Parasite Induced Summer Mortality in the Cockle Cerastoderma edule by the Trematode Gymnophallus choledochus

In late summer 2004, a conspicuous cockle (Cerastoderma edule) mortality event was observed on a tidal flat in the northern Wadden Sea (North Sea, Germany) with many fresh valves and still living cockles lying on the sediment surface. To investigate whether trematode parasites utilizing the cockle as first or second intermediate host were involved in this mortality, buried and surfaced cockles were sampled and analyzed, and a laboratory experiment conducted. The field survey showed no statistical difference in intensity of parasites encysted in the foot of cockles. Three species of Himasthla utilizing the cockle as second intermediate host and known to impair the cockle’s burrowing ability were found in buried cockles with 148.4±111.1 metacercariae/foot and in surfaced cockles with 164.2±84.4. There was also no difference in infection levels of parasites utilizing the cockles as second intermediate host in other cockle tissues between buried and surfaced cockles. In contrast, surfaced cockles showed a ten times higher prevalence (71.0%) than buried cockles (7.4%) of the trematode Gymnophallus choledochus – a parasite utilizing the cockle as first (and second) intermediate host – filling almost the entire body cavity and eliminating gonad structures. In an aquarium experiment of 14 days, all cockles found buried on the tidal flat survived compared to only 23.3% found on the surface. This suggests G. choledochus to be a castrating agent and a serious mortality factor in adult cockle populations.     

Inertia of parasite infection versus host biomass fluctuation

Infection by parasites with complex life cycles such as trematodes depends on many environmental factors which may result in a time-lag between host biomass fluctuations and parasite density in hosts. A cockle (marine bivalve, second intermediate host) population and its associated parasite community were monitored over 15 years. A time-shift correlation analysis suggests that trematode abundance in cockles responds to cockle biomass after a long delay (8 year time-lag). Thus, these parasites can sustainably support a deficit of their intermediate host.     

Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone?

Understanding the influence of parasites on the community ecology of free-living organisms is an emerging theme in ecology. The cockle Austrovenus stutchburyi is an abundant mollusc inhabiting the sheltered shores of New Zealand. This species, which lives just few centimetres under the surface, plays a key role for many benthic invertebrate species, because in these habitats the cockle shell is the only available hard surface where invertebrates can establish. However, the behaviour of this cockle can be altered locally by a parasite, the trematode Curtuteria australis. Indeed, heavily infected cockles are unable to bury perfectly and typically lie entirely exposed at the surface of the mud. In this study, we investigated the ecological consequences of this behavioural alteration for two invertebrates species commonly associated with cockles, the anemone Anthopleura aureoradiata and the limpet Notoacmea helmsi. A field study first demonstrated that in both infected and non-infected populations of cockles, there was a negative relationship between the number of anemones and limpets found on cockles. In the laboratory, we showed that predation of limpets by anemones is possible when they share the same cockle shell. In a heavily infected population of cockles, limpets were significantly more frequent and more abundant on cockles manipulated by C. australis than on cockles with a normal behaviour. A colonization test conducted in natural conditions demonstrated that the predominance of limpets on manipulated cockles results from a direct habitat preference. Conversely, anemones were significantly less frequent and less abundant on manipulated cockles than on cockles manipulated by C. australis. A desiccation test revealed that, relative to limpets, they had a lower resistance to this physical stress. We discuss our results in relation to current ideas on ecosystem engineering by organisms.     

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.     

Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare

Parasites with complex life cycles, relying on trophic transmission to a definitive host, very often induce changes in the behaviour or appearance of their intermediate hosts. Because this usually makes the intermediate host vulnerable to predation by the definitive host, it is generally assumed that the parasite's transmission rate is increased, and that the modification of the host is, therefore, of great adaptive significance to the parasite. However, in the ecological "real world" other predators unsuitable as hosts may just as well take advantage of the facilitation process and significantly erode the benefit of host manipulation. Here we show that the intertidal New Zealand cockle (Austrovenus stutchburyi), manipulated by its echinostome trematode (Curtuteria australis) to rest on the sediment surface fully exposed to predation from the avian definitive host, is also subject to sublethal predation from a benthic feeding fish (Notolabrus celidotus, Labridae). The fish is targeting only the cockle-foot, in which the parasite preferentially encysts, reducing the infection intensity of manipulated cockles to levels comparable with those in non-manipulated, buried cockles. Based on the frequency and intensity of the foot cropping and predation rates on surfaced cockles by avian hosts, it is estimated that 2.5% of the parasite population in manipulated cockles is transmitted successfully whereas 17.1% is lost to fish. We argue that the adaptive significance of manipulation in the present system depends critically on the feeding behaviour of the definitive host. If cockles constitute the majority of prey items, there will be selection against manipulation. If manipulated cockles are taken as an easily accessible supplement to a diet composed mostly of other prey organisms, behavioural manipulation of the cockle host appears a high risk, high profit transmission strategy. Both these feeding behaviours of birds are known to occur in the field.     

Cockle emergence at the sediment surface: 'favourization' mechanism by digenean parasites?

The aim of the present work was to assess the effect of digenean trematodes on indirect mortality of the cockle Cerastoderma edule, an infaunal bivalve. The tested hypothesis was that parasites altered the burrowing capacity of cockles and thus exposed them at the sediment surface, where they are more vulnerable to predators. If the predator is the final host, this mechanism, which drives the cockle out of the sediment, is considered as a 'favourization'. Cockle populations from 2 stations in Arcachon Bay (France)-Banc d'Arguin (oceanic situation) and La Canelette (lagoonal situation)--were sampled for 1 yr. At La Canelette, monitoring every 2 d showed that 50% of adult cockles regularly migrated to the sediment surface at a rate of 5 cockles m(-2) yr(-1) and disappeared in a few days. In the laboratory, 67% of these 'surface cockles' did not burrow again, suggesting that they would die in the field. Moreover, mortality measured after 7 d in the laboratory was 2 to 5 times higher than mortality of 'buried cockles', at both stations and particularly during summer. Species richness and abundance of digeneans from both stations were compared in 'buried' and 'surface' individuals to determine whether parasites played a role in cockle migration and mortality. Ten and 9 digeneans were found at Banc d'Arguin and La Canelette, respectively, with Himasthla quissetensis and Labratrema minimus being the most prevalent and abundant species at both stations. The abundance of H. quissetensis was slightly higher in surface cockles at Banc d'Arguin, but the difference fluctuated with station and cockle age (or size). L. minimus prevalence was only higher in surface cockles at La Canelette. In the latter station, we estimated that L. minimus and H. quissetensis were responsible for the emergence of 9 and 2%, respectively, of the buried cockles. Although this favourization mechanism may induce some mortality in cockles, it does not alone explain the magnitude of the observed mortalities (41 and 57% at La Canelette and Banc d'Arguin, respectively). A correspondence analysis did not show the presence of a particular parasite community in buried or surface cockles, which could explain these high surface cockle mortalities in association with the 2 dominant digeneans.     

Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve

Spatial heterogeneities in the abundance of free-living organisms as well as in infection levels of their parasites are a common phenomenon, but knowledge on parasitism in invertebrate intermediate hosts in this respect is scarce. We investigated the spatial pattern of four dominant trematode species which utilize a common intertidal bivalve, the cockle Cerastoderma edule, as second intermediate host in their life cycles. Sampling of cockles from the same cohort at 15 sites in the northern Wadden Sea (North Sea) over a distance of 50 km revealed a conspicuous spatial heterogeneity in infection levels in all four species over the total sample as well as among and within sampling sites. Whereas multiple regression analyses indicated the density of first intermediate upstream hosts to be the strongest determinant of infection levels in cockles, the situation within sites was more complex with no single strong predictor variable. However, host size was positively and host density negatively correlated with infection levels and there was an indication of differential susceptibility of cockle hosts. Small-scale differences in physical properties of the habitat in the form of residual water at low tide resulted in increased infection levels of cockles which we experimentally transferred into pools. A complex interplay of these factors may be responsible for within-site heterogeneities. At larger spatial scales, these factors may be overridden by the strong effect of upstream hosts. In contrast to first intermediate trematode hosts, there was no indication for inter-specific interactions. In other terms, the recruitment of trematodes in second intermediate hosts seems to be largely controlled by pre-settlement processes both among and within host populations.     

