Skip to main content
SpringerLink
Log in

Serotonergic neurotransmission in the bivalve Venus verrucosa (Veneridae): a neurochemical and immunohistochemical study of the visceral ganglion and gonads

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Serotonin (5-hydroxytryptamine, 5-HT) is well known to be involved in many aspects of bivalve biology, especially in the control of reproductive function. In this work, a neurochemical and immunohistochemical study was carried out in the visceral ganglion of Venus verrucosa (Bivalvia: Veneridae), with the aim of elucidating the features of 5-HT neurotransmission and its influence on gamete emission in this poorly investigated bivalve species. 5-HT release was characterized: tritium efflux, evoked from the isolated [3H]5-HT-preincubated visceral ganglion by high potassium concentrations, was shown to possess the characteristics of neurotransmitter release (sodium and calcium dependence, auto-feedback regulation). Serotonergic cell bodies and axonal tracts were labeled by immunohistochemistry, confirming that the released 5-HT originates in a pool of neurons in the visceral ganglion. The presence and distribution of serotonin were immunohistochemically checked in the gonads as well. A plexus of immunopositive fibers was observed in the gonadic tissue of both sexes, specifically located in the follicle walls, and this innervation appeared to come from branching of the cerebro-visceral connectives, whereas no peripheral serotonergic neurons were identified. The immunohistochemical data were supported by light and electron microscope observations. Exogenous 5-HT was applied to V. verrucosa specimens by intramuscular injection; it induced spawning in both sexes, and the response rate was significantly higher in males than in females, as previously observed in some other species of gonochoric bivalves. These findings suggest the existence of a serotonergic neurotransmission in V. verrucosa, possibly regulating the reproductive process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A, B
Fig. 2A–F
Fig. 3A–C

Similar content being viewed by others

References

  • Arneri E, Giannetti G, Antolini B (1998) Age determination and growth of Venus verrucosa L. (Bivalvia: Veneridae) in the southern Adriatic and the Aegean Sea. Fish Res (Amst) 38:193–198

    Article  Google Scholar 

  • Arranz B, Marcusson J (1994) [3H]paroxetine and [3H]citalopram as markers of the human brain 5-HT uptake site: a comparison study. J Neural Transm Gen Sect 97:27–40

    CAS  PubMed  Google Scholar 

  • Barbin L, Sbrenna G, Micciarelli-Sbrenna A (2001) Annual gonad cycle in Venus verrucosa (Bivalvia, Veneridae): an ultrustructural study of oogenesis and spermatogenesis. Biol Mar Mediterr 8:809–811

    Google Scholar 

  • Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083–1152

    Article  CAS  PubMed  Google Scholar 

  • Beani L, Bianchi C, Siniscalchi A, Sivilotti L, Tanganelli S, Veratti E (1984) Different approaches to study acetylcholine release: endogenous ACh versus tritium efflux. Naunyn-Schmiedebergs Arch Pharmacol 328:119–126

    Google Scholar 

  • Breese WP, Robinson A (1981) Razor clam, Siliqua patula (Dixon): gonadal development, induced spawning and larval rearing. Aquaculture 22:27–33

    Article  Google Scholar 

  • Campioni D, Sbrenna G (1995) Induzione dello spawning in Tapes philippinarum (Bivalvia: Veneroida) e Scapharca inaequivalvis (Bivalvia: Arcidae) mediante somministrazione di serotonina (5-idrossitriptamina). Biol Mar Mediterr 2:307–309

    Google Scholar 

  • Cavallini S, Barbin L, Sbrenna G, Turolla E, Siniscalchi A (2002) Caratterizzazione della liberazione di serotonina dal ganglio viscerale di Venus verrucosa. Biol Mar Mediterr 9:859–862

    Google Scholar 

  • Cerrito F, Raiteri M (1979) Serotonin release is modulated by presynaptic autoreceptors. Eur J Pharmacol 57:427–430

    Article  CAS  PubMed  Google Scholar 

  • Costello TJ, Hudson JH, Dupuy JR, Rivkin S (1973) Larval culture of the calico scallop, Argopecten gibbus. Proc Natl Shellfish Assoc 63:72–77

