The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis

Abstract

Digenean trematodes are common and abundant in aquatic habitats and their free-living larvae, the cercariae, have recently been recognized as important components of ecosystems in terms of comprising a significant proportion of biomass and in having a potentially strong influence on food web dynamics. One strategy to enhance their transmission success is to produce high numbers of cercariae which are available during the activity peak of the next host. In laboratory experiments with 13 Lymnaea stagnalis snails infected with Trichobilharzia szidati the average daily emergence rate per snail was determined as 2,621 cercariae, with a maximum of 29,560. During a snail’s lifetime this summed up to a mass equivalent of or even exceeding the snail’s own body mass. Extrapolated for the eutrophic pond where the snails were collected, annual T. szidati biomass may reach 4.65 tons, a value equivalent to a large Asian elephant. Emission peaks were observed after the onset of illumination, indicating emission synchronizing with the high morning activities of the definitive hosts, ducks. However, high cercarial emission is possible throughout the day under favorable lightning conditions. Therefore, although bird schistosomes, such as T. szidati constitute only a fraction of the diverse trematode communities in the studied aquatic ecosystem, their cercariae can still pose a considerable risk for humans of getting cercarial dermatitis (swimmer's itch) due to the high number of cercariae emitted from infected snails.

Hidden diversity: parasites of stream arthropods

“…Parasites of these organisms might alter the distribution and abundance of their hosts, thereby influencing the outcome of ecological assessments. Nevertheless, in most studies on the ecology of free‐living aquatic organisms, parasites are not considered as a factor despite their importance for food‐web structure, biomass and ecosystem integrity (Marcogliese & Cone, ; Marcogliese, ; Lafferty, Dobson & Kuris, ; Dobson, Lafferty & Kuris, ; Kuris et al ., ; Lagrue & Poulin, ; Soldánová, Selbach & Sures, ). These characteristics give parasites key roles in some ecosystems, where they significantly influence the ecological relationships of free‐living species, and thereby modify species diversity and habitat structure (Mouritsen & Poulin, ; Hatcher, Dick & Dunn, ).…”

Small snails, high productivity? Larval output of parasites from an abundant host

“…Lagrue & Poulin, ). Despite the high snail abundance, overall trematode prevalence in Tomahawk Lagoon is lower than in other systems where infection rates often reach 30% or more in summer (e.g., Preston et al., ; Soldánová et al., ). This further supports the assumption of Lagrue and Poulin () that intermediate host populations in the system are potentially underexploited by parasites and that parasite populations might rather be constrained by other factors, such as transmission dynamics or other epidemiological processes than by limited host resources.…”

“…Finally, we converted the individual cercarial body volume into wet mass by multiplication with 1.1 g/cm 3 (Kuris et al., ). This method has been used previously in studies of cercarial productivity (Kuris et al., ; Soldánová et al., ; Thieltges et al., ). However, Llopis‐Belenguer, Blasco‐Costa, and Balbuena () recently showed that such geometric approximation methods lead to a roughly threefold overestimation of the actual volume of trematode flatworms, due to their flattened bodies (see Supporting Information Figure ).…”

“…Parasite biomass remarkably exceeded that of top predators in the habitat. Following this pioneering assessment, several studies have revealed comparable patterns in various freshwater and marine systems, showing that parasites, especially the asexually produced larval stages of trematodes (i.e., flukes), contribute significantly to the energy flow in aquatic ecosystems (Preston, Orlofske, Lambden, & Johnson, ; Soldánová, Selbach, & Sures, ; Thieltges et al., ). Consequently, these abundant and glycogen‐rich larvae, the cercariae, typically ranging in size between 0.2 and 2 mm, constitute an important planktonic food source to a wide range of non‐host predators (Johnson et al., ; Kaplan, Rebhal, Lafferty, & Kuris, ; Morley, ; Thieltges et al., ; Welsh, Liddell, Van Der Meer, & Thieltges, ).…”

“…Altogether, ecosystem‐wide studies remain scarce and documented examples do not necessarily allow general conclusions to be drawn regarding productivity patterns in other host–parasite systems. Existing studies on cercarial productivity are based on relatively large first intermediate snail hosts, such as Lymnaea stagnalis , Helisoma trivolvis and Cerithidea californica , with typically high infection prevalence (>30%) of parasites that can release thousands of larvae per infected snail (Kuris et al., ; Preston et al., ; Soldánová et al., ). Cercarial productivity depends on host size (i.e., resources available for parasite productivity) and infection prevalence in the snail population (i.e., the proportion of infected individuals).…”