subjected to ambient LD cycles. As locomotion may be influenced by a circadian clock (New- indicated in subsequent figures, the light intensity during the comb et al., 2004). Importantly, the central pattern genera- day was typically 375–800 lux. tor underlying swimming has been characterized and con- sists of only eight individually identifiable neurons Activity experiments
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