Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects

Parasitism has long been emphasised as an important process structuring animal communities. However, empirical evidence documenting the impact of parasites in other than simple laboratory settings is lacking. Here we examine the trait-mediated indirect effects of echinostome trematodes on a New Zealand soft bottom intertidal community of macroinvertebrates. Curtuteria australis and a second related but undescribed trematode both utilise the cockle Austrovenus stutchburyi as second intermediate host in which the parasites infect the foot tissue. Heavily infected cockles are therefore more sessile than lightly infected individuals, and, unable to bury, often rest on the sediment surface. We utilised these behavioural changes in two long term field experiments, respectively manipulating the parasite load of buried cockle (i.e. bioturbation), and the density of surfaced cockles (i.e. surface structures and seabed hydrodynamics). Both high parasite loads in buried cockles and the presence of surfaced cockles increased species richness and generally also the density of certain species and of major systematic and functional groups of benthic macroinvertebrates. Species diversity (alpha) peaked under intermediate densities of surfaced cockles. Our results demonstrate that parasites, solely through their impact on the behaviour of a single community member, can be significant determinants of animal community structure and function.     

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.     

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.     

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.     

Der bemerkenswerte Lebenszyklus des marinen VogeltrematodenGymnophallus choledochus

Summary Two species of trematodes occur in the gall-bladder of European Laro-Limicolae and Anatids. One of them,Gymnophallus deliciosus, is fairly rare in the North Sea area. The second one,G. choledochus, is very common. Its length is about 1 mm, it may live up to several months and in heavy infections causes severe pathogenic changes in the gall-bladder.This fluke has a peculiar life-history in which two kinds of trematode life-cycles are combined with each other. The first intermediate host ofG. choledochus is the cockle. In it the sporocysts — simple sac-like trematode larvae — give rise to fork-tailed cercariae leaving the cockle in spring and summer, penetrating in polycheats where they become infectious metacercariae. Eating the polychaets the bird, such as gull or wader, becomes infected with the fluke. So far this life-cycle represents a normal type of trematode life-history. In the other part of the year, though, a shortened development-cycle is adopted. In late autumn and winter the cercariae in the sporocysts loose their tails and as metacercariae remain there until the cockle gets eaten by a suitable host.The biological purpose of these two alternative cycles is evident. In the first cycle which is the primary one in evolution only worm-eating birds could be infected. Then the second cycle developed in which the cockle remained the only intermediate host. With this step bivalve-eating birds can be infected, too. From the fact thatG. choledochus is not yet adapted very well to Anatids can be seen that the shortened winter cycle is the younger one. Though eating much more bivalves than do gulls or waders less trematodes develope in Anatids and most of them do not become adult but remain small and immature.

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Herrn Prof. Dr. Erwin Stresemann zum 80. Geburtstag     

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.     

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.     

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.     

Genetics,intensity‐dependence,and host manipulation in the trematode Curtuteria australis: following the strategies of others?

Manipulation of host phenotype by parasites can require a collective effort from many individuals. The cost of manipulation may only be paid by the individuals actually inducing the manipulation, while its benefits are reaped by all. Here, we determine if there is genetic variation in manipulative effort among different clonal lineages of the trematode Curtuteria australis, and whether the decision to manipulate is context‐dependent. C. australis impairs the burrowing efficiency of its second intermediate host, the cockle Austrovenus stutchburyi, by encysting at the tip of the cockle's foot, which facilitates the parasite's trophic transmission to shorebirds. However, manipulative individuals at the tip of the foot are vulnerable to non‐host predators (foot‐cropping fish); in contrast, those encysted at the base of the foot, although they do not contribute to manipulation, are safe from foot‐croppers and can benefit from altered host phenotype. In an experimental study, different clonal lineages showed no significant variation in their tendency to encyst in the tip versus the base of the foot, with only the former contributing to host manipulation. However, the decision to manipulate was intensity‐dependent: the greater the number of parasites already committed to manipulation (i.e. already encysted in the foot tip), the more likely newly arriving parasites were to join them. These findings indicate considerable intraspecific variation in the strategies adopted by ‘manipulator’ parasites, with external influences determining what a parasite actually does.     