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.     

A trade-off between energy intake and exposure to parasites in oystercatchers feeding on a bivalve mollusc.

Models of animal dispersion between habitat patches that differ in resource density assume that animals maximize their fitness by maximizing the rate at which they consume resources. How valid is this assumption? Studies on wading birds have been central to the application of dispersion models to predator-prey systems. However, these birds do not always attempt to maximize their rate of energy intake, implying that maximization involves costs as well as benefits. Overwintering oystercatchers feeding on cockles in the Burry Inlet, South Wales, do not consume the larger more energetically profitable cockles even though consuming these prey would increase their rate of energy intake. This paper tests the hypothesis that maximizing energy intake involves a trade-off with exposure to helminth parasites. Cockles are important intermediate hosts for helminth parasites, for which oystercatchers are the definitive host. The helminth intensity of cockles increased significantly with cockle size. A functional response model was used to examine how size selection by the birds influenced energy intake and the ingestion rate of parasites. To maximize energy intake birds should selectively consume the larger size classes, but to minimize the ingestion rate of parasites they should consume the smallest size classes. In the wild, birds selectively consumed intermediate size classes, which could represent a compromise between these conflicting demands. The implications for animal dispersion models are discussed.     

Ambient fauna impairs parasite transmission in a marine parasite-host system

To understand possible factors controlling transmission of trematode larvae between first and second intermediate hosts we examined the impact of ambient fauna on parasite transmission in a marine intertidal parasite-host association. Cockle hosts (Cerastoderma edule) kept together with selected co-occurring macrozoobenthic species in mesocosms acquired a lower parasite load compared to cockles kept alone, when targeted by cercariae of the trematode Himasthla elongata. The reduction of parasite load in the cockles differed between the 7 macrozoobenthic species tested and was between 35 and 91%. Three different types of reduction could be distinguished: (1) predators (Carcinus maenas, Crangon crangon) actively preying upon cercariae, (2) non-host filter feeders (Crepidula fornicata, Mya arenaria, Crassostrea gigas) filtering cercariae but not becoming infected and (3) alternative hosts (Mytilus edulis, Macoma balthica) becoming infected by the cercariae and thus distracting cercariae from the target hosts. In addition, interference competition may occur in the form of disturbance of cockles by ambient organisms resulting in lower filtration rates and subsequently lower parasite loads. Our results suggest that the species composition and relative abundance of the ambient fauna of parasite-host systems play an important role in controlling trematode transmission rates in benthic marine systems.     

Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae)

