Spatial and energy compromise between host and parasite: The Biomphalaria glabrata-Schistosoma mansoni system

Inrernarionalfournalfor Primed in Great Brifnin

Parasitology

Vol. 22. No. I, pp. 91-94, 1992 0

002&7519/92 S5.M) + O.CKl Pergamn Press p/c 1992 Auslralian Society forParasitology

SPATIAL AND ENERGY COMPROMISE BETWEEN HOST AND PARASITE: THE BIOMPHALARIA GLABRATA-SCHISTOSOiMA MANSONI SYSTEM ANDRB THBRON, HBLBNE MONB

and CLAUDIA GERARD

Laboratoire de Biologie Animale, URA CNRS 698, Centre de Biologie et d’Ecologie tropicale et mediterrantenne, 52, Av. de Villeneuve, 66860 Perpignan Cedex, France (Received22

Universite,

March 1991; accepted 31 July 1991)

Abstract-T&RON A., MONBH. and GERARDC. 1992. Spatial and energy compromise between host and parasite: the Biomphalaria glabrata_Schistosoma mansoni system. International Journalfor Parasitology 22: 91-94. The development of a sporocyst infrapopulation of Schistosoma mansoni within the Biomphalaria glabrata snail is, from a spatial point of view, detrimental to the host’s digestive-genital gland complex

growth. For mono- and plurimiracidial infections, the digestive gland volumes are, respectively 51 and 24% of those of control snails. Identical reduction of the infected genital gland volume (43% of controls) occurs in both cases. After the prepatent period, the ratio of parasite/digestive gland volumes (P/PDG) remains fairly constant at around 0.60 independent of the miracidial dose infection, indicative of a balanced hostparasite development which is discussed in relation to the spatial and energy constraints of this system. INDEX KEY WORDS: Schistosoma mansoni; Biomphalariaglabrata; sporocyst; infrapopulation; dynamic; digestive gland; genital gland; interactions; growth; spatial constraints; energy constraints.

INTRODUCTION WHEN

a host-parasite

association is establishing within a mollusc-trematode system, the development of the parasite infrapopulation (sporocysts or rediae) is detrimental in energy terms to the host’s development: either by direct drain of nutrient resources (Becker, 1980) or indirectly through more complex behavioural manipulations, in particular those linked with the host’s reproductive physiology (Minchella & Loverde, 1981; Crews & Yoshino, 1989; De JongBrink, Elsaadany & Boer, 1988a,b). Whatever the

modalities of these interactions, competition for the resources between parasite development and certain host organs occurs. To be sufficiently durable according to the fitness of the parasite, this mollusctrematode association has to reach an energy compromise compatible on the one hand with the needs of the parasite for its reproduction, and on the other hand with the needs of the host for its survival. Biochemical and physiological interactions between host and parasite have been the subject of a large number of different types of study, recently reviewed (Bayne & Loker, 1987; Hurd, 1990). The host-parasite interactions related to the spatial constraints imposed by such a system have been studied far less (Schwanbek, Becker & Rupprecht, 1986). In addition to their energy needs, the infrapopulations of larval parasites also need space to develop fully. In the snailtrematode association this spatial constraint is all the

more important since: (i) the preferential biotope of the parasite, primarily the digestive gland (DG) and the genital gland (GG), has only a few lacunary spaces capable of harbouring the very numerous larvae; (ii) the volumetric growth of the sporocysts infrapopulation is high and very rapid during prepatency. A study of the respective volumes of parasite and host tissues (DGG complex) and the evolution of their relative proportions during the infection of Biomphalaria glabrata by Schistosoma mansoni was carried out in order to show whether spatial competition exists between the parasite and its host biotope, and the limits not to be exceeded to reach a viable energy compromise. MATERIALS AND METHODS An albino strain of B. glabrata of Brazilian origin (Recife) and a Brazilian strain of S. mansoni (maintained on Swiss OF1 mice) were used. Infection of snails was obtained after individual exposure of molluscs between 4.5 and 6.5 mm in shell diameter to one (Sml) or eight (Sm8) miracidia in 5 ml of spring-water. For all the experiments, the control and infected snails were kept individually in glasses containing 150 ml of well-water at a constant temperature of 26°C and fed on lettuce leaves ad libitum. The water in the beakers was changed every 7 days. Individuals were randomly removed at regular intervals from the three batches of snails, to evaluate the different parameters used: proportion of parasites (P) in relation to the ‘parasite-digestive gland’ complex (P/PDG); volume of the ‘parasite-digestive genital gland’ complex 91

92

A. THBRON, H. MONB and C. GERARD 1s

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FIG. I. Growth kinetics of B. glabrafa control (O-O) infected with one miracidium ( q - 0) and eight miracidia A) of S. mansoni. WPI, Week post-infection.

and (A -

(PDGG). For the snail growth study, the size of each snail was measured every week for 12 weeks using 15 control snails, 10 snails infected with one miracidium (Sml) and 21 infected with eight miracidia (Sm8). Data are reported as mean values f confidence limits (P=O.Ol). The MannWhitney U test was used for statistical comparison and results were considered statistically significant at P