Abstract
Larval development in crabs is characterized by a striking double metamorphosis in the course of which the animals change from a pelagic to a benthic life style. The larval central nervous system has to provide an adequate behavioural repertoire during this transition. Thus, processes of neuronal reorganization and refinement of the early larval nervous system could be expected to occur in the metamorphosing animal. In order to follow identified sets of neurons throughout metamorphosis, whole mount preparations of the brain and ventral nerve cord of laboratory reared spider crab larvae (Hyas araneus) were labelled with an antibody against the neurotransmitter serotonin. The system of serotonin-immunoreactive cell bodies, fibres and neuropils is well-developed in newly hatched larvae. Most immunoreative structures are located in the protocerebrum, with fewer in the suboesophaegeal ganglia, while the thoracic and abdominal ganglia initially comprise only a small number of serotonergic neurons and fibres. However, there are significant alterations in the staining pattern through larval development, some of which are correlated to metamorphic events. Accordingly, new serotonin-immunoreactive cells are added to the early larval set and the system of immunoreactive fibres is refined. These results are compared to the serotonergic innervation in other decapod crustaceans.
Similar content being viewed by others
References
Anger, K. (1983) Moult cycle and morphogenesis inHyas araneus larvae (Decapoda, Majidae), reared in the laboratory.Helgol. Wiss. Meeresunters.,36, 285–302.
Anger, K. and Dawirs, R. R. (1981) Influence of starvation on the larval development of Hyas araneus (Decapoda, Majidae).Helgol. Wiss. Meeresunters,34, 287–311.
Anger, K. and Nair, K. K. C. (1979) Laboratory experiments on the larval development ofHyas araneus (Decapoda, Majidae).Helgol. Wiss. Meeresunters,32, 36–54.
Baker, M. W., Vohra, M. W. and Croll, R. P. (1993) Serotonin depletors, 5,7-dihydroxytryptamine and p-chlorophenylalanine, cause sprouting in the CNS of the adult snail.Brain Res.,623, 311–315.
Barlow, L. A. and Truman, J. W. (1992) Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abalone,Haliotis rufescens.J. Neurobiol.,23, 829–844.
Barthe, J. Y., Bevengut, M. and Clarac, F. (1993)In vitro, proctolin and serotonin induced modulations of the abdominal motor system activities in crayfish.Brain Res.,623, 101–109.
Beltz, B. S. and Kravitz, E. A. (1983) Mapping of serotonin-like immunoreactivity in the lobster nervous system.J. Neurosci.,3, 585–602.
Beltz, B. S. and Kravitz, E. A. (1987) Physiological identification, morphological analysis, and development of identified serotonin-proctolin containing neurons in the lobster ventral nerve cord.J. Neurosci.,7, 533–546.
Beltz, B. S., Pontes, M., Helluy, S. M. and Kravitz, E. A. (1990) Patterns of appearance of serotonin and proctolin immunoreactivity in the developing nervous system of the american lobster.J. Neurobiol.,21, 521–542.
Benton, J., Helluy, S., Huber, R., Ruchhoeft, M. and Beltz, B. S. (1994) Serotonin depletion by 5,7-dihydroxytryptamine alters deutocerebral development in the lobster,Homarus americanus.Soc. Neurosci. Abstr.,20, 775.
Bicker, G. (1994) Serotonin influences neurite morphology of cultured insect neurons. InGöttingen Neurobiology Report 1994, ed. N. Elsner and H. Breer, p. 152. Stuttgart: Thieme.
Bisgrove, B. W. and, Burke, R. D. (1986) Development of serotonergic neurons in embryos of the sea urchin,Strongylocentrotus purpuratus.Dev. Growth Differ.,28, 569–574.
Bisgrove, B. W. and Burke, R. D. (1987) Development of the nervous system of the pluteus larva ofStrongylocentrotus droebachiensis.Cell Tissue Res.,248, 335–343.