Marine bivalves harbour a diversity of trematode parasites affecting population and community dynamics of their hosts. Although ecologically and economically important, factors influencing transmission between first (snail) and second (bivalve) intermediate hosts have rarely been studied in marine systems. In laboratory experiments, the effect of temperature (10, 15, 20, 25 degrees C) was investigated on (1) emergence from snails, (2) survival outside hosts and (3) infectivity in second intermediate hosts of cercariae of the trematode Renicola roscovita (Digenea: Renicolidae), a major parasite in North Sea bivalves. Emergence of cercariae peaked at 20 degrees C (2609 +/- 478 cercariae snail(-1) 120 h(-1)) and was considerably lower at 10 degrees C (80 +/- 79), 15 degrees C (747 +/- 384) and 25 degrees C (1141 +/- 334). Survival time decreased with increasing temperature, resulting in 50% mortality of the cercariae after 32.8 +/- 0.6 h (10 degrees C), 26.8 +/- 0.8 h (15 degrees C), 20.2 +/- 0.5 h (20 degrees C) and 16.6 +/- 0.3 h (25 degrees C ). Infectivity of R. roscovita cercariae in cockles Cerastoderma edule increased with increasing temperature and was highest at 25 degrees C (42.6 +/- 3.9%). However, mesocosm experiments with infected snails and cockle hosts in small aquaria, integrating cercarial emergence, survival and infectivity, showed highest infection of cockles at 20 degrees C (415 +/- 115 metacercariae host(-1)), indicating 20 degrees C to be the optimum temperature for transmission of this species. A field experiment showed metacercariae of R. roscovita to appear in C. edule with rising water temperature in April; highest infection rates were in August, when the water temperature reached 20 degrees C. Since another trematode species (Himasthla elongata; Digenea: Echinostomatidae) occurring at the experimental site showed a similar temporal pattern, trematode transmission to second intermediate bivalve hosts may peak during especially warm (> or = 20 degrees C) summers in the variable climate regime of the North Sea.     

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.     

Infection of the cockle Cerastoderma edule in the Baie des Veys (France) by the microsporidian parasite Steinhausia sp

We report the occurrence of the microsporidian parasite Steinhausia sp. in the oocytes of the common cockle Cerastoderma edule in a natural population in France, where high mortalities occurred. Steinhausia sp. appeared primarily as sporocysts containing many small spores, and putative earlier developmental stages were also observed. Both its prevalence and infection intensity were low, and no host defence reaction was recognized, suggesting that Steinhausia sp. had no detrimental effect on C. edule. Its prevalence was higher in cockles lying on the sediment surface, but the significance of this observation could not be explained given the poor knowledge of the Steinhausia life cycle. The present data did not allow specific identification of the parasite, and further studies are required to determine whether Steinhausia sp. in the cockle is a new species, or a microsporidian infecting multiple host species.     

Intra-host competition between co-infecting digeneans within a bivalve second intermediate host: Dominance by priority-effect or taking advantage of others?

We experimentally investigated the interactions between two parasites known to manipulate their host's phenotype, the trematodes Acanthoparyphium sp. and Curtuteria australis, which infect the cockle Austrovenus stutchburyi. The larval stages of both species encyst within the tissue of the bivalve's muscular foot, with a preference for the tip of the foot. As more individuals accumulate at that site, they impair the burrowing behaviour of cockles and increase the probability of the parasites' transmission to a bird definitive host. However, individuals at the foot tip are also vulnerable to non-host predators in the form of foot-cropping fish which selectively bite off the foot tip of exposed cockles. Parasites encysted at the foot base are safe from such predators although they do not contribute to altering host behaviour, but nevertheless benefit from host manipulation as all parasites within the cockle are transmitted if it is ingested by a bird. Experimental infection revealed that Acanthoparyphium sp. and C. australis have different encystment patterns within the host, with proportionally fewer Acanthoparyphium metacercariae encysting at the foot tip than C. australis. This indicates that Acanthoparyphium may benefit indirectly from C. australis and incur a lower risk of non-host predation. However, in co-infections, not only did C. australis have higher infectivity than Acanthoparyphium, it also severely affected the latter's infection success. The asymmetrical strategies and interactions between the two species suggest that the advantages obtained from exploiting the host manipulation efforts of another parasite might be offset by traits such as reduced competitiveness in co-infections.     

