Changes Occur in the Central Nervous System of the Nudibranch <i>Berghia verrucicornis</i> (Mollusca, Opisthobranchia) During Metamorphosis

Carroll, David J.; Kempf, Stephen C.

doi:10.2307/1542054

Cited by 13 publications

(13 citation statements)

References 33 publications

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“…As in other nudibranchs described, the CNS of Aeolidiella stephanieae becomes more concentrated during metamorphosis [51,95,100-103]. In Berghia verrucicornis the pleural and cerebral ganglia fuse together to cerebropleural ganglia, the visceral ganglion fuses with the left cerebropleural ganglion to become the pleurovisceral loop, and all the connectives become shorter [95].…”

Section: Discussionmentioning

confidence: 96%

Neuromuscular development of Aeolidiella stephanieae Valdez, 2005 (Mollusca, Gastropoda, Nudibranchia)

Kristof

Klussmann‐Kolb

2010

Front Zool

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BackgroundStudies on the development of the nervous system and the musculature of invertebrates have become more sophisticated and numerous within the last decade and have proven to provide new insights into the evolutionary history of organisms. In order to provide new morphogenetic data on opisthobranch gastropods we investigated the neuromuscular development in the nudibranch Aeolidiella stephanieae Valdéz, 2005 using immunocytochemistry as well as F-actin labelling in conjunction with confocal laser scanning microscopy (cLSM).ResultsThe ontogenetic development of Aeolidiella stephanieae can be subdivided into 8 stages, each recognisable by characteristic morphological and behavioural features as well as specific characters of the nervous system and the muscular system, respectively. The larval nervous system of A. stephanieae includes an apical organ, developing central ganglia, and peripheral neurons associated with the velum, foot and posterior, visceral part of the larva. The first serotonergic and FMRFamidergic neural structures appear in the apical organ that exhibits an array of three sensory, flask-shaped and two non-sensory, round neurons, which altogether disappear prior to metamorphosis. The postmetamorphic central nervous system (CNS) becomes concentrated, and the rhinophoral ganglia develop together with the anlage of the future rhinophores whereas oral tentacle ganglia are not found. The myogenesis in A. stephanieae begins with the larval retractor muscle followed by the accessory larval retractor muscle, the velar or prototroch muscles and the pedal retractors that all together degenerate during metamorphosis, and the adult muscle complex forms de novo.ConclusionsAeolidiella stephanieae comprises features of the larval and postmetamorphic nervous as well as muscular system that represent the ground plan of the Mollusca or even the Trochozoa (e. g. presence of the prototrochal or velar muscle ring). On the one hand, A. stephanieae shows some features shared by all nudibranchs like the postmetamorphic condensation of the CNS, the possession of rhinophoral ganglia and the lack of oral tentacle ganglia as well as the de novo formation of the adult muscle complex. On the other hand, the structure and arrangement of the serotonergic apical organ is similar to other caenogastropod and opisthobranch gastropods supporting their sister group relationship.

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Section: Discussionmentioning

confidence: 96%

Neuromuscular development of Aeolidiella stephanieae Valdez, 2005 (Mollusca, Gastropoda, Nudibranchia)

Kristof

Klussmann‐Kolb

2010

Front Zool

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“…The developmental sequence of neurogenesis in the anaspidean A. californica stands in striking contrast to that of nudibranch gastropods in which the genesis of rhinophores and the rhn preceeds the development of the labial tentacles and cln (Chia and Koss 1982;Carroll and Kempf 1994). Although some authorities consider the rhinophores of A. californica to be homologous to the rhinophores of nudibranchs and the cephalic tentacles of prosobranch gastropods, they develop in the late juvenile phase, whereas both of the last-mentioned structures appear during the veliger phase, indicating strong ontogenetic heterochrony of these sensory organs in the various gastropod taxa.…”

Section: Neuronal Organization Of Csos In Opisthobranch Taxamentioning

confidence: 94%

“…Although some authorities consider the rhinophores of A. californica to be homologous to the rhinophores of nudibranchs and the cephalic tentacles of prosobranch gastropods, they develop in the late juvenile phase, whereas both of the last-mentioned structures appear during the veliger phase, indicating strong ontogenetic heterochrony of these sensory organs in the various gastropod taxa. In the nudibranch Berghia verrucicornis, all major nerves other than the "rhinophoral nerve" develop significantly later after metamorphosis (Carroll and Kempf 1994). Both P. sibogae ) and A. californica exhibit a rhinophoral ganglion, whereas a labial tentacle ganglion only occurs in the latter species.…”

