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Environment | Tim Kaine | U.S. Senator for Virginia

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The Official U.S. Senate Website of Senator Tim Kaine

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Economic And Environmental Impacts Of Climate Change In Virginia

Virginia's climatic changes have been thoroughly documented over recent decades. The overwhelming weight of scientific evidence predicts that climate change will continue and may accelerate unless strong action is taken to reduce global greenhouse gas emissions. Climate change threatens serious harm to Virginia's economy, its people and its treasured natural resources. Virginia's political leaders should promote vigorous state, national and international policies to halt global warming. Virginia's current leadership, both in government and in the private sector, should take up this mission.

Although Virginia has experienced a relatively moderate rate of climate change compared to many other parts of the country over the past century as a whole, the speed and scale of climatic changes has gained momentum and has been accelerating throughout the last 50 years. Warming has occurred across the state, mostly during the winter months, when average temperatures rose about one degree C.1 Precipitation patterns also changed: summer rainfall declined on average by 0.50mm/day but in the fall months, precipitation increased by about the same amount.2 Correspondingly, there were more days of intense precipitation and precipitation became more variable, with greater frequency of both wet and dry periods, including the pronounced drought of 2010.3

All regional climate models project rising temperatures over coming decades. Annual average temperatures are expected to rise by three to four degrees centigrade over this century and possibly much more if emission levels continue to grow rapidly, with corresponding increases in both maximum and minimum temperatures. Overall precipitation is expected to increase by about ten percent and some models forecast that most of the increase will occur during the summer. The number of hot and humid days and the corresponding "misery index" will climb substantially. There are likely to be more heat waves like the one that Virginia suffered in the summer of 2011.4 Virginia's seasons will change: spring will come earlier, summer will last longer into the fall and winters will be milder.

INCREASED STORM SURGES AND SEA LEVEL RISE

The combination of land subsidence, sea level rise, flat and low tidewater topography and intensive coastal real estate and infrastructure development puts southeastern Virginia, namely the Virginia Beach/Norfolk/Hampton Roads region, at extreme risk from storm surges. Past tropical storms, such as Hurricane Isabel, did extensive damage from storm surge. An analysis based on catastrophe models developed by RMS, a risk management firm, identified this region as the 10th most vulnerable in the entire world to flooding from storm surges and in the United States, second only to Miami.5 Some of those at risk have already taken notice. The US Navy and Air Force, which have spent many millions of dollars to harden their facilities against flooding, are taking climate change into account in plans for the future of their bases in the region.6 Insurance companies have realized the potential for serious losses. CoreLogic, a real estate data firm, estimates that in the event of a major storm more than one-third of the houses in the Hampton Roads region would suffer flood damages7.

Most property and casualty insurers operating in the mid-Atlantic area now refuse to insure businesses and primary residences in the coastal region.8 Many industry members believe it will soon become too costly to cover many of these potentially high-risk properties, even with higher premiums. Some insurers have begun to refuse coverage for vacation homes. Limited insurance coverage puts property owners at great risk. Less than one-quarter of homes in the Hampton Roads area now have flood insurance, even in the highest flood risk areas. Insurance coverage for losses from storms is less than 25 percent of actual losses.9 Though that area will bear the brunt, these storm surge risks extend far into Chesapeake Bay and up Virginia's rivers as far as Richmond and Alexandria. The National Weather Service estimates that a Category 3 storm making landfall in the Carolinas could produce a 13-foot surge as far north as Baltimore and 14-16 foot surges further south in the Bay.10

Climate change will make the situation much worse. The pace of sea level rise at Norfolk is the highest on the East Coast because the shoreline is subsiding and global warming is increasing the rate of sea level rise, both because of thermal expansion and the melting of land ice.11 The lower tidewater area around Virginia Beach and Norfolk, as the result of climate change, will lose 19 percent of undeveloped dry land, 79 percent of beaches, and a third of brackish and freshwater marshes. An extensive analysis based on catastrophe modeling and 10,000 simulated storm tracks super-imposed on shoreline characteristics found that the mid-Atlantic region is more at risk than even the Gulf Coast or Atlantic Florida.12

