Cost of interspecific competition between trematode colonies.

In a range of trematode species, specific members of the parthenitae colony infecting the molluscan first intermediate host appear specialized for defence against co-infecting species. The evolution of such division of labour requires that co-infection entails fitness costs. Yet, this premise has very rarely been tested in species showing division of labour. Using Himasthla elongata (Himasthlidae) and Renicola roscovita (Renicolidae) infecting periwinkles Littorina littorea as study system, we show that the size of emerged cercariae is markedly reduced in both parasite species when competing over host resources. Cercarial longevity, on the other hand, is negatively influenced by competition only in R. roscovita. Season, which may impact the nutritional state of the host, also affects cercarial size, but only in H. elongata. Hence, our study underlines that cercarial quality is, indeed, compromised by competition, not only in the inferior R. roscovita (no division of labour) but also in the competitively superior H. elongata (division of labour).

Climate change, parasitism and the structure of intertidal ecosystems.

Evidence is accumulating rapidly showing that temperature and other climatic variables are driving many ecological processes. At the same time, recent research has highlighted the role of parasitism in the dynamics of animal populations and the structure of animal communities. Here, the likely interactions between climate change and parasitism are discussed in the context of intertidal ecosystems. Firstly, using the soft-sediment intertidal communities of Otago Harbour, New Zealand, as a case study, parasites are shown to be ubiquitous components of intertidal communities, found in practically all major animal species in the system. With the help of specific examples from Otago Harbour, it is demonstrated that parasites can regulate host population density, influence the diversity of the entire benthic community, and affect the structure of the intertidal food web. Secondly, we document the extreme sensitivity of cercarial production in parasitic trematodes to increases in temperature, and discuss how global warming could lead to enhanced trematode infections. Thirdly, the results of a simulation model are used to argue that parasite-mediated local extinctions of intertidal animals are a likely outcome of global warming. Specifically, the model predicts that following a temperature increase of less than 4 degrees C, populations of the amphipod Corophium volutator, a hugely abundant tube-building amphipod on the mudflats of the Danish Wadden Sea, are likely to crash repeatedly due to mortality induced by microphallid trematodes. The available evidence indicates that climate-mediated changes in local parasite abundance will have significant repercussions for intertidal ecosystems. On the bright side, the marked effects of even slight increases in temperature on cercarial production in trematodes could form the basis for monitoring programmes, with these sensitive parasites providing early warning signals of the environmental impacts of global warming.

Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi.

Metacercariae of the trematode Curtuteria australis (Echinostomatidae) accumulate in the foot of the New Zealand cockle Austrovenus stutchburyi, severely impairing the cockle's ability to burrow under the sediments. This results in increased predation by birds on cockles, and thus enhanced transmission rates of the parasite to its bird definitive hosts. This host manipulation by the trematode is costly: fish regularly crop the tip of the foot of cockles stranded on the sediment surface, killing any metacercariae they ingest. A second, previously undetected trematode species (characterized by 23 collar spines) co-existing with C. australis, has been found in the foot of cockles in the Otago Harbour, South Island, New Zealand. The relative abundance of the two species varies among localities, with the identity of the numerically dominant species also changing from one locality to the next. Both C. australis and the new species have a strong preference for encysting in the tip of the cockle's foot, where their impact on the burrowing ability of the host is greatest, and where they both face the risk of cropping by fish. Results indicate that these two species are ecological equivalents, and their combined numbers determine how the cockle population is affected.

Use of ITS rDNA for discriminating of larval stages of two microphallid (Digenea) species using Hydrobia ulvae (Pennant, 1777) and Corophium volutator (Pallas, 1766) as intermediate hosts.

Digenean trematodes encompass several species with little morphological differentiation in the larval stages and, as a result, uncertainty prevails regarding species identification. The microphallid trematode Maritrema subdolum occurs widespread geographically in mud snail and crustacean hosts in European marine shallow-water ecosystems. Larval stages of this and other congeneric species are, however, difficult to separate morphologically. To verify the species status and to secure identification of two co-occurring microphallids, M. subdolum and microphallid sp. no. 15 (Deblock, 1980), we examined the nucleotide sequences of the internal transcribed spacer regions (ITS1, ITS2). From fragments consisting of both ITS regions and the 5.8S gene (nearly 1,200 bp), a sequence divergence of 2.9% between the two types was recorded. In accordance with the morphological traits of the cercariae (stylet shape, length), the results support the view that the two types actually represent different species. Species-specific primers were prepared for each species. They proved to be efficient diagnostic tools for identifying single larval-stage individuals. Using these primers, infections in host organisms were also verified without performing a dissection of the host individuals.

