Melibe

Figure 1: Ventral view of Melibe leonina. Anterior is to the right.

''Melibe leonina'' (Gould, 1852)[1] is a nudibranch mollusc in the suborder Dendronotoidea, which has been a model neurobiological system for almost two decades in the study of central pattern generator circuits, neuromodulation, neurotransmitter distribution/function, and behavior. (Taxonomy ID: 76178 in NCBI Taxonomy browser)

[edit] Physiology and Ecology

The body of Melibe is characterized by the lack of a radula and the presence of a large oral hood, lined with short tentacles, which it rhythmically opens and closes to capture nauplii and other zooplankton floating by in the water column (Agersborg, 1921; Hurst, 1968; Ajeska and Nybakken, 1976; Watson and Trimarchi, 1992; Watson and Chester, 1993). These animals are found primarily in eel grass and kelp beds from Alaska to California on the Pacific coast of the United States (MacFarland, 1966; McDonald, 1983). After hatching, Melibe has a planktotrophic veliger stage (Bickell and Kempf, 1983). This is followed by metamorphosis and several juvenile stages that resemble the adult in form (Page, 1993). Very little is known about the ecology of these animals, as most studies have focused on behavior and physiology in a laboratory setting. Their habitat distribution appears to be patchy and they sometimes can be seen swimming in relatively large numbers. It has been hypothesized that these “migrations” may be a method of population dispersal (Mills, 1994).

[edit] Chemical and Behavioral Defenses

As with many other nudibranchs, they secrete chemicals from epithelial glands (Ayer and Andersen, 1983) that likely serve as predator deterrents, although little is known about the level and nature of natural predation. At least two of these chemicals have been identified as 2,6-dimethyl-5-heptenal and 2,6-dimethyl-5-heptonic acid (Ayer and Andersen, 1983) and are least partly responsible for the sweet, musky scent of these animals. 2,6-dimethyl-5-heptenal has also been shown to be created de novo by Melibe, as opposed to co-opting it from their diet as is commonly done by many other nudibranchs (Barsby et al., 2002). Melibe also exhibits a rhythmic escape response, lateral flexion swimming, to the touch of a predatory seastar (Lawrence and Watson, 2002) and this swimming has been the subject of neurophysiological study.

[edit] Organization of the central nervous system

Figure 2: Schematic of Melibe central ganglia. C=Cerebral Ganglion; P=Pleural Ganglion; PD=Pedal Ganglion; S=statocyst; T=Tentacular Lobe. Body wall nerves are named after their ganglion of origin plus the number indicated.

The central nervous system of Melibe consists of four bilaterally symmetric ganglia (Hurst, 1968; Watson et al., 2001). As with all other nudibranchs (Chase, 2002), the cerebral and pleural ganglia are fused together to form a cerebropleural ganglia. Melibe also has a small ganglion associated with the cerebropleural ganglion that is not commonly found in other nudibranchs, the tentacular lobe. Lateral to the cerebropleural ganglia are the pedal ganglia. Nerves emanate from the brain to the periphery. In general, nerves emanating from the cerebral ganglia project to the anterior region of the animal, such as the oral hood, rhinophores, mouth, esophagus, and buccal ganglion. Nerves from the pedal ganglia project to the foot and nerves from the pleural ganglia project to the posterior region of the animal and visceral organs. The eyes, which are not image-formed are located almost directly on the brain as is true of some other nudibranchs.

Each ganglion, with the exception of the tiny tentacular lobe, is comprised of hundreds of individual neurons. These neurons can range in size from only a few microns in diameter to upwards of 0.5 millimeters in diameter. Individual neurons are consistently identifiable between animals, although only a dozen or so of these neurons have been identified and characterized to date (Newcomb and Watson, 2001; Thompson and Watson, 2005; Baltzley, 2006; Newcomb and Katz, 2007).

[edit] Feeding

Melibe has a unique form of feeding compared to other nudibranchs (Hurst, 1968). First, unlike most gastropods, Melibe lacks a radula and a buccal mass. Second, it has a large oral hood, lined with two rows of tentacles. Melibe opens and closes its oral hood to capture nauplii, zooplankton, and other small organisms present in the water column. The oral hood is controlled by a variety of muscles and probably also hemal pressure. The opening and closing of the oral food during feeding is a rhythmic behavior most likely controlled by a central pattern generator (Watson and Trimarchi, 1992). Due to the lack of a radula and buccal mass, the buccal ganglia are not associated with muscular movements of these structures and instead are involved with movements of the esophagus to transport food from the mouth to the stomach (Trimarchi and Watson, 1992). The frequency of rhythmic feeding movements by the oral hood is proportional to the concentration of prey in the water and is stimulated by both tactile and chemical cues (Watson and Chester, 1993). Stochastic analysis of feeding and other behaviors has confirmed the tendency for Melibe to continually feed as long as food is present and additionally determined that larger animals have a higher probability of spontaneously transitioning from resting to feeding behaviors (Schivell et al., 1997).