Breidbach, O. (1990) Serotonin-immunoreactive brain interneurons persist during metamorphosis of an insect: a developmental study of the brain ofTenebrio molitor L. (Coleoptera).Cell Tissue Res.,259, 345–360.
Budnik, V., Wu, C. F. and White, K. (1989) Altered branching of serotonin-containing neurons inDrosophila mutants unable to synthesize serotonin and dopamine.J. Neurosci.,9, 2866–2877.
Christiansen, M. E. (1973) The complete larval development ofHyas araneus (Linnaeus) andHyas coarctatus (Decapoda, Brachyura, Majidae) reared in the laboratory.Norw. J. Zool.,21, 63–89.
Cooke, I. M. and Goldstone, M. W. (1970) Fluorescence localization of monoamines in crab neurosecretory structures.J. Exp. Biol.,53, 651–668.
Elofsson, R. (1983) 5-HT-like immunoreactivity in the central nervous system of the crayfish,Pacifastus leniusculus.Cell Tissue Res.,232, 221–236.
Falugi, C. and Davoli, C. (1993) Localization of putative biochemical messengers duringEisenia foetida (Annelida, Oligochaeta) development.Tissue Cell,25, 311–323.
Fingerman, M., Nagabhushanam, R., Sarojini, R. and Reddy, P. S. (1994) Biogenic amines in crustaceans: identification, localization, and roles.J. Crust. Biol.,14, 413–437.
Glanzman, D. L. and Krasne, F. B. (1986) 5,7-Dihydroxytryptamine lesions of crayfish serotonin-containing neurons: effect on the lateral giant escape reaction.J. Neurosci.,6, 1560–1569.
Goldberg, J. I. and Kater, S. B. (1989) Expression and function of the neurotransmitter serotonin during development of theHelisoma nervous system.Dev. Biol.,131, 483–495.
Goldstone, M. W. and Cooke, I. M. (1971) Histochemical localization of monamines in the crab central nervous system.Z. Zellforsch.,116, 7–19.
Granger, N. A., Homberg, U., Henderson, P., Towle, A. and Lauder, J. M. (1989) Serotonin-immunoreactive neurons in the brain ofManduca sexta during larval development and larval-pupal metamorphosis.Int. J. Dev. Neurosci.,7, 55–72.
Harris, W. A. (1990) Neurometamorphosis.J. Neurobiol.,21, 953–957.
Harris-Warrick, R. M., Flamm, R. E., Johnson, B. R. and Katz, P. S. (1989) Modulation of neural circuits in Crustacea.Amer. Zool.,29, 1305–1320.
Harris-Warrick, R. M. and Kravitz, E. A. (1984) Cellular mechanisms for modulation of posture by octopamine and serotonin in the lobster.J. Neurosci.,4, 1976–1993.
Harzsch, S. and Dawirs, R. R. (1993) On the morphology of the central nervous system in larval stages ofCarcinus maenas L. (Decapoda, Brachyura).Helgol. Meeresunters.,47, 61–79.
Harzsch, S. and Dawirs, R. R. (1994) Neurogenesis in larval stages of the spider crabHyas araneus (Decapoda, Brachyura): proliferation of neuroblasts in the ventral nerve cord.Roux's Arch. Dev. Biol.,204, 93–100.
Haydon, P. G., McCobb, D. P. and Kater, S. B. (1984) Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons.Science,226, 561–564.
Hay-Schmidt, A. (1990) Catecholamine-containing, serotonin-like, and FMRFamide-like immunoreactive neurons and processes in the nervous system of the early actinotroch larva ofPhoronis vancouverensis (Phoronida): distribution and development.Can. J. Zool.,68, 1525–1536.
Hay-Schmidt, A. (1992) Ultrastructure and immunocytochemistry of the nervous system of the larvae ofLingula anatina andGlottida sp. (Brachiopoda).Zoomorphol.,112, 189–205.
Helluy, S., Sandeman, R., Beltz, B. and Sandeman, D. (1993) Comparative brain ontogeny of the crayfish and clawed lobster: implications of direct and larval development.J. Comp. Neurol.,335, 343–354.