The intertidal zoning of cockles (<Emphasis Type="Italic">Cerastoderma edule</Emphasis>) in the Wadden Sea,or why cockle fishery disturbed areas of relatively high biodiversity

Recently, Kraan et al. (ICES J Mar Sci 64:1735–1742, 2007) reported that areas in the Wadden Sea selected by mechanical cockle dredgers were of greater zoobenthic diversity than areas that remained undredged. The present paper attempts to explain this observation, focussing on the elevation-related zoning of the macrobenthic fauna on tidal flats. Dense beds of cockles Cerastoderma edule occur in a specific intermediate intertidal-height zone where more species are present (and reach their maximal abundance) than in either lower or higher zones. This coincidence of preferred intertidal zones in many species, including cockles, may cause the higher species richness (and higher total macrozoobenthic biomass) of the fisher-chosen dredging areas as compared to other nearby non-dredged tidal-flat areas.     

Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp

The complex life cycle of digenean trematodes with alternating stages of asexual multiplication and sexual reproduction can generate interesting within-host population genetic patterns. Metacercarial stages found in the second intermediate host are generally accumulated from the environment. Highly mobile second intermediate hosts can sample a broad range of cercarial genotypes and accumulate genetically diverse packets of metacercariae, but it is unclear whether the same would occur in systems where the second intermediate host is relatively immobile and cercarial dispersal is the sole mechanism that can maintain genetic homogeneity at the population level. Here, using polymorphic microsatellite markers, we addressed this issue by genotyping metacercariae of the trematode Gymnophallus sp. from the New Zealand cockle Austrovenus stutchburyi. Despite the relatively sessile nature of the second intermediate host of Gymnophallus, very high genotypic diversity of metacercariae was found within cockles, with only two cockles harbouring multiple copies of a single clonal lineage. There was no evidence of population structuring at the scale of our study, suggesting the existence of a well-mixed population. Our results indicate that (i) even relatively sessile second intermediate hosts can accumulate a high diversity of genotypes and (ii) the dispersal ability of cercariae, whether passive or not, is much greater than expected for such small and short-lived organisms. The results also support the role of the second intermediate host as an accumulator of genetic diversity in the trematode life cycle.     

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.     

An estimate of the sustainable rate of shell extraction from the Dutch Wadden Sea

1. Shell production by cockles Cerastoderma edule was studied to examine whether or not the present licensed rate of shell extraction in the Dutch Wadden Sea exceeds the current rate of shell addition to the exploitable stocks.
2. Long-term data on numbers of cockles and weights of their shells were used to estimate their annual production on Balgzand, a 50-km² tidal flat area in the western-most part of the Wadden Sea. During the 1969–97 period, it amounted to an average of 125 g m^–2, including 107 g m^–2 of shells large enough to be exploitable for shell-lime fishery.
3. The very irregular annual recruitment of cockles was the main cause of the wide 95% confidence limits (74 and 140 g m^–2 year^–1) of this 28-year estimate. Moreover, high mortality rates in severe winters substantially reduced production per recruit in some year classes.
4. About one-third of the estimated production does not reach exploitable stocks, because it is fragmented by birds (particularly eider ducks), permanently buried in the sediment, or removed by the fishery for live cockles.
5. During the last few decades, the estimated mean amount added annually to the exploitable stocks was 88 million kg or 132 000 m³ of large cockle shells. This amount compares favourably with the current annual level of removal of 134 000 m³ of shells, three-quarters of which are cockles.
6. Even at temporarily lower production rates, the exploitation of shell stocks at its present rate is not expected to lead to a rapid exhaustion of the existing stocks in the tidal inlets of the Dutch Wadden Sea, as these stocks will be in the order of a few million m³.     

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.     