[edit] Locomotion

Figure 3: Melibe escape swimming.

Figure 4: Swim circuit for lateral flexion swimming in Melibe. Si1=swim interneuron 1; Si2=swim interneuron 2. Black circles indicate inhibitory synaptic connections. Solid lines indicate a monosynaptic connection and dotted lines indicate synaptic connections which may be monosynaptic or polysynaptic. Resister symbols indicate electrical coupling.

As with other nudibranchs, the primary form of locomotion for Melibe is crawling, which consists of both ciliary locomotion on a mucus trail and muscular contractions of the foot. In addition, Melibe can also “swim” by alternately flexing its body from side-to-side (Agersborg, 1919, 1921; Hurst, 1968; Watson et al., 2001; Lawrence and Watson, 2002). It is not clear why or how often Melibe chooses to swim, although it has been hypothesized that it is a means of population dispersal (Mills, 1994) and there is strong evidence supporting its role as an escape mechanism from predators. Swimming is somewhat directional in this animal and therefore may potentially be a way to move from one feeding area or eelgrass blade to another (Lawrence and Watson, 2002).

The central pattern generator responsible for rhythmic swimming consists of at least two types of bilaterally symmetric interneurons, swim interneuron 1 (Si1) and swim interneuron 2 (Si2) (Thompson and Watson, 2005). Si1 is located in the cerebral ganglion and Si2 is located in the pedal ganglion. Ipsilateral swim interneurons are electrically coupled and work together, whereas contralateral swim interneurons are inhibitory, creating a classic half-center oscillator. Efferent swim neurons are located in the pedal ganglia and control the rhythmic contractions of the body wall (Watson et al., 2002).

[edit] Modulation of swimming

The brain of Melibe contains two nitric oxide-producing neurons (Newcomb and Watson, 2001). Bath application of nitric oxide in both semi-intact and isolated brain preparations inhibits swimming, most likely via a cGMP-dependent mechanism (Newcomb and Watson, 2002). Additional studies have confirmed that the two nitrergic neurons in the Melibe brain also inhibit swimming and do so via nitric oxide (Newcomb, 2001).

In contrast to nitric oxide, bath application of serotonin stimulates swimming in quiescent isolated brain preparations of Melibe (Newcomb and Katz, 2006). Serotonin can also increase the frequency of an ongoing swim motor pattern. Additional studies have identified a set of serotonergic neurons in the cerebral ganglion of Melibe, the CeSP-A neurons (Newcomb and Katz, 2007), which also elicit swimming via release of serotonin (Newcomb and Katz, 2006).

[edit] Patterns of locomotor activity

Melibe exhibits a nocturnal pattern of locomotor activity, as determined by monitoring the amount of crawling and swimming in normal light/dark cycles (Watson et al., 2001; Newcomb et al., 2004). This nocturnal pattern of activity continues for several days of constant darkness, indicating that there may be an endogenous circadian component to this locomotor pattern of activity. In constant light, locomotion is inhibited throughout a 24-hour period. Because the eyes of Melibe are located almost directly on the brain and are functional in isolated brain preparations, the effect of light on fictive locomotion can be studied. Similar to behavioral studies, light inhibits swim motor pattern activity in isolated brain preparations and this inhibition is mediated by the eyes (Newcomb et al., 2004).

