Lo (1999) examined 365 humbugs, Dascyllus aruanus, a small (few cm long) coral-reef fish, infected with a single species of gill monogenean, Haliotrema sp., and recorded the number of 'couples', i.e. monogeneans showing microhabitat overlap, on fish with low intensities of infection (fewer than five monogeneans per gill). A very high percentage of monogeneans occurred in couples, suggesting (possibly chemical) attraction by worms, because intraspecies microhabitat overlap should be very scarce if coupling occurred on a random basis. Attraction seems to be effective over relatively great distances, for example between gill arches. Haseeb and Fried (1988) also suggested that adult monogeneans, Diclidophora merlangi, migrate towards each other. Lo (1999) concluded that 'mating is a main focus of monogenean life', supporting Rohde's mating hypothesis. Kearn et al. (1993) made extensive studies of the monogenean E. soleae, a parasite of the sole, Solea solea, in England. They concluded that the parasite is unable to self-fertilize in the wild. Mathematical modelling showed that random locomotion with searching movements of the body would lead to mate finding on small fish within the reproductive lifetime of the worm. However, it is unlikely that mating will occur soon after maturation. Attraction by pheromones could ensure early mating and the thin layer of water, stagnant between the lower surface of the fish and the sea bottom, would be an ideal environment for the action of such pheromones. The authors suggest that this may explain the preferred habitat of the worm: the lower surface of the fish. However, pheromones have not yet been demonstrated.
Nollen (1997b) has given a review of mating and chemical attraction in trematodes, Basch (1991) reviewed the reproductive biology in the dioecious schistosomes and Haas (2000) included a brief section on mating in his review of the behavioural ecology of echinostomes. In vitro experiments by Fried and collaborators showed chemoattraction between immature and mature adults of echinostomes. The free sterol fraction of lipophilic extracts of the worms was found to be responsible (Fried et al., 1980; Fried and Diaz, 1987; Fried and Haseeb, 1990). Interspecific attraction between adult E. caproni and Echinostoma trivolvis also occurred, but was less significant than that between individuals of E. trivolvis. Interestingly, E. trivolvis, which occurs along the whole small intestine, showed greater intraspecific chemoattraction than E. paraensei, which is very site-specific - to the duodenum. Trouve and Coustau (1998) demonstrated differences in the excretory-secretory products of three strains of E. caproni, which may be the basis of selective mating. In this species, populations are highly subdivided along their microhabitat, the small intestine, promoting local mate competition (Trouve et al., 1999b). An alternative mechanism of reproductive isolation, not dependent on mate attraction, is suggested by the findings of Trouve and Coustau (1999). These authors examined mating between two geographical isolates of E. caproni and another species of the same genus. They recorded similar attraction for intraisolate, interisolate and interspecific combinations and suggested that reproductive isolation may be due to sperm selection. Some studies have demonstrated chemoattraction by neutral lipids in mating of schistosomes (review in Nollen, 1997b). In vitro, excretion of such lipids is increased in the presence of other worms, and males and females that were separated and allowed to reunite paired more frequently with the original partner than with new ones. Males of schisto-somes may have more than one female in their gynaecophoric groove, or they may share females or also hold males if there is an undersupply of females. Also, female reproductive organs do not fully develop in unpaired worms, and females of some species (review in Basch, 1991) need stimulation by males to continue growth and production of eggs. Female reproductive organs even regress in the absence of a male, but production of eggs begins again after re-pairing. Females obtain glucose from males, and male extracts stimulate development of female vitellaria. Some schistosomes, at least, may also reproduce by parthenogenesis (references in Nollen, 1997b). In the two species Schistosoma haematobium (primarily parasitic in humans) and Schistosoma mattheei (parasitic in livestock and wild ungulates), hybridization, leading to the production of viable offspring, occurs in experimentally infected mice (Southgate et al., 1995), indicating that mate attraction is not limited to males and females of the same species. However, hybridization in nature is highly unlikely, considering the different hosts. Also, specific mate choice systems do not appear to exist in some other combinations of different Schistosoma species, whereas they do in others (Southgate et al., 1998). Nevertheless, overall, most schistosomes infecting the same final host maintain their genetic identity (Southgate et al., 1998).
Among the acanthocephalans, endoparasites of vertebrates, aggregation for mating is known to occur in some species. In a study on Acanthocephaloides propinquus infecting the gobiid fish Gobius bucchichii, Sasal et al. (2000) determined infection intensities, sex ratios and testicular size and found that, when the percentage of males increased (suggesting increased competition between males), the size of the testes increased as well. The authors also concluded that competition for access to females was more important than competition for space.
Numerous studies of mating of nematodes have been made, but most of them deal with the free-living C. elegans. Copulation involves a series of complicated steps (e.g. Liu and Sternberg, 1995), copulatory plugs are used to assure paternity (Barker, 1994), and even mutations that affect neurons involved in certain copulatory behaviour patterns have been identified (Loer and Kenyon, 1993). In T. spiralis, differences in distributions of mixed, single male and single female infections suggest that males migrate in search of females (Sukhdeo and Bansemir, 1996), and experimental studies have indeed shown that males and females are attracted to each other (references in Sukhdeo and Bansemir, 1996). The same authors report that, when females and males of Heligmosomoides polygyrus are transplanted together into the terminal ileum of mice, males migrate faster to the duodenum (their normal habitat) than females, leaving the females behind, implying that males choose habitat over female. This is hardly an argument against the importance of mate selection, since mating occurs once both sexes are established in the duodenum.
Mating behaviour of copepods has been studied in a number of species, but most of them are free-living. Sophisticated behaviour patterns lead to mate encounters, and males show distance chemoreception, as well as recognition at close range, which may involve fluid mechanism signals of short duration and contact chemical signals. i.e. species- and sex-specific glycoproteins (Boxshall, 1998, and references therein). Precopulatory mate-guarding appears to be common not only in free-living species, but in parasitic species as well (e.g. in Lernaeocera branchialis (Heuch and Schram, 1996)). The mating behaviour of Lepeophtheirus salmonis and some other parasitic copepods was described by Anstensrud (1990a-d, 1992) and Ritchie et al. (1996). The latter study suggests that long-range, short-range and contact chemical stimuli play a role in pairing and mate recognition, either on their own or jointly. It must be emphasized that sea lice are highly mobile, both on and between their hosts (salmon) (Hull et al., 1998), which may explain the involvement of long-range chemical stimuli. But, overall, little is known about the role of chemoreception in mating sea lice (Hull et al., 1998).
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