[Pharmwaste] Sex-changing fish - article about Pacific ocean fish off CA coast

[Tenace, Laurie]

http://pubs.acs.org/doi/full/10.1021/es8036912


Sex-changing fish: caused by contamination or nature?

Environ. Sci. Technol., Article ASAP
Publication Date (Web): January 14, 2009

The Los Angeles Times brought a startling discovery to the public’s attention
in 2005: during a small monitoring survey off the coast of Southern
California, scientists found male flatfish with female characteristics. The
intersex fish were found in the vicinity of the three massive wastewater
outfalls that dump treated sewage effluent into the Pacific Ocean and serve
the booming metropolis of Los Angeles and adjacent Orange County. As a
result, the scientists hypothesized that the discharges−almost 4 billion
gallons a day from more than 10 million people−were disrupting the endocrine
systems of the fish.

Flash forward to November 2008 and the annual meeting of the Society of
Environmental Toxicology and Chemistry (SETAC), where biologist Steve Bay
with the Southern California Coastal Water Research Project (SCCWRP) summed
up the 2005 findings.

“We knew that the results were not statistically significant, but all the
intersex fish were found between the Los Angeles and Orange County outfalls”
he said. The numbers were small: in total, 82 male hornyhead turbot and
English sole were caught at 30 sites along 600 miles of coastline. Eleven out
of 64 caught in the vicinity of the outfalls had ovary tissue in their
testes. No such sexual defects were found elsewhere. Additional studies
appeared to support these findings. Two-thirds of the male turbot and sole
caught near Orange County’s sewage outfall had vitellogenin, or egg-producing
proteins, more commonly found in female fish (Environ. Toxicol. Chem. 2003,
22, 1309−1317). In laboratory experiments, male fish exposed to ocean
sediment collected from the same area all produced vitellogenin (Environ.
Toxicol. Chem. 2005, 11, 2820−2826).

To follow up on these findings, SCCWRP, a research institute supported by
county, state, and federal funds, in 2006 organized “Emerging Contaminant
Effects on Coastal Fish,” one of the biggest studies of endocrine disruption
in marine fish to date. But preliminary results from the larger study are
revealing even more puzzling data. The turbot appear to be healthy, but the
males still have hormone levels that are abnormal in comparison with most
other fish. Now the scientists are trying to determine whether the fish are
altered by contaminants, or just odd.
The ongoing SCCWRP is a collaboration of 11 experts from several California
universities, the National Oceanic and Atmospheric Administration (NOAA),
private laboratories, water treatment agencies, and the cities of Los Angeles
and San Diego. The project end date is scheduled for 2009.

The research focuses on the hornyhead turbot, a common flatfish that lives on
soft sandy bottom sediments and eats tube worms and clam siphons. The turbot
seemed a good choice because it doesn’t migrate; it occurs throughout the
area; it is not a target for commercial fishing; and its life among the
sediments should lead to the highest levels of contaminant exposure, says
Bay. But the scientists knew relatively little about its reproductive
behavior and endocrinology. And because the fish has not been studied by
other research groups, Bay’s group was on its own.

The ambitious aim of the project is to identify the contaminants responsible
for the endocrine disruption and remove them from the treated effluent. This
is a potentially enormous job because the effluent contains steroid hormones,
pesticides in current use, and pharmaceutical and personal-care products−many
of which are endocrine disrupters. A legacy of DDT and PCB contamination in
the sediments adds to the mix.

Now, after 3 years; hundreds of analyses of effluent, sea water, and sediment
for a host of emerging contaminants; and 373 histological analyses of male
turbot gonads, the researchers have found only one fish with developing eggs
in the male gonad. This leaves the researchers uncertain about how widespread
the endocrine disruption isor even if it is occurring at all. “We spent 10
times the money and found one-tenth the number of intersex fish [as in the
2005 survey],” Bay told the SETAC attendees.

Over the past 3 years, the scientists studied sites close to wastewater
outfalls and one control site known as Dana Pointa National Benthic
Surveillance Project reference site chosen by NOAA some 20 years ago because
it was considered relatively free of contamination. The scientists sampled
effluent and water 4 times from May 2006 to February 2007. Using a trawler to
reach the turbot that live some 60 meters underwater, the researchers took
one set of sediment samples and 50 hornyheads from each site numerous times.
They studied the condition of the fish, sampled their blood and gonads, and
also analyzed composite liver samples.