Influence of disseminated neoplasia, trematode infections and gametogenesis on surfacing and mortality in the cockle Cerastoderma edule

Cerastoderma edule is a widely distributed bivalve mollusc, commercially exploited throughout Europe and is also an important food source for birds and crustaceans. Recently, mass surfacing and mortalities of cockles have been observed and reported at sites in Ireland and elsewhere, particularly in the summer months. One such site is Flaxfort Strand, Courtmacsherry Bay, County Cork, Ireland, an important feeding area used by many seabirds during the summer months. For the past few years large numbers of surfaced cockles have been observed at the site in a moribund condition. Samples of cockles from this area were collected over the summer months and their health status assessed. Cockles that had surfaced (moribund) and those still buried in the sediment were quantified and screened: sex, gonadal maturity and size class of cockles were also determined. Disseminated neoplasia and trematodes were observed in screened cockles. The most significant finding during the study was that mortalities and surfacing of cockles was related to a greater incidence of disseminated neoplasia. No neoplasia was observed in the smallest and largest size classes. There was a significantly higher prevalence of neoplasia in moribund cockles than in buried cockles, whereas in both groups a similar concentration of trematode metacercariae was observed in the screened tissues. Also, most of the cockles that had surfaced were either in the process of spawning or were spent. Overall a much larger percentage of moribund cockles exhibited both trematode infections plus neoplasia compared with buried cockles. A combination of the presence of neoplasia and trematodes, along with stress related to spawning, may immunocompromise the cockless, causing the animals to surface and become moribund.     

Environmental parasitology: What can parasites tell us about human impacts on the environment?

There are a variety of ways that environmental changes affect parasites, suggesting that information on parasites can indicate anthropogenic impacts. Parasitism may increase if the impact reduces host resistance or increases the density of intermediate or definitive hosts. Parasitism may decrease if definitive or intermediate host density declines or parasites suffer higher mortality directly (eg. from toxic effects on parasites) or indirectly (infected hosts suffer differentially high mortality). Although these scenarios are opposing, they can provide a rich set of predictions once we understand the true associations between each parasite and impact. In this review, Kevin Lafferty discusses how parasite ecologists have used and can use parasites to assess environmental quality.     

The combined influence of trematode parasites and predatory salamanders on wood frog (<Emphasis Type="Italic">Rana sylvatica</Emphasis>) tadpoles

Predators can have important impacts on host–parasite dynamics. For many directly transmitted parasites, predators can reduce transmission by removing the most heavily infected individuals from the population. Less is known about how predators might influence parasite dynamics in systems where the parasite relies on vectors or multiple host species to complete their life cycles. Digenetic trematodes are parasitic flatworms with complex life cycles typically involving three host species. They are common parasites in freshwater systems containing aquatic snails, which serve as obligate first intermediate hosts, and multiple trematode species use amphibians as second intermediate hosts. We experimentally examined the impact of predatory salamanders (Ambystoma jeffersonianum) and trematode parasites (Echinostoma trivolvis and Ribeiroia ondatrae) on short-term survival of wood frog tadpoles (Rana sylvatica) in 150-L outdoor pools. Two trematode species were used in experiments because field surveys indicated the presence of both species at our primary study site. Parasites and predators both significantly reduced tadpole survival in outdoor pools; after 6 days, tadpole survival was reduced from 100% in control pools to a mean of 46% in pools containing just parasites and a mean of 49% in pools containing just predators. In pools containing both infected snails and predators, tadpole survival was further reduced to a mean of 5%, a clear risk-enhancement or synergism. These dramatic results suggest that predators may alter transmission dynamics of trematodes in natural systems, and that a complete understanding of host–parasite interactions requires studying these interactions within the ecological framework of community interactions.     

Latitudinal influence on gametogenesis and host–parasite ecology in a marine bivalve model