The analysis considered only flood damages to above-ground structures, not in-ground infrastructure, but did include losses to building contents and interrupted use. Wind damages were not considered. Tests of the model showed that estimated losses compared closely with actual losses in past storms. The analysis considered three levels of risk: 1) losses at the current sea level height; 2) losses at the predicted higher sea level; and 3) losses at the higher sea level combined with warmer sea surface temperatures, which increase the intensity of tropical storms. Warmer sea surface temperatures significantly increase the number of hurricane-strength storms making landfall along the Atlantic coast.13

At the predicted level of sea level rise, expected annual losses exceed those at current sea levels by about 20 percent because storm surges would be higher and would extend further inland and up the estuaries. However, the combination of higher sea level and warmer sea surface temperatures elevated expected annual losses by roughly 55 percent above current levels because of the higher probability of intense storms making landfall. A particularly intense storm, one with a 50-year return period, would raise expected damages by 25 percent above current levels with only a higher sea level but by about 95 percent with both sea level rise and higher sea surface temperatures, almost four times as high as the current expected losses. The study concludes that the risks to coastal property from global warming are greatest in the mid-Atlantic region.14

Although these studies serve as serious warnings, they badly underestimate the actual risks. First, they consider only damages from storm surges, ignoring damages from high winds or from flooding caused by intense rainfall. Second, the analysis considered damages only to property that exists now but did not consider that population and construction in the coastal area will increase even as global warming continues, so future risks and damages will be considerably higher. Third, these studies consider only property damage, not potential injuries or loss of life and not the disruption that such storms bring to businesses and households. In the aftermath of a severe storm, these disruption losses alone are estimated to be equivalent to about a week's worth of total income, which is currently about $1.5 billion just for the Hampton Roads area. In only measuring a fraction of the absolute damage wrought by such storms, these analyses diminish the true scale of devastation that would result from storms that are more common and more powerful.

HURRICANES AND EXTREME STORMS

The effects of climate change on hurricane frequencies and intensities have been the subject of considerable scientific research and discussion. As they generate power from warm, moist air over warm ocean waters, hurricanes are becoming more intense as climate change continues to increase ocean temperatures. The current scientific understanding is that sustained warming will result in the more intense hurricanes becoming more frequent in Virginia's latitudes and the less intense hurricanes growing less frequent.15 With climate change driven by increasing emissions, the frequency of the most intense Category 4 and 5 storms would be expected to increase by 80 percent by 2080, or by roughly one percent per year. Over the same period the frequency of the less intense Category 1-3 hurricanes will diminish by 38 percent.

These changes are unlikely to be steady trends, since the most intense hurricanes strike the mid-Atlantic region only rarely and the effects of global warming will be superimposed on considerable short-term variability. Historically, no Category 4 or Category 5 hurricane has ever struck in Virginia but climate change is making it more likely that one will eventually do so. The implication is that overall hurricane risks are increasing because historically Category 4 and 5 hurricanes have caused 86 and 48 percent of recorded hurricane damages respectively, even though they represented only 24 and 6 percent of hurricane landfalls in the United States.16 Higher winds cause more devastation, persist longer at damaging levels and generally affect a wider area.

ECONOMIC DAMAGES FROM HURRICANES

In 2003, Hurricane Isabel did an estimated $5.5 billion dollars in damages to the Hampton Roads region, even though the region was not directly hit.17 A recent analysis carried out by a risk management firm, First American Corporation, estimated that if the least intensive hurricane, a Category 1 storm, made landfall in Southeast Virginia, it would probably cause $7.4 billion in damages, in 2010 prices.18 Another firm, CoreLogic made a similar estimate of $10 billion in damages to residential properties.19 Moreover, while the probabilities of more intense hurricanes are increasing, Virginia's economy is changing in ways that put more people and value in harm's way. Population and commercial and real estate development are again increasing in the coastal zone after the great recession of 2008-2010. The potential loss from any given storm is expected to double in each decade.20 Without a vigorous adaptation effort, Virginia is becoming more vulnerable to the effects of climate change.

