The Nervous System of the Pike-Tapeworm Triaenophorus nodulosus (Cestoda: Pseudophyllidea): Ultrastructure and Immunocytochemical Mapping of Aminergic and Peptidergic Elements

Abstract

The nervous system of the adult pike-tapeworm Triaenophorus nodulosus was studied to identify nerve cells and fibers immunoreactive to serotonin (5-HT) and RFamide (RF) on whole-mount preparations and frozen sections. Neurons immunoreactive to 5-HT were seen solely in the central nervous system, while those immunoreactive to RF occurred in the peripheral nervous system as well as in the central nervous system. In the scolex, both types of nerve fibers were found. While the gonads were not innervated by either fiber type, the reproductive tract showed RF-immunoreactive nerves. On the ultrastructural level, five types of neurons and three types of release sites and a neuromuscular junction could be distinguished. Levels of 5-HT, measured spectrofluorimetrically, were found to be lower in the tapeworm than in the tissues where it resides in its host, indicating a possibility that the parasite absorbs this bioamine from its environment. Additional key words: 5-HT, RFamide, neuron types, neurotransmitter release sites, spectrofluorimetry During the last two decades, knowledge of the neuroanatomy of flatworms has grown (for review, see Reuter & Gustafsson 1995). For the parasitic flatworms, however, ultrastructure of neuronal elements is still rather poorly known, and information on the nature and number of neuronal mediators in flatworms in general is sparse. To fill part of this gap, we have studied the nervous system (NS) of the pike-tapeworm Triaenophorus nodulosus (PALLAS 1781) with immunocytochemical, ultrastructural, and spectrofluorimetric methods. T. nodulosus parasitizes the intestine of pike as an adult and parasitizes other economically important fishes, such as burbot, as a plerocercoid, the last larval stage. The first parasitic larval stage, the procercoid, develops in fresh-water crustaceans. Apart from the studies of Michajlow (1932, 1933, 1934) little information is available on the histology, especially the neuroanatomy, of the Triaenophoridae. Gustafsson (1973), investigating cellular composition in the neck region of plerocercoids of T. nodulosus, a To whom correspondence should be addressed. Phone: 358 21 2654603; FAX: 358 21 2654748; E-mail: magustaf@ra.abo.fi noted that the cells surrounding the main nerve cords constitute as much as 19% of the total cell population. In light microscopical studies of the general neuroanatomy of T. nodulosus, Kotikova & Kuperman (1977) monitored acetylcholinesterase activity during ontogenesis and documented formation of nerve plexuses and cholinergic nervous elements in the scolex and an increase in the number of longitudinal nerve cords at each successive stage of development; Biserova et al. (1991) used the glyoxylic-acid method to study the aminergic NS of adults and showed evidence of serotonin in ganglia of the brain, connecting commissure, and main nerve cords. Ultrastructure of sensory structures in the scolex was investigated by Biserova et al. (1991); and ultrastructure of the integument, frontal glands, and excretory system was examined by Kuperman (1973, 1988) and Kuperman & Davydov (1982a,b). We have extended the study of adults of T. nodulosus by comparing patterns of peptidergic and aminergic nerve elements, distinguishing types of nerve cells and neurotransmitter-release sites, and measuring serotonin (5-HT) concentrations. The nervous system of flatworms can be subdivided into central and peripheral elements (see Reuter & This content downloaded from 157.55.39.35 on Thu, 01 Sep 2016 04:58:52 UTC All use subject to http://about.jstor.org/terms Biserova, Gustatsson, Reuter, & Terenina Gustafsson 1995 and Reuter et al., in press, for discussion of terminology). The central nervous system of T. nodulosus consists of the bilobed brain and the two main nerve cords (MC's). The peripheral nervous system comprises all the other longitudinal cords (the minor cords), ring commissures in the cortical parenchyma, and nervous structures associated with the genital organs.