Section: Neuronal Organization Of Csos In Opisthobranch Taxamentioning

confidence: 99%

Neurogenesis of cephalic sensory organs of Aplysia californica

2007

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The opisthobranch gastropod Aplysia californica serves as a model organism in experimental neurobiology because of its simple and well-known nervous system. However, its nervous periphery has been less intensely studied. We have reconstructed the ontogeny of the cephalic sensory organs (labial tentacles, rhinophores, and lip) of planktonic, metamorphic, and juvenile developmental stages. FMRFamide and serotonergic expression patterns have been examined by immunocytochemistry in conjunction with epifluorescence and confocal laser scanning microscopy. We have also applied scanning electron microscopy to analyze the ciliary distribution of these sensory epithelia. Labial tentacles and the lip develop during metamorphosis, whereas rhinophores appear significantly later, in stage 10 juveniles. Our study has revealed immunoreactivity against FMRFamides and serotonin in all major nerves. The common labial nerve develops first, followed by the labial tentacle base nerve, oral nerve, and rhinophoral nerve. We have also identified previously undescribed neuronal pathways and other FMRFamide-like-immunoreactive neuronal elements, such as peripheral ganglia and glomerulus-like structures, and two groups of conspicuous transient FMRFamide-like cell somata. We have further found two distinct populations of FMRFamide-positive cell somata located both subepidermally and in the inner regions of the cephalic sensory organs in juveniles. The latter population partly consists of sensory cells, suggesting an involvement of FMRFamide-like peptides in the modulation of peripheral sensory processes. This study is the first concerning the neurogenesis of cephalic sensory organs in A. californica and may serve as a basis for future studies of neuronal elements in gastropod molluscs.

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“…A number of structures critical to the metamorphic event or subsequent juvenile and adult life develop as the larva grows and attains competence; these include the radula, most ganglia of the adult nervous system, the propodium, and the primary cerata in some species (Thompson, 1958(Thompson, , 1962Bonar and Hadfield, 1974;Kempf and Willows, 1977;Bickell and Kempf, 1983;Carroll and Kempf, 1994). Some such structures (e.g., eyespots, digestive organs, propodium, certain nervous system components) serve multiple roles concerned with larval growth, settlement and metamorphosis, and juvenile and adult life (see Table 3).…”

Section: If This Is Correct the Organization Of The Pores Of The Amentioning

confidence: 99%

Anti-Tubulin Labeling Reveals Ampullary Neuron Ciliary Bundles in Opisthobranch Larvae and a New Putative Neural Structure Associated With the Apical Ganglion

Kempf

Page

2005

The Biological Bulletin

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This investigation examines tubulin labeling associated with the apical ganglion in a variety of planktotrophic and lecithotrophic opisthobranch larvae. Emphasis is on the ampullary neurons, in which ciliary bundles within the ampulla are strongly labeled. The larvae of all but one species have five ampullary neurons and their associated ciliary bundles. The anaspid Phyllaplysia taylori, a species with direct development and an encapsulated veliger stage, has only four ampullary neurons. The cilia-containing ampulla extends to the pretrochal surface via a long, narrow canal that opens to the external environment through a very small pore (0.1 microm diameter). Cilia within the canal were never observed to project beyond the opening of the apical pore. The ampullary canals extend toward and are grouped with the ciliary tuft cells and remain in this location as planktotrophic larvae feed and grow. If, as has been reported, the ciliary tuft is motile, the pores may be continually bathed in fresh seawater. Such an arrangement would increase sensitivity to environmental chemical stimuli if the suggested chemosensory function of these neurons is correct. In general, ciliary bundles of newly hatched veligers are smaller in planktotrophic larvae than in lecithotrophic larvae. In planktotrophic larvae of Melibe leonina, the ciliary bundles increase in length and width as the veligers feed and grow. This may be related to an increase in sensitivity for whatever sensory function these neurons fulfill. An unexpected tubulin-labeled structure, tentatively called the apical nerve, was also found to be associated with the apical ganglion. This putative nerve extends from the region of the visceral organs to a position either within or adjacent to the apical ganglion. One function of the apical nerve might be to convey the stimulus resulting from metamorphic induction to the visceral organs.

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Changes Occur in the Central Nervous System of the Nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia) During Metamorphosis

Cited by 13 publications

References 33 publications

Neuromuscular development of Aeolidiella stephanieae Valdez, 2005 (Mollusca, Gastropoda, Nudibranchia)

Neuromuscular development of Aeolidiella stephanieae Valdez, 2005 (Mollusca, Gastropoda, Nudibranchia)

Neurogenesis of cephalic sensory organs of Aplysia californica

Anti-Tubulin Labeling Reveals Ampullary Neuron Ciliary Bundles in Opisthobranch Larvae and a New Putative Neural Structure Associated With the Apical Ganglion

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