    Google Scholar 

  • Deguchi R, Osanai K (1995) Serotonin-induced meiosis reinitiation from the first prophase and from the first metaphase in oocytes of the marine bivalve Hiatella flaccida: respective changes in intracellular Ca2+ and pH. Dev Biol 171:483–496

    Article  CAS  PubMed  Google Scholar 

  • Durocher Y, Guerrier P (1996) Activation of an 85 kDa ribosomal S6 kinase during serotonin-induced oocyte maturation. Int J Dev Biol 40:557–566

    CAS  PubMed  Google Scholar 

  • Fong PP, Kyozuka K, Abdelghani H, Hardege JD, Ram JL (1994) In vivo and in vitro induction of germinal vesicle breakdown in a freshwater bivalve, the zebra mussel Dreissena polymorpha (Pallas). J Exp Zool 269:467–474

    CAS  PubMed  Google Scholar 

  • Fu XW, Nurse CA, Wong V, Cutz E (2002) Hypoxia-induced secretion of serotonin from intact pulmonary neuroepithelial bodies in neonatal rabbit. J Physiol 539:503–510

    Article  CAS  PubMed  Google Scholar 

  • Gebauer A, Merger M, Kilbinger H (1993) Modulation by 5-HT3 and 5-HT4 receptors of the release of 5-hydroxytryptamine from the guinea-pig small intestine. Naunyn-Schmiedebergs Arch Pharmacol 347:137–140

    Google Scholar 

  • Gibbons MC, Castagna M (1984) Serotonin as an inducer of spawning in six bivalve species. Aquaculture 40:189–191

    Article  CAS  Google Scholar 

  • Gibbons MC, Castagna M (1985) Response of the hard clam Mercenaria mercenaria (Linné) to induction of spawning by serotonin. J Shellfish Res 5:65–67

    Google Scholar 

  • Gobet I, Durocher Y, Leclerc C, Moreau M, Guerrier P (1994) Reception and transduction of the serotonin signal responsible for meiosis reinitiation in oocytes of the Japanese clam Ruditapes philippinarum. Dev Biol 164:540–549

    Article  CAS  PubMed  Google Scholar 

  • Goethert M, Schlicker DK (1991) Regulation of serotonin release in the central nervous system by presynaptic heteroreceptors. In: Feigenbaum J, Hanani L (eds) Presynaptic regulation of neurotransmitter release: a handbook. Freund, Tel Aviv, pp 845–876

  • Hervas I, Queiroz CM, Adell A, Artigas F (2000) Role of uptake inhibition and autoreceptor activation in the control of 5-HT release in the frontal cortex and dorsal hippocampus of the rat. Br J Pharmacol 130:160–166

    CAS  PubMed  Google Scholar 

  • Hirai S, Kishimoto T, Kadam AL, Kanatani H, Koide SS (1988) Induction of spawning and oocyte maturation by 5-hydroxytryptamine in the surf clam. J Exp Zool 245:318–321

    CAS  Google Scholar 

  • Kent GN, Maguire GB, John M, Cropp M, Frankish K (1998) Broodstock conditioning, spawning induction, and larval rearing of the stepped venerid, Katelysia scalarina (Lamarck, 1818). J Shellfish Res 17:1065–1070

    Google Scholar 

  • Kent GN, Maguire GB, Duthie I, Pugh R (1999) Spawning settlement, and growth of the New Zealand venerid Ruditapes largillierti (Philippi, 1849) in culture. NZ J Mar Freshw Res 33:55–62

    Google Scholar 

  • Kreiling JA, Jessen-Eller K, Miller J, Seegal RF, Reinisch CL (2001) Early development of the serotonergic and dopaminergic nervous system in Spisula solidissima (surf clam) larvae. Comp Biochem Physiol A Physiol 130:341–351