Parasite-induced surfacing in the cockle Austrovenus stuchburyi: adaptation or not?

Parasite manipulation of host behaviour is a compelling example of the extended phenotype. However, in many cases, such manipulation may be incorrectly assumed. Previous work has demonstrated that Austrovenus stuchburyi cockles stranded on mud-flat surfaces due to an inability to re-burrow both contain significantly more metacercariae of the trematode Curtuteria australis and are predated by the definitive host of this parasite at a faster rate than burrowed cockles. These results have been interpreted as strong evidence for a manipulation of cockle behaviour by the trematode to facilitate transmission to the definitive host. The model presented here, however, indicates that the selective advantage to the parasite of the altered host behaviour is currently of a negligible level at our study site that is highly unlikely to have been realized as an adaptation over evolutionary time. Hence, there are no grounds on which the more parsimonious explanation, that the altered host behaviour observed is simply an incidental side-effect of infection, can be rejected. We thus maintain that for any change in the behaviour of infected hosts to be confirmed as potentially a parasite trait that has evolved in response to selection, the adaptive benefit taking into account the entire parasite life cycle may need to be considered.

From first to second and back to first intermediate host: the unusual transmission route of Curtuteria australis (Digenea: Echinostomatidae).

The trematode Curtuteria australis uses the whelk Cominella glandiformis as first intermediate host and the cockle Austrovenus stutchburyi as second intermediate host before maturing in shorebirds. The whelk also happen to be an important predator of cockles on intertidal mudflats. In this study we show that whelks can act as temporary paratenic hosts for the trematode. A single whelk feeding on 1 cockle can ingest large numbers of metacercariae, which remain within the whelk for 1-3 days before passing out in feces. The viability of these metacercariae assessed as the percentage capable of successfully excysting under conditions simulating those inside a bird's digestive tract, is lower after passage through a whelk (48%) than before (59%). Still, given that shorebird definitive hosts prey on whelks as well as cockles, survival inside the whelk allows C. australis to complete its life cycle: overall, though, whelk predation is likely to be an important sink for the trematode population. To our knowledge, this is the first report of a trematode using a snail as both first intermediate host and paratenic host, offering an alternative transmission route for the parasite as a result of the unusual trophic relationships of its hosts.

The Hydrobia ulvae-Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity.

The effects of environmental factors and exudates from the amphipod Corophium volutator on the emergence of Maritrema subdolum cercariae (Digenea: Microphallidae) from the snail Hydrobia ulvae were investigated in the laboratory. Increasing the temperature (15 to 25 degrees C) caused an overall 11-fold increase in emergence rate under varying salinities (24 to 36 per thousand). The effect of salinity depended on the experimental temperature. Emergence increased with increasing salinity at higher temperatures, but decreased with increasing salinity at 15 degrees C. Whereas the different levels of salinity had no effect, increasing the temperature significantly reduced the life span of cercariae. In comparison with complete darkness, light caused a two-fold increase in emergence, whereas an increment of the water pressure from 1.0 to 1.3 ATM (corresponding to 0 and 3 m of depth) left the shedding rate unaffected. Unidentified exudates from the second intermediate host, C. volutator, significantly depressed the cercarial emergence rate. The main transmission window of M. subdolum seems to occur during low water in tidal pools where light levels are high and solar radiation rapidly elevates the water temperature, as well as salinity through evaporation. The consequence of such a transmission strategy is discussed in relation to the impact of M. subdolum on the population dynamics of the second intermediate host.

The Hydrobia ulvae-Maritrema subdolum association: cercarial emergence controlled by host activity.

