Ultrastructural characteristics of the vitellarium of Brandesia turgida (Brandes, 1888) (Digenea: Pleurogenidae) and an examination of the potential usefulness of such vitelline traits in digenean systematics

Abstract

SummaryTransmission electron microscopical observations were made on the vitelline structure of the digenean Brandesia turgida (Brandes, 1888) collected from crypts within the intestinal wall of the frog Pelophylax ridibundus (Pallas, 1771). Ultrastructural details of the vitelline follicles of B. turgida include: (a) the presence within the vitellarium of a single type of cell, i.e. vitellocytes at different stages of their development; (b) a narrow region between the vitellocytes filled with the processes of surrounding parenchymal cells; and (c) the occurrence of the junctional complexes between the vitellocytes and the surrounding parenchymal cells at the periphery of the vitelline follicles. It is shown that the vitelline globules and a few lipid droplets are the main inclusions resulting from vitellocyte synthetic activity. The limited amount of nutritive reserves in the vitellocytes can be explained by the nature of the parasite's life-cycle, which is characterized by fully-embryonated intrauterine eggs containing a fully-formed miracidium. Despite the small number of digenean species studied in relation to their vitelline cytoarchitecture, two structural patterns of the vitellarium can be elucidated; these are examined in terms of digenean systematic relationships.

The unusual cytoarchitecture of “vitelline follicles” in freshwater blood flukes of the genus Sanguinicola (Digenea, Aporocotylidae)

“…Interestingly, these intercellular junctions have been observed between vitelline cells at the same stage and at different stages of maturation. There are previous reports of the presence of heterologous and homologous contact sites between the vitelline follicles, i.e., in the monopisthocotylean monogenean Ancyrocephalus paradoxus [26], the aspidogastrid aspidogastrean Aspidogaster limacoides [26] and digeneans of the families Diplostomatidae [5], Microphallidae [11,35], Pleurogenidae [25] and Aporocotylidae ( [27], present study). The presence of intercellular junctions in digeneans possessing a proper follicular vitellarium may suggest a close relationship between vitelline cells and between vitelline and muscle cells.…”

“…The cytoarchitecture of vitelline follicles proper has previously been described for another aporocotylid, Aporocotyle simplex, which belongs to the marine, teleost-infecting aporocotylid lineage [27]. Vitelline follicles with the usual cytoarchitecture have also been described in digeneans of the orders Diplostomida, i.e., the diplostomatid Pharyngostomoides procyonis [5], and Plagiorchiida, i.e., the microphallids Maritrema linguilla [11] and M. feliuli [35], the cryptogonimids Aphallus tubarium [6] and Metadena depressa [7], the pleurogenid Brandesia turgida, [25] and the opecoelid Cainocreadium labracis [36]. However, in the gorgoderids Gorgoderina vitelliloba [12] and Phyllodistomum angulatum [24], the fasciolid Fasciola hepatica [10,13], the gyrabascid Allassogonoporus amphoraeformis [30] and the azygiid Azygia lucii [24], a different kind of vitelline cytoarchitecture has been indicated, where both vitelline and interstitial cells are found surrounded by a basal matrix.…”

“…and 0.8-1.8 lm with 10-20 globules in A. simplex (Present study, [27]). Differences in the morphology, size and number of digenean vitelline clusters and globules within the clusters may be related to variations in the structure, size and number of the eggs and the size of the egg-shell [3,11,24,25,[34][35][36]. Vitelline globules represent building material for eggshell formation [34], which is deposited on the developing eggshell [14,40].…”

“…Taking into account the fact that the eggshell of species of Sanguinicola and Aporocotyle is very thin [16,18,27,32,33,38], this may explain the presence of a rather small number of globule clusters and globules within the clusters in their mature vitellocytes. The proportions of lipid droplets and glycogen in digenean vitelline cells, both of which represent nutritive material available to the developing embryo, vary between different digenean species [3,11,24,25,35,36,39]. Such differences may reflect variations in the retention of the eggs within host tissues or their development in the external environment, where they may survive for long periods waiting for transmission of the miracidium to the new host [2,9,10,24,35,38].…”

“…Its configuration has been used as an important taxonomic or even phylogenetic criterion at several levels [4]. Furthermore, judging from the existing literature on ultrastructure, some characteristics of the vitelline cytoarchitecture have been used as discriminatory traits for digenean lineages [24,25]. The latter traits include the presence of one or two types of cell components within the vitellarium, i.e., vitelline cells (vitellocytes) at different stages of development and interstitial cells; the occurrence of junctional complexes between cells within the vitellarium; and the presence or absence of a specialized sheath of the basal matrix, which isolates the vitellarium from the surrounding cells and organs.…”