Helluy, S. M., Ruchhoeft, M. L. and Beltz, B. S. (1995) Development of the olfactory and accessory lobes in the American lobster: an allometric analysis and its implications for the deutocerebral structure of decapods.J. Comp. Neurol., in press.
Johansson, K. U. I. (1991) Identification of different types of serotonin-like immunoreactive olfactory interneurons in four infraorders of decapod crustaceans.Cell Tissue Res.,264, 357–362.
Johnson, B. R., Peck, J. H. and Harris-Warrick, R. M. (1993) Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion.J. Comp. Physiol. A,172, 715–732.
Katz, P. S. and Eigg, M. H. and Harris-Warrick, R. M. (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells.J. Neurophysiol.,62, 558–570.
Katz, P. S. and Harris-Warrick, R. M. (1990) Neuromodulation of the crab pyloric central pattern generator by serotonergic/cholinergic proprioceptive afferents.J. Neurosci.,10, 1495–1512.
Lipton, S. A. and Kater, S. B. (1989) Neurotransmitter regulation of neuronal outgrowth, plasticity and survival.Trends Neurosci.,12, 265–270.
Livingstone, M. S., Harris-Warrick, R. M. and Kravitz, E. A. (1980) Serotonin and octopamine produce opposite postures in lobsters.Science,208, 76–79.
Livingstone, M. S., Schaeffer, S. F. and Kravitz, E. A. (1981) Biochemistry and ultrastructure of serotonergic nerve endings in the lobster: serotonin and octopamine are contained in different nerve endings.J. Neurobiol.,12, 27–54.
Mayford, M., Barzilai, A., Keller, F., Schacher, S. and Kandel, E. R. (1992) Modulation of NCAM-related adhesion molecule with long-term synaptic plasticity inAplysia.Science,256, 638–644.
Maynard, D. M. (1961) Thoracic neurosecretory structures in Brachyura. II. Secretory neurons.Gen. Comp. Endocrinol.,1, 237–263.
McCobb, D. P., Cohan, C. S., Connor, J. A. and Kater, S. B. (1988) Interactive effects of serotonin and acetylcholine on neurite elongation.Neuron,1, 377–385.
Mellon, DeF. and Alones, V. (1993) Cellular organization and growth-related plasticity of the crayfish olfactory midbrain.Microsc. Res. Tech.,24, 231–259.
Meyrand, P., Weimann, J. M. and Marder, E. (1992) Multiple axonal spike initiation zone in a motor neuron: serotonin activation.J. Neurosci.,12, 2803–2812.
Moss, C., Burke, R. D. and Thorndyke, M. C. (1994) Immunocytochemical localization of the neuropeptide S1 and serotonin in larvae of the starfishPisaster orchraceus andAsterias rubens.J. Mar. Biol. Ass. UK,74, 61–71.
Murrain, M., Murphy, A. D., Mills, L. R. and Kater, S. B. (1990) Neuron-specific modulation by serotonin of regenerative outgrowth and intracellular calcium within the CNS ofHelisoma trivolvis.J. Neurobioi,21, 611–618.
Nakajima, Y., Burke, R. D. and Noda, Y. (1993) The structure and development of the apical ganglion in the sea urchin pluteus larvae ofStrongylocentrotus droebachiensis andMespilia globulus.Dev. Growth Differ.,35, 531–538.
NÄssel, D. R. (1988) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects.Prog. Neurobiol.,30, 1–85.
Pasztor, V. M. and Golas, L. B. (1993) The modulatory effects of serotonin, neuropeptide F1 and proctolin on the receptor muscles of the lobster abdominal stretch receptor and their exoskeletal muscle homologues.J. Exp. Biol.,174, 363–374.
Peter, N., Aronoff, B., Wu, F. and Schacher, S. (1994) Decrease in growth cone-neurite fascilitation by sensory or motor cells in vitro accompanies downregulation ofAplysia cell adhesion molecules by neurotransmitters.J. Neurosci.,14, 1413–1421.