When these projections of rising sea levels and storm surges, more frequent intense hurricanes, and increasing values at risk are brought together in an integrated analysis, using numbers that represent the best current scientific estimates, the results are ominous. The findings from such an integrated analysis for the coastal Virginia area are presented below.21

The National Hurricane Center, part of NOAA, estimates hurricane probabilities in each vulnerable region by fitting probability curves to historical data. Until now, the Center has neither estimated the effects of past climate change on hurricane frequencies nor predicted future effects. Nonetheless, the following table accepts the Center's estimates of hurricane return periods for 201022 and uses the scientific predictions discussed above to show the changing return periods from 2000 through 2060 of tropical storms and Category 1 through 5 hurricanes striking the Norfolk/Virginia Beach region. As the following table shows, though the probabilities of tropical storms and less intense hurricanes decline, the probabilities of major hurricane strikes increase by 50 percent over the period. By 2060 the hundred-year storm would be a Category 4 or 5 hurricane.

A study by Yale Economics Professor William Nordhaus, based on all recorded previous hurricanes striking the United States, found that damages increase exponentially as the maximum wind speed increases.23 In order to construct an overall risk analysis, these return periods, expressed as annual probabilities, were combined with the damage function estimated by Nordhaus and the estimate of a $7.4 billion dollar loss from a Category 1 hurricane. Damage estimates also factored in the effects of rising sea levels and the increase in coastal population and value at risk.24 Consequently, the damages to be expected from hurricanes striking the region increase dramatically over time, as the following table shows.

Expected losses are the damages that would be suffered from a storm of each intensity, multiplied by the probability of such a storm occurring, and then added up for all possible storms. These losses represent the actuarially fair value of hurricane damages to the region - the amount that insurers would have to collect in premiums (without overhead) to break even over time. As seen below, they rise dramatically, more than doubling in each decade because of the combined effects of global warming on hurricane intensities and sea level, along with the increase in value at risk. This perfect storm of heightened vulnerability and amplified risk will put Virginia's insurance sector under great pressure. Private insurers will have to raise rates dramatically or more will withdraw from the market. Coastal residents and communities also face an increasingly perilous future.

Another illustration of the increasing economic risks is to make use of loss exceedance curves, which are widely used in the insurance and other financial industries to measure risk exposure. A loss exceedance curve is the probability that a loss will be incurred that is equal to or greater than some amount. Loss exceedance curves for each decade from 2010 through 2060 for the Norfolk/Virginia Beach area are plotted in the following graph. Two things are immediately evident. First, the curves "flatten out" as loss amounts rise. Though probabilities of occurrence decline as maximum wind speeds rise, this is offset by the exponential increase in damages, so the probabilities of loss - combining the two - hardly fall. By 2050 there will be a 1 in 10 chance of a loss in coastal Virginia exceeding $9 billion dollars. Second, the loss exceedances rise rapidly over time. For example, the probability of damages exceeding $5 billion dollars rises from about 1 in 40 in the year 2010 to about 1 in 8 by the year 2050. The likelihood of even much greater losses rises almost as rapidly.

The implication of these estimates, when put together, is that climate change is sharply amplifying the risks to Virginia's economy and citizens and substantially increasing the likelihood of a natural disaster.

IMPACTS ON VIRGINIA'S NATURAL ENVIRONMENT

Degradation of Chesapeake Bay and loss of its economic value

Among climate change's many environmental impacts, Virginians must be especially concerned about the consequences for Chesapeake Bay and other estuaries, which are incredibly valuable recreational and economic resources. Attempts to put an overall economic value on these resources, which include not only its fisheries and recreational uses but also its many ecological functions, are necessarily speculative though the billions of dollars and tens of thousands of jobs in fishery-related and recreational activities have been documented.25 Nonetheless, the Chesapeake Bay Blue Ribbon Finance Panel put an overall value on the Bay in excess of a trillion dollars.26 Economists in Delaware estimated that a mere one percent of the Chesapeake Bay watershed generated economic benefits of $20 billion over a decade, which gives a perspective on the value of Virginia's much larger share.27 Climate change will not only impair this value but also negate the billions of dollars currently being spent to rehabilitate the Chesapeake Bay resource.

Over the course of this century, scientists predict that the CO2 content of Bay waters will increase by 50-150 percent, leading to higher acidity. Water temperatures will rise by two to six degrees C and water levels will increase by 0.7 to 1.6 meters and possibly much more if emissions grow rapidly.28 Storm intensities in the watershed and some seasonal inflows from higher precipitation and runoff are likely to increase as well. The consequences are likely to be profound even though they are hard to predict due to the complex ecology of the Bay.