Impact of trematode parasitism on the fauna of a North Sea tidal flat

The impact of larval trematodes on the fauna of a North Sea tidal flat is considered at the individual and at the population level, depicting the digenean parasites of the common periwinkle,Littorina littorea, and their life cycles, as an example. On the German North Sea coast,L. littorea is first intermediate host for 6 larval trematodes representing 6 digenean families —Cryptocotyle lingua (Heterophyidae),Himasthla elongata (Echinostomatidae),Renicola roscovita (Renicolidae),Microphallus pygmaeus (Microphallidae),Podocotyle atomon (Opecoelidae) andCercaria lebouri (Notocotylidae). All exceptP. atomon utilize shore birds as final hosts; adultP. atomon parasitize in the intestine of teleosts, mainly pleuronectid flatfish. Second intermediate hosts ofC. lingua are various species of fish; the cercariae ofH. elongata encyst in molluscs and polychaetes, those ofR. roscovita in molluscs;M. pygmaeus has an abbreviated life cycle;C. lebouri encysts free on solid surfaces; and the fish trematodeP. atomon utilizes benthic crustaceans, mainly amphipods, as second intermediate hosts. On the tidal flats of the Königshafen (Sylt), up to 77% of the periwinkles have been found to be infested by larval trematodes. Maximum infestations in individual samples were 23% forC. lingua, 47% forH. elongata and 44% forR. roscovita. The digeneans cause complete parasitic castration of their carriers and hence exclude a considerable proportion of the snails from the breeding population. Infestation reduces the longevity of affected hosts, and size-related, trematode-induced differential mortality causes changes in the normal size-frequency distribution of individual snail-age classes. Young flatfishPleuronectes platessa from the Königshafen are 100% infested with metacercariae ofC. lingua. Heavy infestation of the gills causes obstruction of blood vessels and respiratory impairment; metacercariae in the eyes and optic nerves cause visual and neurological disturbances. A single metacercaria is sufficient to kill a larval fish.Mytilus edulis andCardium (Cerastoderma) edule are 100% infested with metacercariae ofH. elongata. Heavy infestation impairs the byssus-thread production in mussels and affects the burrowing ability of cockles. Longevity and resistance to environmental — particularly thermal — stress are reduced in bivalves infested withH. elongata andR. roscovita. There is evidence that, in the study area, population size and age composition of the molluscs discussed are (indirectly) controlled by trematode parasites employing sea birds as final hosts, rather than directly by the predatory activities of these birds.     

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.     

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.     

Buffering role of the intertidal anemone Anthopleura aureoradiata in cercarial transmission from snails to crabs

In nature, parasite transmission from one host to the next takes place within complex biotic communities where non-host organisms can reduce transmission rates, for instance by preying on infective stages. We experimentally investigated the impact of four very different non-host organisms on the transmission of the microphallid trematode Maritrema novaezealandensis from its snail first intermediate host to its crustacean second intermediate host. We show that in laboratory mesocosms, accumulation of parasites in juvenile stalk-eyed mud crabs, Macrophthalmus hirtipes (Ocypodidae), was not reduced in the presence of cockles, Austrovenus stutchburyi, barnacles, Balanus sp., or the algae Enteromorpha spp., three organisms whose feeding mode or general abundance could negatively impact the parasite's infective stages (cercariae). In contrast, the presence of the anemone Anthopleura aureoradiata in the mesocosms caused a more than 4-fold reduction in the number of parasites acquired by crabs when compared to control mesocosms. Observations on fluorescent-dyed cercariae confirmed that they are ingested by anemones. Given the often high densities of anemones on mudflats, they may represent an important regulator of the abundance of M. novaezealandensis, and thus of the impact of this parasite on its hosts. These anemones may decrease cercarial transmission for many other trematode species as well. Our results stress the need for studies of parasite transmission in natural contexts rather than under simplified laboratory conditions.     

Parasites and pathologic conditions of the cockle Cerastoderma edule populations of the coast of Galicia (NW Spain).

A survey of pathological conditions affecting cockle populations of the most economically important natural beds of Galician estuaries in NW Spain was performed. Samples of 30 adult cockles were collected from each of 34 natural beds in the spring of 1999 and processed by histological techniques. Disseminated neoplasia were seen in samples from most of the natural beds, in some cases with a high prevalence. The gregarine Nematopsis sp., larval trematode stages, and branchial extracellular large cysts enclosing bacteria-like microorganisms were the most prevalent parasites. Paravortex cardii, intracellular colonies of rickettsiae-like organisms in digestive and gill epithelium, Pseudoklossia sp. coccidians, Trichodina sp., and other ciliates were frequently seen in the samples. Copepods in gills and intestine and unidentified gregarines in intestine epithelia and surrounding connective tissue were less prevalent and were observed in samples of some natural beds. Large foci of heavy hemocytic infiltration were detected in a few sites only. Cysts of Steinhausia sp. and plasmodia and spores of a haplosporidian were seen in cockles from two localities. Inflammation was frequently observed in the samples. Some of the parasites and pathological conditions could be associated with mortality.