[edit] Links to additional information

[edit] References

Agersborg HPK (1919) Notes on Melibe leonina (Gould). Publ Puget Sound Biol Sta 2: 269-277, pls. 49-50.
Agersborg HPK (1921) Contribution to the knowledge of the Nudibranchiate Mollusc, Melibe leonina (Gould). Amer Nat 55: 223-253.
Ajeska RA, Nybakken J (1976) Contributions to the biology of Melibe leonina (Gould, 1852). Veliger 19: 19-26.
Ayer SW, Andersen RJ (1983) Degraded monoterpenes from the opisthobranch mollusc Melibe leonina. Experientia 39: 255-256.
Baltzley MJ (2006) Evolution and neurobiology of the neural circuitry underlying crawling in nudibranch molluscs. Ph.D. Dissertation. University of North Carolina, Chapel Hill, NC.
Barsby T, Linington RG, Andersen RJ (2002) De novo terpenoid biosynthesis by the dendronotid nudibranch Melibe leonina. Chemoecol 12: 199-202.
Bickell LR, Kempf SC (1983) Larval and metamorphic morphogenesis in the nudibranch Melibe leonina (Mollusca: Opisthobranchia). Biol Bull 165: 119-138.
Chase R (2002) Behavior and its neural control in gastropod molluscs. Oxford University Press, Inc. New York.
Gould AA (1852) United States exploring expedition during the years 1838, 1839, 1840, 1841, 1842 under the command of Charles Wilkes. USN 12: Mollusca shells. 1-510.
Hurst A (1968) The feeding mechanism and behaviour of the opisthobranch Melibe leonina. Symp Zool Soc Lond 22: 151-166.
Lawrence KA, Watson WH, III (2002) Swimming behavior of the nudibranch Melibe leonina. Biol Bull 203: 144-151.
MacFarland F (1966) Studies of opisthobranchiate mollusks of the Pacific coast of North America. Mem Calif Acad Sci 6: 1-546.
McDonald G (1983) A review of the nudibranchs of the California coast. Malacologia 24: 114-276.
Mills CE (1994) Seasonal swimming of sexually mature benthic opisthobranch molluscs (Melibe leonina and Gastropteron pacificum) may augment population dispersal. Reproduction and development of marine invertebrates. Eds: Wilson SA, Stricker SA, Shinn GL. Johns Hopkins Press. Baltimore. 313-319.
Newcomb JM (2001) Nitric oxide in the central nervous system of the gastropod Melibe leonina and its role in modulation of swimming. MS Thesis: University of New Hampshire. Durham, NH.
Newcomb JM, Katz PS (2006) Phylogenetic reconfiguration of neural circuits underlying locomotion in nudibranch molluscs. Program No 350.2. Society for Neuroscience, Washington.
Newcomb JM, Katz PS (2007) Homologues of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors. J Comp Physiol A 193: 425-443.
Newcomb JM, Watson WH, III (2001) Identifiable nitrergic neurons in the central nervous system of the nudibranch Melibe leonina localized with NADPH-diaphorase histochemistry and nitric oxide synthase immunoreactivity. J Comp Neurol 437: 70-78.
Newcomb JM, Watson WH, III (2002) Modulation of swimming in the gastropod Melibe leonina by nitric oxide. J Exp Biol 205: 397-403.
Newcomb JM, Lawrence KA, Watson WH, III (2004) The influence of light on locomotion in the gastropod Melibe leonina. Mar Fresh Behav Physiol 37: 253-269.
Page LR (1993) Development of behaviour in juveniles of Melibe leonina (Gastropoda; Nudibranchia). Mar Behav Physiol 22: 141-161.
Schivell AE, Wang SS-H, Thompson SH (1997) Behavioral modes arise from a random process in the nudibranch Melibe. Biol Bull 192: 418-425.
Thompson SH, Watson WH, III (2005) Central pattern generator for swimming in Melibe. J Exp Biol 208: 1347-1361.
Trimarchi J, Watson WH, III (1992) The role of the Melibe buccal ganglia in feeding behavior and its modification by prey density. Mar Behav Physiol 19: 195-209.
Watson WH, III, Trimarchi J (1992) A Quantitative description of Melibe feeding behavior and its modification by prey density. Mar Behav Physiol 19: 183-194.
Watson WH, III, Chester CM (1993) The influence of olfactory and tactile stimuli on the feeding behavior of Melibe leonina (Gould, 1852) (Opisthobranchia: Dendronotacea). Veliger 36: 311-316.
Watson WH, III, Lawrence KA, Newcomb JM (2001) Neuroethology of Melibe leonina swimming behavior. Amer Zool 41: 1026-1035.
Watson WH, III, Newcomb JM, Thompson S (2002) Neural correlates of swimming behavior in Melibe leonina. Biol Bull 203: 152-160.

Internal references

Valentino Braitenberg (2007) Brain. Scholarpedia, 2(11):2918.

Peter Jonas and Gyorgy Buzsaki (2007) Neural inhibition. Scholarpedia, 2(9):3286.

Paul S. Katz (2007), Tritonia. Scholarpedia, 2(6):3504.