Point of No Return
Fishing may be such a powerful evolutionary force that we are running up a Darwinian debt for future generations
By Natasha Loder
Illustration © Jon Krause
Contrary to the opinion of a number of the citizens of Kansas, evolution is not merely a “nice theory” but rather a demonstrable fact. Evolution is all around us. In our hospitals, bacteria have become so difficult to control that fatal postoperative infections are now common. Insects in agricultural fields develop resistance to pesticides. And those unfortunate enough to have been infected with HIV know that their bodies have become evolutionary battlefields—with HIV constantly mutating and evolving resistance to antiviral drugs.
Against this background several years ago, Stanford biologist Stephen Palumbi issued a warning in the journal Science (1) that humans are dramatically accelerating evolutionary change in other species and that this is costing at least US$33-50 billion a year in the United States. Most of this cost stems from the hospitalization of people whose diseases have become resistant to treatment, but large costs also emerge when pests or disease organisms escape chemical control.
Overlooking the consequences of evolution can be costly for conservation as well. In recent years, evidence has been accumulating that evolution is having an impact on the productivity of commercial fisheries. Although research is only starting to quantify the extent of the problem, the prospect of evolutionary effects in fisheries is to be expected. Consider, for example, a farmer who, from year to year, grew seeds from only the smallest, weakest plants in the field. He would hardly be surprised to find his crops growing successively smaller and feebler as the years went on. Good farmers grow seeds from the largest or most productive plants and thus maximize their yields. Oddly, this is almost the reverse of what happens in commercial fisheries: every year, nets scoop up the largest fish and leave the smallest behind.
In February this year, fisheries scientists met in Washington, D.C., at the annual meeting of the American Association for the Advancement of Science (AAAS) to discuss the emergence of “evolutionary fisheries science”—and to lament the fact that, until now, the evolutionary dimensions of fisheries have been overlooked. They also gathered together some of the best evidence available on the subject. Their models suggest that each year in which current levels of exploitation continue will require several years of evolutionary recovery. This results in a “Darwinian debt” to be paid by future generations.
Fisheries science has managed to embrace some evolutionary ideas. There is certainly an appreciation of the need for conservation of unique gene pools and of genetic diversity within populations. Nevertheless, David Conover, a professor at the Marine Sciences Research Center at Stony Brook University in New York warns that fishery managers treat variation in size as having “no genetic basis or evolutionary consequences at all.” This is odd because the signs of size change in some important fish stocks are already apparent. For example, in the 1940s, cod in the northeast Arctic had an average size of 95 cm. Today they average only 65 cm. And average size and age of fish at maturation have been decreasing for decades in many commercially exploited fish stocks.
Until recently, it could have been argued that the lack of interest in the possibility of evolutionary change in commercial fisheries arose from the difficulty in proving that it was happening. Size changes in fish might equally be due to environmental effects on fisheries—after all, when fish are being harvested, the community they are part of is also changing. Food availability, temperature, and population density do not remain the same. According to Conover, many fisheries scientists predict that, as fish density declines due to harvesting, fish will grow faster because there is less competition for food. On the other hand, commercial fisheries are subject to strong size-selective mortality, and it would be highly surprising if this were not reflected in their genetics. “One has to take the position that, despite all other organisms in the world being subject to the rules of natural selection and evolution, somehow fisheries are not,” says Conover.
So Conover and Stony Brook colleague Stephan Munch began asking some fundamental questions. They wondered why, despite mounting evidence of rapid life history evolution in fish, current models and management plans for sustainable fishing ignore the Darwinian consequences of selective harvesting. This might be due in part to a lack of proof that size-selective mortality actually causes genetic changes.
They realized the key to proving this connection was to separate genetic from environmental changes. If fish were smaller merely because of current environmental conditions, they would bounce back quite quickly from these smaller sizes after conditions were changed. However, if size-selective mortality were exerting genetic pressure, this could be far harder to reverse and thus have long-term implications for fisheries. What’s more, some of the affected traits, such as growth and sexual maturation, are closely connected to productivity.