Real, D. and Czternasty, G. (1990) Mapping of serotonin-like immunoreactivity in the ventral nerve cord of crayfish.Brain Res.,521, 203–212.
Rossi-Durand, C. (1993) Peripheral proprioceptive modulation in crayfish walking leg by serotonin.Brain Res.,632, 1–15.
Rudolph, P. H. and Spaziani, E. (1990) Distribution of serotonergic neurons in the eyestalk and brain of the crab,Cancer antennarius.Comp. Biochem. Physiol.,97C, 241–245.
Sandeman, D. C. and Sandeman, R. E. (1994) Electrical responses and synaptic connections of giant serotonin-immunoreactive neurons in crayfish olfactory and accessory lobes.J. Comp. Neurol.,341, 130–144.
Sandeman, D. C., Sandeman, R. E. and Aitken, A. R. (1988) Atlas of serotonin-containing neurons in the optic lobes and brain of the crayfish,Cherax destructor.J. Comp. Neurol.,269, 465–478.
Sandeman, D. C., Sandeman, R. E., Derby, C. and Schmidt, M. (1992) Morphology of the brain of crayfish, crabs and spiny lobsters: a common nomenclature for homologous structures.Biol. Bull.,183, 304–326.
Sandeman, D. C., Scholtz, G., and Sandeman, R. E. (1993) Brain evolution in decapod Crustacea.J. Exp. Zool.,265, 112–133.
Sandeman, R. E. and Sandeman DC (1987) Serotonin-like immunoreactivity of giant olfactory interneurons in the crayfish brain.Brain Res.,403, 371–374.
Scholtz, G. (1992) Cell lineage studies in the crayfishCherax destructor (Crustacea, Decapoda): germ band formation, segmentation and early neurogenesis.Roux's Arch. Dev. Biol.,202, 36–48.
Selverston, A. I. and Moulins, M. (1987)The crustacean stomatogastric system. Berlin: Springer-Verlag.
Siwicki, K. K., Beltz, B. S. and Kravitz, E. A. (1987) Proctolin in identified serotonergic, dopaminergic, and cholinergic neurons in the lobster,Homarus americanus.J. Neurosci.,7, 522–532.
Taghert, P. H. and Goodman, C. S. (1984) Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo.J. Neurosci.,4, 989–1000.
Valles, A. M. and White, K. (1988) Serotonin-containing neurons inDrosophila melanogaster: development and distribution.J. Comp. Neurol.,268, 414–428.
Voronezhskaya, E. E. and Elekes, K. (1993) Distribution of serotonin-like immunoreactive neurones in the embryonic nervous system of lymnaeid and planorbid snails.Neurobiology (Budapest),1, 371–383.
Windoffer, R. (1992) Immunohistochemische und elektronenmikroskopische Untersuchungen am Nervensystem zweier Dinophilus-Arten mit unterschiedlichem Lebenszyklus. Ph.D. Thesis, UniversitÄt Osnabrück.
Witten, J. L. and Truman, J. W. (1991a) The regulation of transmitter expression in postembryonic lineages in the mothManduca sexta: I. Transmitter identity and developmental acquisition of expression.J. Neurosci.,11, 1980–1989.
Witten, J. L. and Truman, J. W. (1991b) The regulation of transmitter expression in postembryonic lineages in the mothManduca sexta: II. Role of cell lineage and birth order.J. Neurosci.,11, 1990–1997.
Yazawa, T. and Kuwasawa, K. (1992) Intrinsic and extrinsic neural and neurohumoral control of the decapod heart.Experientia,48, 834–840.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Harzsch, S., Dawirs, R.R. A developmental study of serotonin-immunoreactive neurons in the larval central nervous system of the spider crabHyas araneus (Decapoda, Brachyura). Invertebrate Neuroscience 1, 53–65 (1995). https://doi.org/10.1007/BF02331832
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02331832