Dead zones might masculinize fish
In oxygen-starved water, females look and act like males.
Aquatic dead zones, infamous worldwide for suffocating fish, may also be transforming female fish into males, according to research published today on ES&T’s Research ASAP website (DOI: 10.1021/es0522579). The study not only has dire implications for fish populations: It also hints that hypoxic conditions—water containing less than 2.8 milligrams of oxygen per liter—may be interacting directly with the hormones of the reproductive system, experts say.
It’s well known that gender in fish is determined by both genes and environmental factors such as pH and temperature, explains Rudolf Wu, an ecotoxicologist at the City University of Hong Kong and a coauthor of the study. Now, for the first time, he and his colleagues have shown that hypoxia can also determine gender by upsetting the normal balance of sex hormones, leading to a male-dominated fish population.
The scientists raised zebra fish, a hardy freshwater species popular in aquariums, in tanks with normal and hypoxic oxygen concentrations. After the zebra fish developed for 120 days in the tanks, the fish in the hypoxic tanks were 74.4% male, whereas the control group was 61.9% male, which is normal. Some of the “males” in the hypoxic treatment tanks, testicles and all, were genetically female.
Compared with males raised in normal oxygen concentrations, hypoxic males had about 70% less testosterone and estradiol, hormones that regulate sex differentiation, Wu says. The oxygen-poor water elevated testosterone concentrations in females by about 57%, and this significantly increased the ratio of testosterone to estradiol. These changes could account for the male-biased population, he says.
As young zebra fish develop, they all pass through a stage in which their gonads look like ovaries, regardless of whether they are genetically male or female, Wu explains. Then, at 23–25 days, ovaries continue to develop in about half the fish, whereas testicles replace the ovaries in the other half. A specific ratio of testosterone to estradiol is required to choreograph this whole process. It’s plausible that hypoxia boosts the number of males in the population by altering the levels and ratios of these hormones, he says.
Further evidence comes from the observation that four genes—3β-HSD, CYP11A, CYP19A, and CYP19B—that control the synthesis of sex hormones were significantly suppressed in the hypoxic fish. Some of these genes promote the conversion of testosterone into estradiol. Previous studies have shown that inhibition of these genes during sex differentiation in fish can cause those that are genetically female to develop into males, Wu says.
“What’s so interesting about this paper is that the researchers are targeting a mechanism whereby hypoxia might interact directly with the reproductive system,” says Ann Cheek, an environmental endocrinologist at the University of Texas, Dallas. It wouldn’t be surprising if fish reacted to hypoxia by generally suppressing their reproductive system in order to save their limited energy for maintenance and locomotion, she says. However, in that case, you wouldn't expect to see a change in the ratio of testosterone to estradiol. The finding that hypoxic females have a higher ratio of testosterone to estradiol suggests that hypoxia encourages a buildup of testosterone, which results in more male fish, she says.
Permanent marine dead zones now cover about 1 million square kilometers worldwide and are predicted to grow, Wu says. If other species respond the way zebra fish do, hypoxia might result in fewer fish as egg production declines, he says.
If the phenomenon were widespread, it could affect wild populations, but that would depend on when and where young fish develop, says Peter Thomas, a fish environmental endocrinologist at the University of Texas, Austin. He has found that episodes of hypoxia in the bays of the eastern Gulf of Mexico, nurseries for many fish species, coincide with the period of gonadal growth in Atlantic croaker, a kind of minnow. The hypoxia causes dramatic impairment of the neuroendocrine system and leads to retardation of egg and sperm development in the croaker.
“I've found that hypoxia appears to have much more dramatic effects than chemical pollutants on endocrine systems in the fish models I’ve looked at,” Thomas says.
