Artemia, commonly known as brine shrimp, are economically and ecologically important organisms found all over the world. Since the 1930s they have been used as feed for fish and other aquatic creatures. They take the form of dormant embryos called cysts that wash up in large amounts along shorelines all over the world and make them easy to harvest, process and trade. According to the Food and Agriculture Organisation, over 2,000 tonnes of Artemia cysts are sold worldwide every year as feed for the seafood industry. The crustacean’s ability to tolerate extreme environments have also made them a popular model organism in toxicology studies.
Now, a group of European scientists, led by Marta Sanchez from Estación Biológica de Doñana, Spain, have discovered that Artemia has a better chance of surviving in water polluted with arsenic if it is infected by a parasite. Their findings, published on March 3 in the journal PLOS Pathogens, contradict the dominant view that pollution and parasites are stressors that both only have negative effects on the health of living organisms.
The team set out to test the effect of well-known water pollutant arsenic on Artemia. They were aware that, in nature, Artemia is commonly infected by a tapeworm parasite that renders its host more prone to predation by birds, which are also the parasite’s final destination. “Infected Artemia are considered as a dead end from an evolutionary point of view as they cannot leave any descendants,” said Sanchez.
Since this parasitic relationship is such a common occurrence, the team acknowledged that it would need to take tapeworm infection into consideration while studying how Artemia responded to the pollutant. Additionally, they wanted to factor in the effects of climate change on these interactions to simulate an environment even closer to real world conditions.
A multitiered approach
To conduct their experiments, the scientists collected Artemia samples from the polluted Odiel and Tinto estuaries in southwest Spain. Relative populations of tapeworm species change through the seasons so the samples were collected in two batches – one in April 2014 and the next in May 2014. The May samples were subjected to toxicity tests with arsenic at two temperatures: 25 ºC and 29 ºC. The difference of 4º between them represents the change in mean temperature expected under climate change (at the time of the study). In April, Artemia season had just begun so the number of individuals in the sample were too few to be able to conduct two tests, so the scientists conducted just the 25 ºC test.
Both in April and May, 98% of the Artemia sample was infected by tapeworm species. The team then proceeded with the toxicity studies.
The results were consistent: in both temperatures, more infected Artemia survived arsenic doses than uninfected Artemia. This indicated to the scientists that, somehow, parasitic infection was protecting the organism from the effects of the toxin. Of course, the parasite wouldn’t do this without a motive. It requires the Artemia to stay alive until it is picked up by a bird, the parasite’s ultimate destination.
Infected Artemia from the May batch were more resistant to arsenic than those from April. This could be due to April’s sample containing two tapeworm species – Flamingolepis liguloides and Cestoda podicipina. “Both share the same intermediate host [Artemia] but have different final hosts [flamingoes and grebes], so there exists a strong competition among them,” explained Sanchez. In such a situation, it is likely that winning this competition is a higher priority for the parasite than protecting their host from toxins. The Artemia individuals from May had only one of these species, so there was no conflict and their priority to protect the host until predation was higher.
In general, the Artemia were found to be more vulnerable to arsenic at 29 ºC. At this elevated temperature, the amount of oxygen in the water is reduced. “Water permeability and drinking in Artemia increase markedly with temperature, hence uptake of pollutants will also increase,” the authors explained.
Survival of the fattest
They went one step further to identify the mechanism underlying their observations as well, waiting until the next May (2015) to collect new Artemia samples. They focused on enzymes known to play a role in detoxification and found that infected organisms had more of these chemicals. Moreover, they also discovered that infected Artemia had a larger number of lipid droplets in them. Lipid droplets are known to play a protective role by sequestering toxins away from sensitive regions in organisms, a principle known as ‘survival of the fattest’. This could explain the biological basis for the resistance displayed by tapeworm-infected Artemia.
The results need not be restricted to arsenic pollution alone. Sanchez said that many other pollutants, such as heavy metals, polycyclic aromatic hydrocarbons, organophosphate pesticides and dioxins, also follow similar mechanisms of toxicity. “Increased antioxidant potential of infected Artemia is expected to protect against a wide range of toxicants.”
Most existing literature supports the contrary view – that parasites and pollution would work together to adversely impact organisms. In 1999, Bernd Sures, an aquatic ecologist from Universität Duisburg-Essen, Germany, made a similar finding. He led a study which described fish parasites that reduced metal concentrations in its host. “This challenges our understanding of parasitism,” Sures, who didn’t participate in the current study, acknowledged. He stressed that such studies are important to show that host-parasite relationships might change when environmental conditions change.
It’s becoming increasingly clear that, as a review article authored by Sures in the journal Parasite put it, “under natural conditions no organism will only be affected by either parasites or pollution.” Despite this, Sanchez says that most ecotoxicological tests for environmental risk assessment still use uninfected organisms. This is slowly changing, as seen by the rising relevance of the multidisciplinary field of environmental parasitology, which combines toxicology, environmental chemistry and parasitology to give more holistic results. “The inclusion of parasites is critical to obtain suitable estimates of risk in natural conditions,” Sanchez said. “The big challenge is to design an experiment that is practical but which can study such complex interactions.”