The release of Maritrema subdolum cercariae (Digenea: Microphallidae) from the marine mud snail Hydrobia ulvae is significantly affected by temperature, salinity, light and exudates from the second intermediate amphipod host. Based on (i) previously published data on temperature-salinity dependent H. ulvae activity, (ii) new experimental data on H. ulvae activity in light and darkness as well as in the presence and absence of host exudates, and (iii) the cercarial emergence rate from free moving snails and snails prevented from crawling, the present analysis indicates that emergence of M. subdolum larvae is regulated mainly by host activity as the ultimate factor for release. The adaptive significance of such an emergence strategy is emphasized.

Parasitism, community structure and biodiversity in intertidal ecosystems.

There is mounting evidence that parasites can influence the composition and structure of natural animal communities. In spite of this, it is difficult to assess just how important parasitism is for community structure because very few studies have been designed specifically to address the role of parasites at the community level, no doubt because it is difficult to manipulate the abundance of parasites in field experiments. Here, we bring together a large amount of published information on parasitism in intertidal communities to highlight the potential influence of parasites on the structure and biodiversity of these communities. We first review the impact of metazoan parasites on the survival, reproduction, growth and behaviour of intertidal invertebrates, from both rocky shores and soft-sediment flats. Published evidence suggests that the impact of parasites on individuals is often severe, though their effects at the population level are dependent on prevalence and intensity of infection. We then put this information together in a discussion of the impact of parasitism at the community level. We emphasize two ways in which parasites can modify the structure of intertidal communities. First, the direct impact of parasites on the abundance of key host species can decrease the importance of these hosts in competition or predator-prey interactions with other species. Second, the indirect effects of parasites on the behaviour of their hosts, e.g. burrowing ability or spatial distribution within the intertidal zone, can cause changes to various features of the habitat for other intertidal species, leading to their greater settlement success or to their local disappearance. Our synthesis allows specific predictions to be made regarding the potential impact of parasites in certain intertidal systems, and suggests that parasites must be included in future community studies and food web models of intertidal ecosystems.

The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms.

The New Zealand cockle Austrovenus stutchburyi, whose foot is commonly infected by the digenean trematode Curtuteria australis (Echinostomatidae), is often found heavily infected and unable to burrow on the sediment surface of tidal flats. This has been interpreted as a Curtuteria-manipulation with the purpose of increasing the transmission of the parasite to shorebirds acting as final hosts. Using a field-experimental approach the alternative hypothesis was tested, that surface-dwelling cockles, caught on the surface for other reasons than parasites, accumulate larval C. australis at a higher rate than buried cockles. During the 3-month experiment, larval trematodes accumulated with a rate of approximately 0.5 metacercariae/day in both surface and buried cockles. The result strengthens the manipulation hypothesis indirectly by rejecting the alternative hypothesis. The metacercariae were unevenly distributed along the cockle-foot, with about 4 times as many cysts being found in the tip than in either the mid or hind part of the foot. In light of existing knowledge of the burrowing behaviour and apparatus in bivalves, and a negative relationship between foot mobility and infection intensity, it is suggested that C. australis manipulates its host through a mechanical obstruction of foot muscles and the dynamic hydrostatic skeleton, both necessary for successful burrowing.

Hitch-hiking parasite: a dark horse may be the real rider.

Many parasites engaged in complex life cycles manipulate their hosts in a way that facilitates transmission between hosts. Recently, a new category of parasites (hitch-hikers) has been identified that seem to exploit the manipulating effort of other parasites with similar life cycle by preferentially infecting hosts already manipulated. Thomas et al. (Evolution 51 (1997) 1316) showed that the digenean trematodes Microphallus papillorobustus (the manipulator) and Maritrema subdolum (the hitch-hiker) were positively associated in field samples of gammarid amphipods (the intermediate host), and that the behaviour of Maritrema subdolum rendered it more likely to infect manipulated amphipods than those uninfected by M. papillorobustus. Here I provide experimental evidence demonstrating that M. subdolum is unlikely to be a hitch-hiker in the mentioned system, whereas the lucky candidate rather is the closely related but little known species, Microphallidae sp. no. 15 (Parassitologia 22 (1980) 1). As opposed to the latter species, Maritrema subdolum does not express the appropriate cercarial behaviour for hitch-hiking.