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Parasites and toxic algae, is it too much for the clams in Arcachon Bay?

Times are hard for Arcachon Bay clams, as they are heavily infected by a parasite and exposed since recently to a new group of planktonic toxins. And yet the study of their physiology shows that they are only moderately affected by the interaction between these two stresses.


The Manila clam was introduced in France in the early seventies. The commercial fishery for this species in Arcachon Bay (south-west of France) is in crisis because of declining stock and caches. Although fishing is partially responsible of this situation, effects of environmental factors cannot be ruled out, as this population is affected by two natural stresses, the infection by a parasite and the blooms of toxic algae. Clams are heavily infected by the protozoan parasite Perkinsus olseni, which resides in the connective tissues. They are also exposed to toxic planktonic algae; since 2005, toxins produced by Alexandrium ostenfeldii, called spirolides, are detected in the clams. Only few studies, however, have reported the effects of simultaneous exposures to algal toxins and pathogens upon bivalve physiology, although this phenomenon is common in the natural environment.

This work addressed three questions:
- What are the effects of different levels of infection by Perkinsus?
- How does exposure to Alexandrium affect clam physiology?
- Does exposure to Alexandrium modify the host–pathogen interaction?

The physiological responses of clams were studied according to infection levels by the parasite, to the exposure to the toxic alga and to the combination of both factors. In the lab, 128 clams were distributed in treatment and control tanks, respectively with and without Alexandrium. Exposure in treatment tanks lasted one week and was preceded (for acclimation) and followed (for depuration) by a week of culture without Alexandrium.


Clams in the experimental tanks in the laboratory

After exposure and depuration phases, samples were collected to perform various analyses:

  • characteristics of blood cells (hemocytes)
  • immunity tests (agglutination and hemolysis) on plasma
  • flesh/shell weight ratio
  • histopathology of gills, muscle, digestive gland, etc.
  • intensity of infection by the parasite
  • antioxidant and digestive enzyme activities
  • accumulation of toxins.



An example of results: the increase of hemocyte size in response to the exposure to Alexandrium; the difference is significant (*) after exposure but not (NS) after a week of depuration

Whether exposed or not to Alexandrium, all clams were infected by Perkinsus, with an average of 77,000 parasites per gram of gill tissue. The three spirolide toxins identified in the exposed clams were more abundant in the digestive gland than in the other tissues. The physiological and biochemical analyses showed few significant differences among treatments (exposure, control) and among sampling dates (after exposure or depuration). The histology revealed symptoms of various intensities according to the degree of infection and the exposure to Alexandrium: hemocyte infiltration in the digestive gland, edema in the mantle, vacuoles in gill cells, passage of hemocytes into the intestine, epithelium sloughing into the stomach lumen.


Histological sections of gills (top), intestine (middle) and digestive gland (bottom); the left section of each row was done on clams not exposed to Alexandrium and the other two show the effects of Alexandrium toxins, except the last one (I) which shows the parasites.

Putting together all these results helps answering the initial questions:

  • effects of Perkinsus

Overall, effects of higher infections were light and did not affect important physiological functions of clams. This can be attributed to the low intensity of infection compared to other studied populations, where rates ten times higher were observed.

  • effects of exposure to Alexandrium

Spirolides accumulated preferentially in the digestive gland, but also in the remaining tissues; however, even before the release of these toxins through digestion, extracellular compounds cause inflammatory responses in the mantle and the gills. Spirolides provoke inflammation and lesions in the digestive organs, probably in relation with an oxidative stress. After a seven-day depuration time, persistent effects of extracellular or spirolide toxic compounds were still observed.

  • modulation of pro/antioxidant mechanisms

The production of reactive oxygen species (ROS, responsible for oxidative stress) in hemocytes increased with the intensity of infection and the exposure to Alexandrium. Yet among exposed clams, the most infested ones did not produce more ROS, suggesting that ROS production reached a threshold or that exposure to Alexandrium is able to neutralize the increase in ROS stimulated by Perkinsus. This could reflect a modification of the immune reaction to the parasite, induced by Alexandrium.

  • effect of Alexandrium exposure on Perkinsus infection

According to the observations, Alexandrium could have a deleterious effect upon the parasite, as was already observed on the same species with a different toxic alga.

Overall, immune functions of Manila clams remained relatively unchanged according to Perkinsus infection level and Alexandrium exposure. Despite histological damage and partial dysfunction of the digestive gland, clams were able to maintain their main nutritional functions. It thus appears that the Alexandrium-Perkinsus interaction does not likely affect survival of Manila clam stocks from Arcachon Bay. Considering the roles of hemocytes in immunity, however, the question of how clam could defend against other more virulent pathogens or other environmental stressors cannot be excluded.



The paper

Lassudrie M., Soudant P., Richard G., Henry N., Medhioub W., Mirella da Silva P., Donval A., Bunel M., Le Goïc N., Lambert C., de Montaudouin X., Fabioux C., Hégaret H., 2014. Physiological responses of Manila clams Venerupis (=Ruditapes) philippinarum with varying parasite Perkinsus olseni burden to toxic algal Alexandrium ostenfeldii exposure. Aquatic Toxicology 154 : 27–38.

See the first page


The authors

To carry on this work, the team of Lemar (IUEM) was associated with researchers from Ifremer (laboratoire Phycotoxines, Nantes), the Institut National des Sciences et Technologies de la Mer (Laboratoire Milieu Marin, Salammbô, Tunisia), the Federal University of Paraiba (Laboratory of Immunology and Pathology of Invertebrates, João Pessoa, Brazil) and the University of Bordeaux (UMR EPOC, Arcachon marine laboratory).


The journal

Published by Elsevier since 1981, Aquatic Toxicology deals with the mechanisms of toxicity (uptake, metabolism and excretion of toxicants) and the responses to toxic agents in aquatic environments, at all levels of organization (community, species, tissue, cell, molecule) and at different angles (genetics and adaptation, biochemical, physiological and behavioral, bioaccumulation, etc.).



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