Reproduction and parasites have significant impacts on marine animal populations globally. This study aimed to investigate the associative effects of host reproduction and a host–parasite interplay on a marine bivalve, along a geographic gradient of latitude. Cockles Cerastoderma edule were sampled from five European sites (54°N to 40°N), between April 2018 and October 2019. A histological survey provided data on trematode (metacercaria and sporocyst life stages), prevalence, and cockle stage of gametogenesis to assess the influence of a latitudinal gradient on both interplays. Sex ratios at the northernmost sites were skewed toward females, and spawning size was reduced at the lower latitudes. Trematode infection did not follow a latitudinal gradient. Localized site‐related drivers, namely seawater temperature, varied spatially, having an impact on cockle–trematode interactions. Spawning was related to elevated temperatures at all sites. Prolonged spawning occurred at southern latitudes, where seawater temperatures were warmer. Trematode prevalence and the impact of trematodes on gametogenesis were found to be spatially variable, but not latitudinally. Therefore, it is not possible to determine the likelihood of boom and bust events in cockles, based on the latitudinal location of a population. In terms of sublethal impacts, it appeared that energy was allocated to reproduction rather than somatic growth in southern populations, with less energy allocated to reproduction in the larger, northern cockles. The demonstrated spatial trend of energy allocation indicates the potential of a temporal trend of reduced cockle growth at northern sites, as a result of warming sea temperatures. This awareness of the spatially varying drivers of populations is crucial considering the potential for these drivers/inhibitors to be exacerbated in a changing marine environment.     

Prey depletion and foraging strategy in the Oystercatcher Haematopus ostralegus

Summary The responses of a population of Oystercatchers to their own depletion of their prey, the edible cockle Cerastoderma edule, have been examined in Strangford Lough, Northern Ireland., Cockle stocks were severely depleted each winter as a result of predation by Oystercatchers and about half the birds present in October in the main study area had left by March: the reduction was greater when the initial population of Oystercatchers was high than when it was low. Oystercatchers were initially widespread around the Lough but tended to aggregate by January into a few good sites. Within each site annual differences in the location of feeding effort were correlated with year to year variation in the location of second winter cockles.Within the feeding areas in a bay the birds apparently hunted in the short-term on the basis of expectation, ceasing to crop, the densest cockle beds once an average yield for the area has been removed; this yield was apparently estimated from the local density of the anvils on which captured cockles were broken open. This effect led to marginal areas being depleted of cockles more rapidly than high density areas, so that the birds gradually concentrated their hunting onto an increasingly restricted area of the bay. The birds initially took only second winter and larger cockles but by late winter cockle densities had fallen so much that smaller cockles were accepted: areas previously abandoned or unused for hunting were then economically viable because of the reduced expectations of the birds and were incorporated into the feeding areas.These results are seen as consistent with Royama's profitability theory.     

Conditional Responses of Benthic Communities to Interference from an Intertidal Bivalve

Habitat-modifying organisms that impact other organisms and local functioning are important in determining ecosystem resilience. However, it is often unclear how the outcome of interactions performed by key species varies depending on the spatial and temporal disturbance context which makes the prediction of disturbance-driven regime shifts difficult. We investigated the strength and generality of effects of the filter feeding cockle Cerastoderma edule on its ambient intertidal benthic physical and biological environment. By comparing the magnitude of the effect of experimental cockle removal between a non-cohesive and a sheltered cohesive sediment in two different periods of the year, we show that the outcome of cockle interference effects relates to differences in physical disturbance, and to temporal changes in suspended sediment load and ontogenetic changes in organism traits. Interference effects were only present in the cohesive sediments, though the effects varied seasonally. Cockle presence decreased only the density of surface-dwelling species suggesting that interference effects were particularly mediated by bioturbation of the surface sediments. Furthermore, density reductions in the presence of cockles were most pronounced during the season when larvae and juveniles were present, suggesting that these life history stages are most vulnerable to interference competition. We further illustrate that cockles may enhance benthic microalgal biomass, most likely through the reduction of surface-dwelling grazing species, especially in periods with high sediment load and supposedly also high bioturbation rates. Our results emphasize that the physical disturbance of the sediment may obliterate biotic interactions, and that temporal changes in environmental stressors, such as suspended sediments, may affect the outcome of key species interference effects at the local scale. Consequently, natural processes and anthropogenic activities that change bed shear stress and sediment dynamics in coastal soft-sediment systems will affect cockle-mediated influences on ecosystem properties and therefore the resilience of these systems to environmental change.