More than 50 percent of estuarine beaches and 25 percent of ocean beaches on Virginia's eastern shore will disappear. One consequence will be a loss of nesting areas for already endangered loggerhead and Kemp's ridley sea turtles.29 The Chesapeake Bay could lose 50-80 percent of its tidal wetlands and marshes to inundation. An estimated 66 percent of the region's commercial

fish species depend on these marshes for nursery and spawning grounds, including menhaden, bluefish, flounder and rockfish. The sport-fishing industry, which generates more than $1.5 billion dollars per year in expenditures, will be seriously affected. Salinity levels will increase, adversely affecting eelgrass, other aquatic plants and associated fish and shellfish species. Some of these changes are potentially irreversible, once ecological tipping points are reached.30

Seagrass losses will be particularly devastating for duck species that depend on submerged aquatic vegetation for food, such as redhead, pintail, widgeon, black duck and canvasback. Duck hunting on the Eastern Shore, a popular activity for residents and visitors, will suffer. More intense storms will wash more non-point-source pollutants into the Chesapeake Bay, increasing turbidity and eutrophication. The occurrence of harmful algal blooms and oxygen deficits in Bay waters will increase.31 Parasites that have helped to destroy oyster and crab populations will proliferate.32 There are likely to be substantial changes in the mix of fish and shellfish species to be found in Chesapeake Bay waters and the productivity of the Bay, already severely impaired, is likely to be affected. The extent of these changes will be determined largely by the pace and degree of climate change.

Loss of Fish Stocks and Decreased Forest Productivity

Ecological impacts will not be limited to the coastal zone. In the upper reaches of Virginia's rivers and streams, warmer waters will reduce habitat for brook trout by up to 90 percent and reduce population numbers by more than half.33 Brook trout cannot tolerate water temperatures higher than 70 degrees F. The numbers of fly fishermen will correspondingly decline. Virginia's forests will experience significant changes. Red spruce and balsam fir will almost disappear and the red maples, yellow poplars, and chestnut oaks will decline, to be replaced by loblolly and shortleaf pine. Forest pests will proliferate, such as the hemlock woolly adelgid, which is likely to eliminate all eastern hemlocks from Virginia's forests. Drought will encourage outbreaks of pine bark beetles and gypsy moths.34 Whether overall forest productivity will rise or fall will depend on the balance between positive forces, such as CO2 fertilization, longer growing seasons and milder winters, and negative forces, such as more frequent droughts, fires, pest outbreaks and intense storms.

IMPACT ON HEALTH AND RELATED COSTS

￼Air Quality

The higher summer and fall temperatures are expected to affect air quality adversely. Release of pollen and other airborne allergens will increase with the changing seasons. Ozone and smog formation is likely to increase because higher temperatures heighten the underlying chemical reactions in the atmosphere and also increase volatile organic compounds released from trees and vegetation.35 Atmospheric ozone exacerbates bronchitis, asthma and other lower respiratory tract diseases, which are among the leading causes of death in Virginia. Climate change will also raise concentrations of fine particulates, which are even more damaging to health.36 The aggravated air pollution that typically accompanies heat waves especially harms children as they have a higher risk of developing asthma, lungs that are still developing and growing, and higher exposure because they breathe at a higher rate than adults do and often play outdoors.

National air quality standards for ozone are to be tightened eventually because of continuing health effects at the current level of standards. Recent EPA assessment concludes that allowable levels for fine particulates should be significantly lowered.37 During 2011, Virginia's air monitoring systems recorded numerous violations of current ozone standards in the Richmond and Hampton Roads areas and across northern Virginia.38 In addition, virtually all of northern Virginia violated the fine particulate standards in 2011.39

Climate change will make it even more difficult for Virginia to meet future air quality standards, particularly because hotter summers will increase summer peak electricity use, necessitating an escalation in the nitrogen oxide emissions that contribute to both ozone and particulate formation. Dominion Power is already scheduled to invest $500 million by 2015 in projects to reduce emissions from its coal-fired power plants in the state and will probably have to spend even more in the future. These amounts will be passed along in higher rates to electricity consumers in Virginia.