They found many contaminants in the treated effluent at low parts-per-billion
concentrations or less. In the seawater, only a small proportion of these
chemicals were detectableand at concentrations 400−1000 times lower than
those found in the effluent. In the sediments, the organochlorines DDT and
various PCBs, the flame retardants known as polybrominated diphenylethers
(PBDEs), and the surfactant nonylphenol were the most frequently detected and
most concentrated contaminants. In the fish livers, the levels of PBDEs and
nonylphenol were comparable to levels of the legacy contaminants.

Relating the contaminant occurrences to the endocrine levels, vitellogenin
levels, or fish populations has proved to be a difficult puzzle. The
sexuality of fish can change as a result of many factors, says toxicologist
Daniel Schlenk at the University of California Riverside. “For example, when
we culture halibut here in the lab, all we get are males,” he says.
Vitellogenin is a great marker for exposure to estrogens but seems to be more
common in males than previously thought, and a certain number of ova−testes
may not indicate an adverse effect when the entire population of fish is
considered. “The bottom line is that we have to know the natural history of
the fish... For the hornyhead turbot, we are developing that,” Schlenk says.

At all of the sites, including the control site, the scientists found that
male turbot have very high levels of the female sex steroid 17 β-estradiol.
These levels in the males’ blood plasma were as high as or higher than the
levels in females. But English sole males from the same sites do not have
elevated estrogen levels. Both sexes of turbot appear to have abnormally low
levels of the stress hormone cortisol. Thyroxine is the only hormone that
shows clearly different levels between the contaminated outfall sites and the
control. Levels of this thyroid hormone were low in fish from the
contaminated site compared with the control site.

With very few differences between the contaminated sites and the control
site, this widespread pattern of odd endocrine levels could mean that the
contamination is much more pervasive than scientists thought, or it could
mean that these hormone levels are normal for these fish, says Bay.

Indeed, the high levels of estrogen in male hornyhead turbot could be normal
for this particular species of flatfish, says Alexander Scott at the Centre
for Environment, Fisheries, and Aquaculture Science (U.K.). Similar high
estrogen levels in males have been observed in plaice, a very widespread
North Sea flatfish species that roams miles away from land and is unlikely to
ever come into contact with sewage treatment effluent, he notes.

But endocrinologist Kevin Kelley at the University of California Riverside
believes that pervasive contamination is the answer. In the study, male
estrogen levels are high overall, he notes, but the levels are highest in the
most contaminated location, Santa Monica Bay. In addition, he says he has
seen a similar pattern of low cortisol and low thyroxine levels in fish from
other contaminated sites in San Francisco Bay.

Kelley also notes that estrogen levels appear to go down once fish are in the
lab. But the decrease in estrogen levels in wild males that are brought into
the laboratory cannot be taken as proof that the estrogen is of external
origin, says Scott. He adds that when his team brought plaice into the
laboratory, the stress of captivity caused plasma levels of all sex steroids
to plummet by up to 100 times.

In the face of these uncertainties, the scientists are trying to find other
control sites that are more pristine. They are also investigating genetic
techniques in an effort to elucidate mechanisms of action and to separate
effects due to chemical exposure from those that are unusual but natural for
the turbot, says Bay.

Finding more control sites is crucial, says John Sumpter at Brunel University
(U.K.). “If there are four contaminated sites, then I would like to also see
data from four control sites. Having those data would considerably strengthen
the conclusionsone way or the other,” he says.“Field studies are extremely
difficult,” Sumpter adds. “To be fairly sure that intersexuality and other
forms of endocrine disruption are a consequence of exposure to effluents, we
have sampled over 4000 roach [fish] in the last decade. And even then, we
still have many unanswered questions,” he concludes.

Laurie Tenace
Environmental Specialist
Waste Reduction Section
Florida Department of Environmental Protection
2600 Blair Stone Rd., MS 4555
Tallahassee FL 32399-2400
P: 850.245.8759
F: 850.245.8811

Mercury: http://www.dep.state.fl.us/waste/categories/mercury/default.htm 

Unwanted Medicine:
http://www.dep.state.fl.us/waste/categories/medications/default.htm



The Department of Environmental 

Protection values your feedback as a customer. DEP Secretary Michael W. Sole is committed to continuously assessing and 

improving the level and quality of services provided to you. Please take a few minutes to comment on the quality of 

service you received. Copy the url below to a web browser to complete the DEP 

survey: http://survey.dep.state.fl.us/?refemail=Laurie.Tenace@dep.state.fl.us Thank you in advance for completing the survey.