    Article  CAS  Google Scholar 

  • Kuwasawa K, Hill R (1997) Evidence for cholinergic inhibitory and serotonergic excitatory neuromuscular transmission in the heart of the bivalve Mercenaria mercenaria. J Exp Biol 200:2123–2135

    CAS  PubMed  Google Scholar 

  • Marano G, Casavola N, Saracino C, Rizzi E (1982) Riproduzione e crescita di Chamelea gallina (L.) e Venus verrucosa (L.) (Bivalvia: Veneridae) nel basso Adriatico. Mem Biol Mar Oceanogr 12:93–110

    Google Scholar 

  • Martínez G, Rivera A (1994) Role of monoamines in the reproductive process of Argopecten purpuratus. Invertebr Reprod Dev 25:167–174

    Google Scholar 

  • Martínez G, Saleh F, Mettifogo L, Campos E, Inestrosa N (1996) Monoamines and the release of gametes by the scallop Argopecten purpuratus. J Exp Zool 274:365–372

    Article  Google Scholar 

  • Martínez G, Mettifogo L, Lenoir R, Olivares A (2000) Prostaglandins and reproduction of the scallop Argopecten purpuratus. II. relationship with gamete release. J Exp Zool 287:86–91

    Article  PubMed  Google Scholar 

  • Masseau I, Bannon P, Anctil M, Dube F (2002) Localization and quantification of gonad serotonin during gametogenesis of the surf clam, Spisula solidissima. Biol Bull (Woods Hole) 202:23–33

    Google Scholar 

  • Matsutani T (1990) Endogenous factors controlling spawning in marine bivalves. In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction, vol 5. Elsevier, Amsterdam, pp 231–237

  • Matsutani T, Nomura T (1986) Serotonin-like immunoreactivity in the central nervous system and gonad of the scallop, Patinopecten yessoensis. Cell Tissue Res 244:515–517

    Google Scholar 

  • Matsutani T, Nomura T (1987) In vitro effects of serotonin and prostaglandins on release of eggs from the ovary of the scallop Patinopecten yessoensis. Gen Comp Endocr 67:111–118

    CAS  PubMed  Google Scholar 

  • Morse DE, Duncan H, Hooker N, Morse A (1977) Hydrogen peroxide induces spawning in molluscs, with activation of prostaglandin endoperoxide synthetase. Science 196:298–300

    CAS  PubMed  Google Scholar 

  • Paulet Y-M, Donval A, Bekhadra F (1993) Monoamines and reproduction in Pecten maximus, a preliminary approach. Invertebr Reprod Dev 23:89–94

    CAS  Google Scholar 

  • Ram JL, Crawford GW, Walker JU, Mojares JJ, Patel N, Fong PP, Kyozuka K (1993) Spawning in the zebra mussel (Dreissena polymorpha): activation by internal or external application of serotonin. J Exp Zool 265:587–598

    CAS  PubMed  Google Scholar 

  • Ram JL, Moore D, Putchakayala S, Paredes AA, Ma D, Croll RP (1999) Serotonergic responses of the siphons and adjacent mantle tissue of the zebra mussel, Dreissena polymorpha. Comp Biochem Physiol C Comp Pharmacol 124:211–220

    Article  CAS  Google Scholar 

  • Sbrenna G, Bizzaro D, Sonetti D, Barbin L, Borasio PG (2001) Studio delle caratteristiche ultrastrutturali, istochimiche ed immunocitochimiche del sistema nervoso di Venus verrucosa. Biol Mar Mediterr 8:41–45

    Google Scholar 

  • Siniscalchi A, Rodi D, Cavallini S, Marino S, Beani L, Bianchi C (2001) Effects of cholecystokinin tetrapeptide (CCK4) and anxiolytic drugs on the electrically evoked [3H]5-hydroxytryptamine outflow from rat cortical slices. Brain Res 922:104–111

    Article  CAS  PubMed  Google Scholar 

  • Sonetti D, Mola L, Casares F, Bianchi E, Guarino M, Stefano GB (1999) Endogenous morphine levels increase in molluscan neural and immune tissues after physical trauma. Brain Res 835:137–147