Health Impacts

These changes in climate will have significant impacts on the health and well being of Virginia's people, especially on the elderly and the very young, who together comprise nearly 20 percent of the population. For example, over the coming decades, Lyme disease, now confined to just one region, will spread across the state.40 The seasonal feeding cycle of the main carrier of Lyme disease, ticks, is heavily influenced by climatic changes and warmer temperatures will result in more severe tick infections in Virginia and the propagation of Lyme disease in the state. Lyme disease can be extremely debilitating, affecting every tissue and every major organ system in the body and can even be fatal in severe cases. Studies have found that almost two-thirds of Lyme disease patients still experience significant symptoms months or years after the infection was treated, including persistent severe fatigue and pain.

The burden on the medical system from increased cases of Lyme disease alone will be substantial. A survey of over 2,000 people who had tested positive found that roughly 26 percent had been on disability or public support, with a majority receiving support for more than two years and 37 percent for more than five years.41 Over half had visited an emergency room as a result of their illness, 15 percent had done so three to five times, and nine percent had done so six or more times. More than half of patients saw seven or more physicians to obtain a diagnosis; over a third saw 10 or more physicians.

In addition, three of the four leading causes of death in Virginia, heart disease, stroke, and chronic diseases of the lower respiratory tract, will be significantly exacerbated by climate changes. Episodes of extreme heat lead to increases in both illness and death.42 Heat waves result in more heart attacks, strokes, and asthma attacks.

A recent study found that "heat wave mortality risk increased 2.49 percent for every one degree F increase in heat wave intensity and 0.38 percent for every 1-day increase in heat wave duration. Mortality increased 5.04 percent the first heat wave of the summer versus 2.65 percent in later heat waves, compared with non-heat wave days."43

In Virginia's cities, "heat island" effects will be intensified by higher nighttime temperatures. Elderly people, who are becoming a higher and higher percentage of the population, are particularly vulnerable because they are less able to effectively regulate body temperature, and often live alone without air conditioning. People who are obese, 25 percent of Virginia's population, are also at higher risk.

Adverse health effects of climate change will also add to Virginia's fiscal pressures. Health-related expenditures account for 30 percent of the state's budget, second only to education. 44 The largest category of spending is on Virginia's Medicaid program, serving children, the elderly and people with disabilities. Despite some of the most stringent eligibility criteria in the nation, the program's budgetary impact is growing, with the elderly and people with disabilities being responsible for the heaviest fiscal burden, largely because of the prevalence of chronic problems, such as heart disease and stroke.

CLIMATE CHANGE'S IMPACT ON TOURISM

Another important sector of the economy that will suffer from these environmental impacts is the tourism and travel industry, which is Virginia's 5th largest employer. Counting direct and induced employment, the industry generated 287,700 jobs in 2010 and more than $7.5 billion in payrolls. Total expenditures by tourists in 2010 exceeded $31 billion, more than seven percent of the state's gross domestic product.45 The leading travel and tourist destinations are in Northern Virginia in Arlington, Fairfax and Loudoun counties, near the nation's capital. Of leisure travelers, 90 percent visited historic sites and battlefields and 84 percent visited beaches, national and state parks, or engaged in other nature-related activities, including hunting, fishing and bird- watching.46

This industry is at risk as climate change threatens many vacation destinations. Historic Jamestown Island could be completely inundated and popular Chincoteague could be battered and lose 80 to 90 percent of its beaches.47 Most tourists arrive in the summer months and their travel plans will be affected by higher heat and humidity, more frequent heat waves, and more frequent intense storms. Families walking with children around urban sites in 100 degree heat and humidity do not greatly enjoy their sightseeing experience. One out of five families whose beach vacations are interrupted by heavy storms cancels their plans to return in the following year.48

THE WAY FORWARD

Near the end of 2007, then Governor Tim Kaine formed a broadly based Climate Change Commission to consider the potential impacts of climate change on the state and to recommend specific actions both to mitigate and to adapt to those impacts. The Commission consulted widely among public, industry and scientific groups and put forward a Climate Change Action Plan in December 2008.49 It contained many well- founded recommendations for cost-effective actions to improve energy efficiency, to mitigate and sequester greenhouse gas emissions and to promote effective adaptation.

