When Parasites Are Good for Health: Cestode Parasitism Increases Resistance to Arsenic in Brine Shrimps

Abstract

Parasites and pollutants can both affect any living organism, and their interactions can be very important. To date, repeated studies have found that parasites and heavy metals or metalloids both have important negative effects on the health of animals, often in a synergistic manner. Here, we show for the first time that parasites can increase host resistance to metalloid arsenic, focusing on a clonal population of brine shrimp from the contaminated Odiel and Tinto estuary in SW Spain. We studied the effect of cestodes on the response of Artemia to arsenic (acute toxicity tests, 24h LC ₅₀) and found that infection consistently reduced mortality across a range of arsenic concentrations. An increase from 25°C to 29°C, simulating the change in mean temperature expected under climate change, increased arsenic toxicity, but the benefits of infection persisted. Infected individuals showed higher levels of catalase and glutathione reductase activity, antioxidant enzymes with a very important role in the protection against oxidative stress. Levels of TBARS were unaffected by parasites, suggesting that infection is not associated with oxidative damage. Moreover, infected Artemia had a higher number of carotenoid-rich lipid droplets which may also protect the host through the “survival of the fattest” principle and the antioxidant potential of carotenoids. This study illustrates the need to consider the multi-stress context (contaminants and temperature increase) in which host-parasite interactions occur.

Author Summary

Virtually all free-living organisms are infected by parasites. Moreover, both parasites and hosts may be exposed to increasing levels of pollution and might be affected by climate change. However, few studies have considered the environmental context in which parasites and hosts interact, and the relationships between these factors remains poorly understood. It is assumed that infection with parasites increases mortality under a cause of stress such as pollution. We studied the combined effect of arsenic (As) pollution, temperature increase and infection by tapeworms on the health of the economically and ecologically important brine shrimp Artemia. We found that tapeworms make Artemia more resistant to As, a major pollutant in aquatic environments, even under increased temperature conditions. These parasites increase the capacity of antioxidant enzymatic defenses, allowing infected individuals to cope better with As. Moreover, tapeworms increase fat reserves in their hosts, which may be advantageous due to the ability of lipids to sequester pollutants (“survival of the fattest” principle). Although our results may be unusual, we find a clear explanation for them. This makes them of broad significance and general interest.