The biology of Gyrdicotylus gallieni (Gyrodactylidea), an unusual viviparous monogenean from the African clawed toad, Xenopus laevis

The viviparous gyrodactylid monogenean Gyrdicotylus gallieni, a parasite of Xenopus laevis, is redescribed. The site of infection is shown to be the mouth, and not the stomach and intestine, as recorded in the original description. In most respects G. gallieni is a typical gyrodactylid, but the haptor is modified for suctorial attachment, having two suckers which develop from tegument between the points and ventral roots of the hamuli. The dorsal lobe of the haptor, bearing the marginal hooks, surrounds the suckers and forms a marginal valve. Although this suctorial attachment mechanism suggests a relationship with the polystomatids, this resemblance is due to convergence (being an adaptation for attachment to highly contractile substrata), and G. gallieni is clearly a member of the Gyrodactylidae. However, this parasite differs from other gyrodactylids in the structure of the excretory system and penis, and it appears to have been distinct and isolated for a considerable period, probably since the first appearance of the clawed toads. Gyrdicotylus gallieni gains access to the host's mouth via the nostrils, wandering over the skin of the toad until these are encountered. The parasite is sensitive to water currents, and probably detects the nostril at close range using the olfactory sampling currents of the toad. Some parasites may also enter the mouth attached to food items or sloughed skin. Population growth within the mouth is slow, and infection levels in freshly caught or newly imported toads are low (0–30% prevalence, 1–7 parasites per infected toad). This is due to a slow rate of reproduction rather than to a high mortality, and the age structure of populations within the mouth is biased in favour of older worms. Within groups of isolated, continuously-monitored toads, detached flukes were occasionally found in the culture vessels; these may have left the host as part of the normal transmission biology of G. gallieni. However, much larger groups of flukes (more than 55 individuals from one toad) were also found detached, normally after 1–2 months in captivity. These losses may have been due to a host reaction. Summary Gyrdicotylus gallieni is a viviparous gyrodactylid monogenean which infects the clawed toad Xenopus laevis. This parasite was originally described from the stomach and intestine of its host, an unusual site of infection for a monogenean. However, in more than 2000 Xenopus examined during the present study, it has been found only in the mouth, and the original report of an enteric site of infection was in error. The morphology of G. gallieni is similar to that of other gyrodactylids, although its haptor is extensively modified for suctorial attachment. The hamuli are bound together in the mid-line to form a strut reinforcing the roof of the haptor, and the tegument between the point and ventral root of each hamulus is modified to form a sucker. The dorsal lobe of the haptor, bearing the marginal hooks, extends over the suckers and its edge is infolded to form a marginal valve. SEM studies revealed that plugs of host oral epithelium are drawn up into each sucker and that the marginal hooks pin the marginal valve to the host tissue, preventing the ingress of water into the suckers. The suctorial attachment mechanism of G. gallieni has previously been considered evidence of a link between gyrodactylids and polystomatid monogeneans. However, in the latter group, each sucker arises as an invagination around a marginal hook, whereas in G. gallieni the suckers are associated with the hamuli. The evolution of suctorial attachment in G. gallieni and in polystomatids is a common adaptation to a highly contractile substratum and is not evidence of a phylogenetic relationship. The structure of the excretory system and the penis (which is armed with an entire ring of hooks) suggests that G. gallieni is not closely related to other gyrodactylids, and has remained isolated as a parasite of the ecologically distinct and phylogenetically ancient clawed toads. Gyrdicotylus gallieni gains access to the mouth of Xenopus laevis via the nostrils. Parasites attached to the skin wander (apparently randomly) until they enter the external nares, which they rapidly traverse to reach the mouth. No external cues appear to be used in orientation on the skin surface. However, when in the vicinity of the nares, the parasite may respond to exhalent and inhalent currents with a remarkable flexing response, which results in them gaining entry to the nostril. Growth of G. gallieni populations within the mouth is slow: experimental infections (founded by a single fluke) attained a maximum size of 13 parasites after 70 days. Infection levels in natural toad populations are also low, with prevalence ranging from 0–30% and intensity from 1–7 parasites per toad in groups of X. laevis imported between January 1971 and April 1982. Populations of G. gallieni in imported toads also grew slowly, the maximum recorded being 37 flukes after 90 days' observation. Detached flukes were occasionally noted in the water in which toads were kept; since accidental dislodgement would result in the parasites being swallowed, these individuals had probably left the mouth to disperse to other hosts. The suctorial attachment mechanism and sheltered site of infection are unlikely to result in high accidental mortality, and the age structure of the G. gallieni population is biased in favour of older flukes. This suggests that the slowness of population growth was due to low fecundity rather than high mortality. Apart from the occasional loss of flukes from the mouth of toads, there was also evidence of synchronized elimination of the majority of flukes infecting individual hosts. In many cases, large numbers of flukes were found detached 1–2 months after observations began; more than 55 flukes were released from one toad in this way. It is thought that these losses may have been associated with an unidentified host response.