So the pair set up an experiment. They subjected captive populations of Atlantic silversides (Menidia menidia) to variation in size-selective harvesting. The Atlantic silverside is a long and slender fish with two dorsal fins and a rounded white belly and is common along the eastern coast of North America. Conover and Munch designed a series of selection experiments in which 90 percent of the silversides were removed. In one experiment the largest fish were taken, in another the smallest, and in a third experiment fish were culled randomly.
The results, published in the journal Science in 2002 (2), turn conventional fisheries management thinking on its head. In most commercial fisheries, fish are removed on the basis of size. There are minimum, not maximum, size limits. But Conover and Munch’s results show that this approach may have results that are exactly the opposite of what is intended. Within only four generations, taking out larger fish produced a smaller and less fertile population that also converted food into flesh less efficiently. In contrast, catching smaller fish increased the average size of fourth-generation fish to nearly double that of fish in populations where only the larger fish had been taken. In the short term, catching the largest fish gave the highest yield and mean weight of fish. But this effect was temporary. After four generations, removing the smaller individuals gave nearly twice the yield of the populations from which larger individuals had been harvested. One reason for this greater productivity was that the larger adults had a greater reproductive potential. Another was that, as expected, removing small individuals selected for fast growth.
Additional evidence is accumulating—from modeling, lab experiments, and studies of wild populations—that the heavy exploitation of fish stocks is indeed causing them to undergo genetic change. Richard Law, an evolutionary biologist at the University of York in the U.K., believes that the effect of evolution on yield has the potential to be quite large (3). Some simple calculations, he says, on the life history of the Northeast Arctic cod suggest that selection due to fishing mortality could halve the yield of the fishery, with the exact reduction in yield depending on the levels of fishing mortality applied on the spawning and feeding grounds. These results should certainly give commercial fisheries managers something to think about.
Co-organizer of this year’s AAAS Evolutionary Fisheries Science Symposium Mikko Heino from the Institute of Marine Research in Norway has been working on fisheries-induced evolution in the wild for a number of years. In total, he has now studied 12 populations of fish, including Atlantic cod (Gadus morhua), Atlantic herring (Clupea harengus), North Sea plaice (Pleuronectes platessa), American plaice (Hippoglossoides platessoides), and grayling (Thymallus thymallus). In all but one case, he finds that evolution plays an important role in trends toward smaller-sized fish. Fisheries-induced evolution, he says, can reduce productivity and reproductive potential. This means that current fishing practices are reducing the productivity of fisheries and may compromise the value of fish stocks as renewable resources.
Many life-history traits may be affected. Symposium co-organizer Ulf Dieckmann, a physicist at the International Institute for Applied Systems Analysis in Austria, says that, besides age and size at maturity, current harvesting also threatens reproductive effort, growth rate, and behavior in other species. The age of sexual maturation in several populations of cod has been reduced by one-fourth and for plaice by nearly one-third. Heino believes such examples are probably just the tip of the iceberg.
What is most worrisome about these evolutionary changes is that all the evidence thus far suggests that they can happen very quickly in fish populations—this is not the stuff of geologic time. Many studies suggest that the selection pressures are large enough for substantial change to occur within decades—even though the heritability of the traits is not large.
Jeffrey Hutchings of Dalhousie University in Canada also spelled out to the meeting the possible consequences of this kind of evolutionary change. By the early 1990s, the numbers of Atlantic cod had declined by 99.9 percent relative to their abundance in the early 1960s (4). New work suggests that evolutionary changes may have been a factor in this decline because, prior to their collapse, cod were rapidly shifting toward younger and smaller sizes. One study shows that, between 1980 and 1987, the age at which 50 percent of the females were mature had dropped from six to five years.
What the researchers are getting at is the idea that, when a population collapses due to overfishing, it is not simply the numbers of fish taken but also the type of fish taken that might be important. And just as evolutionary changes may be relevant to the collapse of populations, they may also be significant factors in the speed with which a population can recover. Hutchings says that, based on data from Newfoundland’s and Labrador’s northern cod, models suggest that “comparatively modest” reductions in age and size at maturity can slow recovery by 25-30 percent and more than double the likelihood of further population decline.
Although the evidence thus far suggests that complete cessation of fishing is likely to halt these worrying trends in fisheries, it is by no means clear whether this would allow them to recover to their historic sizes (5). This is because there is no equivalent-but-opposite, size-selective pressure forcing a population in the opposite direction. As a result, a population will regain its previous character only very slowly—if at all. Conover says there is now evidence to suggest that, when fish size is truncated by harvesting, the size structure of the population may take a long time to re-establish itself.