    Article  CAS  PubMed  Google Scholar 

  • Stefano GB, Brogan JJ, Aiello E, Hiripi L (1980a) Lanthanum blockade of serotonin release from the branchial nerve of the mussel Mytilus edulis. J Exp Zool 214:21–26

    CAS  PubMed  Google Scholar 

  • Stefano GB, Catapane EJ, Aiello E, Hiripi L (1980b) The calcium-dependent neuronal release of serotonin and its antagonism by lithium. J Neurobiol 11:179–191

    CAS  PubMed  Google Scholar 

  • Stephen D, Shetty HPC (1981) Induction of spawning in 4 species of bivalves of the Indian coastal waters. Aquaculture 25:153–159

    Article  Google Scholar 

  • Stephens RE, Prior G (1992) Dynein from serotonin-activated cilia and flagella: extraction characteristics and distinct sites for cAMP-dependent protein phosphorylation. J Cell Sci 103:999–1012

    CAS  PubMed  Google Scholar 

  • Suter HA, Collard KJ (1983) The regulation of 5-hydroxytryptamine release from superfused synaptosomes by 5-hydroxytryptamine and its immediate precursors. Neurochem Res 8:723–730

    CAS  PubMed  Google Scholar 

  • Tierney AJ (2001) Structure and function of invertebrate 5-HT receptors: a review. Comp Biochem Physiol A Physiol 128:791–804

    Article  CAS  Google Scholar 

  • Turolla E, Castaldelli G, Barbin L, Dezfuli SB, Rossi R (2004) Primo ottenimento di spat di tartufo di mare (Venus verrucosa) mediante tecniche di riproduzione controllata. Biol Mar Mediterr (in press)

  • Vélez A, Alifa A, Azuaje O (1990) Induction of spawning by temperature and serotonin in the hermaphroditic tropical scallop, Pecten ziczac. Aquaculture 84:307–313

    Article  Google Scholar 

  • Walker RJ (1984) 5-hydroxytryptamine in invertebrates. Comp Biochem Physiol C Comp Pharmacol 79:231–235

    Article  CAS  Google Scholar 

  • Weiger WA (1997) Serotonergic modulation of behaviour: a phylogenetic overview. Biol Rev Camb Philos Soc 72:61–95

    CAS  PubMed  Google Scholar 

  • Welsh J, Moorehead M (1960) The quantitative distribution of serotonin in invertebrates, especially in their nervous system. J Neurochem 6:146–169

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Italian Ministry of Agricultural Policy. Thanks are due to Dr. E.N. Cartoon for the English revision of the manuscript.

Author information

Authors and Affiliations

  1. Department of Clinical and Experimental Medicine, Section of Pharmacology, University of Ferrara, Via Fossato di Mortara 17, 44100, Ferrara, Italy

    A. Siniscalchi & S. Cavallini

  2. Department of Animal Biology, University of Modena and Reggio Emilia, Via Campi 213/d, 41100, Modena, Italy

    D. Sonetti

  3. Department of Biology, University of Ferrara, Via Borsari 46, 44100, Ferrara, Italy

    G. Sbrenna, S. Capuano, L. Barbin & R. Rossi

  4. C.Ri.M. (Centro Ricerche sui Molluschi), University of Ferrara, Via dell’Agricoltura 17, 44020, Goro (Ferrara), Italy

    E. Turolla

Authors
  1. A. Siniscalchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Cavallini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Sonetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. Sbrenna
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Capuano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. L. Barbin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. E. Turolla
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R. Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Siniscalchi.

Additional information

Communicated by R. Cattaneo-Vietti, Genova

Rights and permissions

Reprints and permissions

About this article

Cite this article

Siniscalchi, A., Cavallini, S., Sonetti, D. et al. Serotonergic neurotransmission in the bivalve Venus verrucosa (Veneridae): a neurochemical and immunohistochemical study of the visceral ganglion and gonads. Marine Biology 144, 1205–1212 (2004). https://doi.org/10.1007/s00227-003-1284-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-003-1284-4

Keywords

Search

Navigation