Post-cyclic transmission in Pomphorhynchus laevis (Acanthocephala)

A series of laboratory experiments was conducted to investigate the possibility of post-cyclic transmission in Pomphorhynchus laevis (Müller, 1776). Rainbow trout Oncorhynchus mykiss (Walbaum) were exposed to P. laevis in naturally infected Cottus gobio Linnaeus, Noemacheilus barbatulus (Linnaeus), Phoxinus phoxinus (Linnaeus) and Leuciscus cephalus (Linnaeus) and sacrificed one month after infection. Post-cyclic transmission was possible from all four species even though they came from three families and differed in respect of their status and suitability as hosts of P. laevis. There was no selection for or against either sex of P. laevis, parasites grew in the rainbows and they occupied the same, normal site in the intestine of rainbows irrespective of source host. Post-cyclic transmission of gravid parasites could occur from C. gobio but not from L. cephalus. It is believed that this failure to transmit larger parasites of either sex reflects the age and so development of the proboscis bulb of P. laevis and the extent of the host encapsulation response rather than size or stage of maturity per se. Post-cyclic transmission has the potential to be important in nature. The phenomenon of post-cyclic transmission has been most clearly described by Nickol (1985) as “When ingested as adults within their definitive hosts some acanthocephalans survive and parasitise the predator”. Nickol further commented that little is known regarding post-cyclic transmission in acanthocephalans, although he listed five species from which it had been reported. Uglem and Beck (1972) achieved post-cyclic transmission of Neoechinorhynchus cristatus Lynch, 1936 experimentally by force feeding of several species of fish, but showed that only sub-adults established in the predator host and even these had all disappeared seven days post infection (dpi). They were completely unable to achieve transmission in the closely related species N. crassus Van Cleeve, 1919. Lassiere and Crompton (1988) demonstrated that post-cyclic transmission could occur in N. rutili (Müller, 1780) when rainbow trout Oncorhynchus mykiss (Walbaum) were allowed to feed on naturally infected Gasterosteus aculeatus Linnaeus in the laboratory. This parasite survived in the predator host for up to 10 dpi. Several authors have suggested that this form of transmission may be important in nature (Hnath 1969, DeMont and Corkum 1982, Nickol 1985, Lassiere and Crompton 1988, Valtonen and Crompton 1990), but they have provided no evidence in support of this. Indeed, until more is known about a phenomenon that has been reported from a few species only and that is not a property of all species or all stages of a species, it is difficult to obtain any idea of its potential significance in natural systems. If parasites transmitted in this manner do not survive long in the predator (Uglem and Beck 1972), post-cyclic transmission may be of little or no importance in nature at all. Post-cyclic transmission has not hitherto been reported from any species of the genus Pomphorhynchus, though Kennedy (1996) drew attention to the possibility of its occurring in P. laevis (Müller, 1776) between Cottus gobio Linnaeus and Salmo trutta Linnaeus in the River Otter. It might in fact be considered unlikely that it would be exhibited by this species in view of the particularly firm attachment of P. laevis its host’s intestine. This involves a host response such that the bulb of the parasite, and indeed often the whole praesoma of adults, is enclosed in a nodule of host fibrous tissue that forms a tough capsule (Hine and Kennedy 1974, Wanstall et al. 1986, 1988). Nevertheless, when a preliminary experiment indicated that post-cyclic transmission of P. laevis from C. gobio to O. mykiss could occur in the laboratory, the system was investigated further to provide wider and more detailed information on the phenomenon. The particular aims of the investigation were to provide information on the range of naturally infected fish species that could be sources of parasites for such transmission, to determine whether all stages and both sexes of the parasite could transmit with equal facility, to see whether the parasite could survive for longer than 7 dpi and grow and, if so, to find out whether it located in the same region of the predator’s intestine as it does when infection is achieved by ingestion of an infected gammarid intermediate host. The results of these experiments, which achieved the aims, are reported and discussed in this paper. Address for correspondence: C.R. Kennedy, School of Biological Sciences, University of Exeter, Hatherly Laboratories, Prince of Wales Road, Exeter EX4 4PS, UK. Phone: ++44