Kim N. Mouritsen

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.

Parasites Affect Food Web Structure Primarily through Increased Diversity and Complexity

Parasites primarily affect food web structure through changes to diversity and complexity. However, compared to free-living species, their life-history traits lead to more complex feeding niches and altered motifs.

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.

DESCRIPTION AND PROPOSED LIFE CYCLE OF MARITREMA NOVAEZEALANDENSIS N. SP. (MICROPHALLIDAE) PARASITIC IN RED-BILLED GULLS, LARUS NOVAEHOLLANDIAE SCOPULINUS, FROM OTAGO HARBOR, SOUTH ISLAND, NEW ZEALAND

Maritrema novaezealandensis n. sp. is described from Otago Harbor, South Island, New Zealand, on the basis of adult specimens collected from the Red-billed gull, Larus novaehollandiae scopulinus, and excysted metacercariae obtained from crabs. It belongs to the “eroliae group” and differs from other related species mainly in the shape, size, and patterns of distributions of the spines on the cirrus, the shape of the metraterm, the presence of an unlobed ovary, and the complete ring of the vitelline follicles. Based on morphometric features of metacercariae and adult specimens, the trophic relationships among invertebrate and vertebrate hosts, experimental infections, and previous reports of species of Maritrema with similar transmission patterns, the life cycle of M. novaezealandensis n. sp. is described. A 3-host life cycle is proposed for this parasite. The first intermediate host is the mud snail, Zeacumantus subcarinatus, in which the cercarial stage is produced in sporocysts located within the gonad of the snail. At least 3 crab species (Hemigrapsus crenulatus, Macrophtalmus hirtipes, and Halicarcinus whitei) and several species of amphipods act as second intermediate hosts, with metacercariae encysted in the body cavity of the crustacean host. Finally, the definitive host, the gull, L. n. scopulinus, harbors the adult worms in its intestine.

Climate warming may cause a parasite-induced collapse in coastal amphipod populations

Besides the direct impact on the general performance of individual organisms, the ecological consequences of climate change in terrestrial and marine ecosystems are expected to be determined by complex cascading effects arising from modified trophic interactions and competitive relationships. Recently, the synergistic effect of parasitism and climate change has been emphasised as potentially important to host population dynamics and community structure, but robust empirical evidence is generally lacking. The amphipod Corophium volutator is an ecologically important species in coastal soft-bottom habitats of the temperate North Atlantic, and commonly serves as host to microphallid trematodes that cause intensity-dependent and temperature-dependent mortality in the amphipod population. Using a simulation model parameterised with experimental and field data, we demonstrate that a 3.8°C increase in ambient temperature will likely result in a parasite-induced collapse of the amphipod population. This temperature increase is well within the range predicted to prevail by the year 2075 in the International Wadden Sea region from where the model data are obtained. Due to the amphipods’ ecological importance, their population decline may impact the coastal ecosystem as a whole.

Change of topography and sediment characteristics on an intertidal mud-flat following mass-mortality of the amphipod Corophium volutator

A Corophium-bed characterized by a mosaic of emerged areas and tidal pools during low water was established on an intertidal flat in the southern part of the Danish Wadden Sea. In spring 1990, the plateaux harboured relatively high densities of the amphipod Corophium volutator , whereas the amphipods were almost absent in the pools. Following a parasite-induced mass-mortality in the population of Corophium , summer 1990, the plateaux of the bed were subjected to sediment erosion. The heterogeneous plateau-pool structure disappeared, accompanied by increased median particle diameter and decreased silt content in the former plateau sediment. These events were accompanied by increased chlorophyll- a concentrations in the sediment of both plateau and pool areas. The results suggest Corophium volutator to be the single most important organism stabilizing the plateau sediment, and hence, the heterogeneous topographic structure of the Corophium -bed. It is proposed that the stabilizing effect of Corophium burrows also in deeper sediment strata may outweigh the surface stabilizing influence of epipelic diatoms, as well as the negative effect of amphipods eating the diatoms, in non-cohesive coarser sediments.

Enhanced erodibility of fine-grained marine sediments by Hydrobia ulvae

The common mud snail Hydrobia ulvae is a widespread and dominant deposit feeder on fine-grained substrata along the European Atlantic coastline. Previous studies have shown that mud snail activities such as grazing, faecal pellet production and mucous production may influence physical properties of the surface sediment layer and thus depositional and erosional processes. To quantify the influence of Hydrobia density on key parameters such as erosion threshold and erosion rate, a shortterm laboratory experiment was conducted. Snails were placed on fine-grained sediment at densities of 10000 and 50000 ind m 2 and erosion experiments were carried out one, three and five days after establishment of the sediment beds. Controls without H. ulvae were treated the same way. The presence of H. ulvae significantly increased the erosion rate and decreased the erosion threshold compared to snail-free control plots. The erosion rate was increased by a factor of 2 to 4 when H. ulvae were present and showed stronger influence by the snail than the erosion threshold. Snail density did not affect the erosion threshold, but the erosion rate doubled with an increase in density from 10000 to 50000 ind m 2 . The erosion rate was only marginally different after one day but the difference increased over time and the erosion rate was significantly different for all treatments after five days. No significant time dependence was observed for the erosion threshold. The results generally confirm results obtained in situ and differences can be related to different hydrodynamic conditions under field and laboratory conditions. D 2002 Elsevier Science B.V. All rights reserved.

The mud flat anemone-cockle association: mutualism in the intertidal zone?

The intertidal cockle Austrovenus stutchburyi exists in a symbiotic relationship with the mud flat anemone Anthopleura aureoradiata, the latter using the shell of buried cockles as the only available hard substrate for attachment. The cockles are also host to a detrimental larval trematode Curtuteria australis that invades the bivalves through the filtration current, and here we demonstrate that the anemones significantly depress the rate by which cockles accumulate parasites in the field. Along the tidal gradient, the relative parasite load of cockles was lowest where anemones were most abundant, and the area occupied by anemones per square meter sediment surface explained 30% of the spatial variation in infection intensity. At a smaller spatial scale, parasite loads were significantly lower (34%) in cockles from patches with than without anemones at the same tidal height. A field experiment manipulating the density of anemones showed that the rate of parasite accumulation in cockles decreased with increasing anemone density, and that the generally positive relationship between infection intensity and cockle size tended to disappear in the presence of anemones. The results suggest that the anemone-cockle symbiosis is a non-obligate mutualistic relationship in which the former is provided with a suitable substrate for attachment whereas the latter obtains protection against parasitic infections.

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.

The influence of the trematode Microphallus claviformis on two congeneric intermediate host species (Corophium): infection characteristics and host survival

In a laboratory experiment the survival of two amphipod species Corophium volutator and C. arenarium was differentially affected by the digenetic trematode Microphallus claviformis, the former suffering from parasite induced mortality. No clear species specific parasite preference was observed, but there was a difference between the two frequency distributions of parasite number per host, indicating a preference for the competitively superior C. volutator. In both species the parasite metapopulation was overdispersed, but to the highest degree in C. volutator. Formation of a penetration cyst on the Corophium cuticle preceeds the penetration of the M. claviformis cercariae, a common feature of microphallid digeneans, but not earlier reported from this species. Dead individuals of both species carried significantly more penetration cysts than the live ones which suggests that massive invasion of cercariae during a short period of time is the cause of death of Corophium, rather than crude parasite intensity. The potential for M. claviformis to act as a structuring agent in communities of Corophium species is discussed.