So now scientists such as Conover are talking about the need for a new Darwinian fisheries science—a way of managing fisheries over time periods longer than the next few years. One management option is marine reserves. We know that marine reserves provide a source of eggs and fish free from evolutionary pressures of size-selective fishing. The trouble is, their effectiveness would depend on there being little gene flow back from areas in which size selection is still taking place. In other words, if fish inside and outside the reserve can mate, the reserve’s gene pool may still show a trend toward smaller sizes because it is being inundated with genes from smaller fish from outside.
There is no quick and easy way to integrate the complexity of fish population dynamics into management. But all scientists seem to agree on the need to preserve large, old fish and maintain the balance of age classes in the population. From a conservation perspective, there may be most traction to be gained by focusing on protecting the largest fish, which play both an evolutionary and an ecological role.
Not only is removing the largest fish harming the genetic status of a fishery, but the largest fish are disproportionately important in sustaining a population because older fish produce exponentially more larvae. A 50-cm-long Boccacio rockfish (Sebastes paucispinis), for example, will produce nearly 200,000 larvae, whereas one only 30 cm longer will produce ten times this number—nearly 2 million larvae.
Steven Berkeley of University of California Santa Cruz reported at this year’s AAAS meeting that the larvae of old fish have hugely improved chances of survival compared to larvae of younger fish. His team found that in Pacific black rockfish (Sebastes melanops), survival rates were nearly three times higher and growth rates were 3.5 times faster for larvae from older mothers. This is partly because older mothers produce larvae with larger oil globules.
The hope is that these developments may force a full about-face in fisheries-management strategies. Could it be time to rethink the minimum-size restriction as a basic management tool and instead to think of maximum-size restrictions? This could involve completely new net designs—ones that allow the very biggest fish to escape. Managing fisheries in such a way that large fish are unlikely to be caught might fulfill the short-term need of increasing the biomass of spawning stock and in the long term place a selective pressure for faster growth in the size range that is being harvested. More work, as scientists frequently say, needs to be done. However, some of these ideas are already encompassed in U.S. and Canadian regulations that protect egg-bearing female lobsters, very large lobsters, and lobsters marked as known breeding females.
Given the accumulating evidence of the obvious, it is difficult to be optimistic. Each harvest introduces tiny, hard-to-reverse genetic changes into a population. By ignoring these changes, we run the risk of reducing productivity in ways that will not be easily reversed in the future. It is a debt we are running up, a Darwinian debt that we owe to future generations of fishermen.
For decades it has been a struggle merely to bring the massive overexploitation of fisheries under control. Today’s struggle involves trying to rebuild fish stocks, and that is difficult enough to do. Changing to maximum-size restrictions would involve something of a sea change in attitudes in fisheries management. And yet this alone is probably not enough. Scientists such as Andy Rosenberg of the University of New Hampshire, a member of the U.S. Commission on Ocean Policy, believe it is necessary to work on multiple fronts if we are to recover the huge losses induced by the overexploitation of the past. We need to protect fish of all ages, we must safeguard genetic diversity, and we must conserve functioning marine ecosystems.
Whatever the science reveals, action is hard to achieve in a world of competing priorities. How on earth does one manage stocks for the day after tomorrow, when managing them for tomorrow is difficult enough? Politicians, who are ultimately faced with making the decisions about how we manage our resources, are caught between good long-term management and harsh short-term realities for their constituents. With politicians, as with fish, it is survival of the fittest. It is a shame that fish cannot vote.
1. Palumbi, S.R. 2001. Humans as the world’s greatest evolutionary force. Science 293:1786-1790.
2. Conover, D.O. and S.B. Munch. 2002. Sustaining fisheries yields over evolutionary time scales. Science 297:94-96.
3. Law, R. 2002. Selective fishing and phenotypic evolution: Past, present and future. ICES Annual Science Conference 2002.
4. Hutchings, J.A. 2004. The cod that got away. Nature 428:899-900.
5. Olsen, E.M. et al. 2004. Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428:932-935.
About the Author
Natasha Loder is a science and technology correspondent for The Economist and is based in London.
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