You are what you eat—Within a factor of 2
ES&T’s runner-up environmental science paper for 2005 explains why two different species living side by side in the same ecosystem can accumulate wildly different amounts of metals from their environment.
“Why is Metal Bioaccumulation So Variable? Biodynamics as a Unifying Concept” by Samuel N. Luoma, U.S. Geological Survey, and Philip S. Rainbow, the Natural History Museum (U.K.), 2005, 37 (7), 1921–1931.
This runner-up top ES&T environmental science paper of 2005—a critical review—was more than 10 years in the making. Two biologists, working independently, began asking questions that weren’t answered by the prevailing theory of toxic metal bioaccumulation. Most importantly, they wondered why a barnacle accumulates as much as 100x more zinc than a mussel living in the nearby muck.
Decades of research, mostly by geochemists, had linked metal bioaccumulation in aquatic animals to concentrations of dissolved metal ions. Even ecotoxicology experiments by biologists, primarily chronic exposure studies, supported this view. “You put animals under very high concentrations [of metals] and watched them die,” says Philip S. Rainbow of the department of zoology at the Natural History Museum in London. “So, [researchers] automatically assumed everything [that is important] is in water.” And at those unnaturally high concentrations, they were right, adds Samuel N. Luoma, who is with the U.S. Geological Survey in Menlo Park, Calif., and is the paper’s corresponding author.
However, Luoma and Rainbow are field biologists—as comfortable digging in the mud as working in the lab—and they saw exposure as more complex. “A small school of thought believed that diet was important, but they couldn’t quantify it,” recalls Luoma.
At that time, Rainbow was investigating patterns of bioaccumulation in invertebrates—barnacles, shrimp, and crabs. He and others demonstrated that two species living side by side in the same ecosystems could have metal concentrations that varied by as much as 2 orders of magnitude. For example, one of his papers reported that barnacles living in Poland’s Gulf of Gdansk bioaccumulate 40–100_ more zinc than neighboring mussels.
Meanwhile, working with Nicholas Fisher at the State University of New York at Stony Brook in the 1990s, Luoma attacked [168KB PDF]the question of diet. “We decided to break [the problem of diet] apart to its component pieces, in terms of its physiology, and look at bioaccumulation from diet using physiological constants,” he says. Luoma and his colleagues then sewed the pieces back together into a “dynamic, multipathway bioaccumulation model.” “What is important is the differences in the chemistries of the metals, the environmental conditions, and the different ways in which [animals] handle the metal under different conditions,” explains Luoma.
In effect, the biodynamic model they promote predicts that some organisms can eliminate certain metals quickly and will be less likely to be affected by their presence in water. Other creatures are quick to take up metals but slow to get rid of them and will show higher bioaccumulation values.
Two analytical advances during the 1990s helped get the model off the ground. “Clean” analytical techniques gave more realistic values for metal concentrations in aquatic ecosystems and revealed that concentrations in the environment were as much as an order of magnitude lower than previously thought. And scientists developed a method that uses radioisotopes, such as zinc-65, for conducting lab experiments at low metal concentrations. “Using radioisotopes, you are working at realistic concentrations, where diet plays a role,” says Rainbow.
By 2004, when Luoma arrived in London as a Fulbright scholar to work with Rainbow on a book about aquatic contamination, several groups were using the biodynamics model to understand bioaccumulation. Rainbow suggested that they also collaborate on a paper that reviewed progress with the model. “We realized that the two of us knew lots of the literature in which folks had used the model and compared the results to field measurements,” says Luoma, “but it was scattered throughout the literature.”
Together, they identified 15 publications that matched model predictions with field data for 14 species of animals living in 11 different ecosystems. What would become the top ES&T paper covered 7 metals. “We synthesized it all and saw a nice fit over 7 orders of magnitude,” says Luoma.
The model does have its limits. Bioaccumulation in animals higher on the food chain, such as fish and birds, requires a more complicated model that tackles metal flux among internal organs. But diet is also important to these predators, and biodynamics can be informative.
For example, selenium is accumulated to very high levels by bivalves but not by copepods in the same environment. The result is that in San Francisco Bay, striped bass, which eat copepods, are relatively unaffected by the metal, but sturgeon, which consume bivalves, are at risk, points out Luoma.
The model “opens up a very different view of metal toxicity,” Luoma explains. “Because once you realize that species have different bioaccumulation of metals, you realize that some species are more vulnerable to metal levels. The next question is: What are these species? We are convinced that metal toxicity eliminates some species and others don’t see it as significant at all.”
Luoma is currently working with the U.S. EPA to develop a new selenium standard by combining results from the biodynamics model with predictions from the agency’s wildlife exposure model for animals nearer the top of the food chain. “We help [EPA] see the results of a regulatory number,” says Luoma. “By looking at how a selenium value affects invertebrates, which then translates up the food chain through predators, biodynamics can help constrain the uncertainty in a regulatory value.”
Rainbow continues to study a group of metal-contaminated estuaries in old mining districts in Cornwall and Devon (U.K.), trying to understand how metal accumulation moves up the food chain. “We are interested in comparative biology and trophic transfer,” says Rainbow. “We want to use the model to look at differences in populations in the different estuaries to draw some conclusions about natural selection in those environments.”
The work also shows the importance of combining lab data and field measurements, emphasize the authors. This dual approach is not recognized in all regulations, and this message will be stressed in their upcoming book, says Rainbow.
Luoma points out that diet could also play a role in the environmental effects of nanomaterials, most of which are metals.
The work has another message, which applies to scientists and regulators. “The ‘B’ part of PBT [persistence, bioaccumulation, toxicity] varies so enormously among species,” says Rainbow, “but don’t despair, because with a few parameters, as in our model, we can begin to understand this!”
