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The African clawed frog Xenopus laevis (Anura: Pipidae) is host to more than 25 parasite genera encompassing most of the parasitic invertebrate groups. Protopolystoma xenopodis Price, 1943 (Monogenea: Polystomatidae) is one of two monogeneans infecting X. laevis. This study focussed on the external morphology of different developmental stages using scanning electron microscopy, histology and light microscopy. Eggs are released continuously and are washed out when the frog urinates. After successful development, an active swimming oncomiracidium leaves the egg capsule and locates a potential post-metamorphic clawed frog. The oncomiracidium migrates to the kidney where it attaches and starts to feed on blood. The parasite then migrates to the urinary bladder where it reaches maturity. Eggs are fusiform, about 300 μm long, with a smooth surface and are operculated. Oncomiracidia are elongated and cylindrical in shape, with an oval posterior cup-shaped haptor that bears a total of 20 sclerites; 16 marginal hooklets used for attachment to the kidney of the host and two pairs of hamulus primordia. Cilia from the 64 ciliated cells enable the oncomiracidium to swim for up to 24 h when the cilia subsequently curl up, become non-functional and are shed from the body. The tegument between the ciliated cells bears a series of sensory papillae. The body of the mature parasite is elongated and pyriform and possesses an opisthaptor armed with three pairs of suckers and two pairs of falciform hooks to ensure a firm grip on the flexible internal surface of the urinary bladder., (© M. Theunissen et al., published by EDP Sciences, 2014.)

The monogenean Protopolystoma xenopodis has been established in Wales for >40 years following introduction with Xenopus laevis from South Africa. This provides an experimental system for determining constraints affecting introduced species in novel environments. Parasite development post-infection was followed at 15, 20 and 25°C for 15 weeks and at 10°C for ⩾1 year and correlated with temperatures recorded in Wales. Development was slowed/arrested at ⩽10°C which reflects habitat conditions for >6 months/year. There was wide variation in growth at constant temperature (body size differing by >10 times) potentially attributable in part to genotype-specific host-parasite interactions. Parasite density had no effect on size but host sex did: worms in males were 1·8 times larger than in females. Minimum time to patency was 51 days at 25°C and 73 days at 20°C although some infections were still not patent at both temperatures by 105 days p.i. In Wales, fastest developing infections may mature within one summer (about 12 weeks), possibly accelerated by movements of hosts into warmer surface waters. Otherwise, development slows/stops in October-April, delaying patency to about 1 year p.i., while wide variation in developmental rates may impose delays of 2 years in some primary infections and even longer in secondary infections.

Factors affecting survival of parasites introduced to new geographical regions include changes in environmental temperature. Protopolystoma xenopodis is a monogenean introduced with the amphibian Xenopus laevis from South Africa to Wales (probably in the 1960s) where low water temperatures impose major constraints on life-cycle processes. Effects were quantified by maintenance of eggs from infections in Wales under controlled conditions at 10, 12, 15, 18, 20 and 25°C. The threshold for egg viability/ development was 15°C. Mean times to hatching were 22 days at 25°C, 32 days at 20°C, extending to 66 days at 15°C. Field temperature records provided calibration of transmission schedules. Although egg production continues year-round, all eggs produced during >8 months/ year die without hatching. Output contributing significantly to transmission is restricted to 10 weeks (May-mid-July). Host infection, beginning after a time lag of 8 weeks for egg development, is also restricted to 10 weeks (July-September). Habitat temperatures (mean 15·5°C in summer 2008) allow only a narrow margin for life-cycle progress: even small temperature increases, predicted with 'global warming', enhance infection. This system provides empirical data on the metrics of transmission permitting long-term persistence of isolated parasite populations in limiting environments.

Naive, full-sibling juveniles of Xenopus laevis laevis were exposed to 10, 30, or 50 larvae of the monogenean Protopolystoma xenopodis from an isolate known to produce relatively low adult establishment (typically less than 25% prevalence) in hosts of the same pedigree. Postlarval survival (worms per host) 7 days postinfection (PI), timing from the end of a 10-day infection window, was significantly related and proportional (approximately 31%) to infection dose. Establishment of newly mature adults 90 days PI was low (0-3 worms/host) and unrelated to infection dose. Results confirm that postlarval mortality is severe in primary infections, and that surviving adult infrapopulations appear to be regulated to a very low level (most often 1 worm/ host), even at relatively high larval infection pressures. This density-dependent process could involve direct antagonistic parasite-parasite interactions or indirect interference mediated by parasite-induced host defenses.

Immune responses in ectothermic vertebrates and the life-processes of their parasites are profoundly linked to ambient temperature, but the functional effect of thermal environment on infectivity and host-specificity in helminths from ectotherms is poorly known. Primary infection establishment of Protopolystoma xenopodis (Monogenea) in compatible hosts ( Xenopus laevis: Anura) is strongly modulated by ambient temperature. Significantly fewer worms survived to the urinary bladder stage at 25 degrees C than at 15 degrees C (relatively high and low temperatures for this system in nature). Pre-infection exposure of X. laevis to cold (10 degrees C) did not significantly affect parasite establishment in the urinary bladder (at 15 or 25 degrees C p.i.), nor shorter-term postlarval survival in the kidneys (at 20 degrees C p.i.), suggesting that residual immunosuppressive effects on host susceptibility are not important. Low temperatures had no permissive effect on the establishment of P. xenopodis in incompatible hosts (Xenopus wittei). The link between thermal conditions and parasitic infection of ectotherms is discussed.

Protopolystoma xenopodis is an oviparous monogenean occurring as an adult in the urinary bladder of the African clawed toad, Xenopus laevis. Egg production was monitored in two groups of infected hosts exposed to decreasing environmental temperatures. Despite possible upward trends in reproductive capacity with parasite age, oviposition rate was severely depressed at lower temperatures. In one experiment, egg production was monitored in a sample of seven hosts at 2 degrees C intervals between 20 and 8 degrees C. Overall mean egg production rate showed a consistent decline from 11.9 eggs/worm/day (e/w/d) at 20 degrees C (days 1-10) to 0.9 e/w/d at 8 degrees C (days 115-124). In a second experiment (n = 11 hosts) oviposition rate was recorded at the same intervals between 20 and 6 degrees C and then hosts were returned to 20 degrees C. Overall mean egg production rate decreased consistently from 4.1 e/w/d at 20 degrees C (days 1-10) to 0.2 e/w/d at 6 degrees C (days 124-131), at which temperature all infections continued to produce eggs. When parasites were then returned to 20 degrees C (141-150 days), mean oviposition rate at this temperature (12.7 e/w/d) was found to have increased by 310% from the start of the experiment (130 days earlier) and by 6350% from production at 6 degrees C (9 days earlier). P. xenopodis has been introduced to South Wales, U.K. and present results show that it could produce eggs here through almost all of the year. However, a massive annual reduction in the reproductive output of this parasite in the U.K., compared with that in natural sites, is predicted.