The Action Plan recognized that despite these opportunities for action within Virginia, climate change is a problem that requires national and international action as well as state and local participation.50 The succeeding administration has shown little interest in implementing those recommendations. According to a very recent report in the Roanoke Times, "This week, the Virginia secretary of natural resources said Gov. Bob McDonnell has no interest in reviving a climate-change commission created by his predecessor, Gov. Tim Kaine."51

The rising risks to Virginia's economy, its people and its irreplaceable natural resources cannot be avoided simply by denying that they exist. Virginia's leaders should recognize the increasing dangers that global warming poses and support implementation of the useful recommendations made by the Climate Change Action Plan or adopt equally effective policies of their own. In particular, Virginia's leaders should follow the example of former Republican Senator John Warner and support strong state, national and international action to reduce greenhouse gas emissions.

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Economic And Environmental Impacts Of Climate Change In Virginia

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Virginia's climatic changes have been thoroughly documented over recent decades. The overwhelming weight of scientific evidence predicts that climate change will continue and may accelerate unless strong action is taken to reduce global greenhouse gas emissions. Climate change threatens serious harm to Virginia's economy, its people and its treasured natural resources.

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VIRGINIA BEACH, Va. - The Chesapeake Bay located in the states of Maryland and Virginia is home to 3,600 species of animal and plant life. The largest estuary in the United States has a very complex ecosystem and unfortunately a variety of environmental issues.

Issues ranging from agriculture to climate change to bay grasses dying off. Professor of Ocean, Earth and Atmospheric Sciences at Old Dominion University Richard Zimmerman says, "The Bay has lost probably 90 percent of its historical distribution of submerged aquatic vegetation since James Town." He says this has occurred mostly in the 20th century resulting from human population, human activity, and corrosion.

There is a lot to put to blame for the various issues the Bay faces but according to Zimmerman he says, "The biggest problem and the one we are most worried about is sea level rise as a result of climate change."

Zimmerman notes three things going on in the Chesapeake region that are responsible for our very high reach of sea level rise. One of them is climate change, second is ground water pumping which causes the land to sink or subside and third isostatic rebound from the last glacial period.

What is standing in peoples ways of believing in climate change is, "short term self interest, i.e. money and jobs, the problem comes from people perceiving that their jobs, lively hood and income is threatened," Zimmerman states.

"More of the same" Zimmerman believes is what we can expect in the future if people do not hop on board with climate change. Climate will get warmer, sea level rise, storm intensities are going to increase, and climate variabilities are going to change.

Zimmerman brings up three things that can be done to prevent future environmental issues from occurring. One, population two, alternative to fossil fuels, and three realize we're on the same boat, we need to cooperate in order to solve these problems.

"If we continue on the way things are going and don't make changes we are going to get to a point of inevitable climate change and nobody is going to be happy with it, we aren't going to be able to stop," Zimmerman says.

Virginia Beach resident and avid beach goer at Chick's Beach, also known as, Chesapeake Beach, Alexa Schneider comments on the issue, "Chick's Beach to the locals of Virginia Beach is a summer haven. It is where you go to relax without the extensive rules of the oceanfront due to it being a tourist location. In the past six years I have lived here in Hampton Roads I have noticed that there is coastal flooding and a great deal of shoreline erosion. The tide has risen to a farther distance than I've ever seen it in the past couple of years."

Unfortunately, there are many other problems besides climate change. According to team members of the Chesapeake Bay Program two other important issues are nutrient and sediment pollution.

Despite these ongoing environmental issues, progress is being made and action is being taken. The Chesapeake Bay Program Communications Director Rachel Felver and Team says, "In 2010, the U.S. Environmental Protection Agency set a total maximum daily load (TMDL) or "pollution diet" for the Bay and its streams, creeks and rivers. This sets limits on nitrogen, phosphorous and sediment pollution necessary to meet water quality standards by 2025."

The Chesapeake Bay Program in terms of nutrients and sediment specifically also has a grant program that funds new and innovative ways to reduce pollution. "Since 2007 the program has awarded more than $69 million to support around 149 projects ranging from oyster reef restoration and rain gardens to tree plantings and agriculture best management practices," says Felver and the program's team.

Not only are there plans in progress but you, the people can become more educated on this topic and get involved in Bay restoration. Felver and the program recommend joining a local environmental organization, participating in stream cleanup or tree planting and keeping up to date with the current news on these issues.

"There is still plenty of more work to do," Felver says. Don't let these issues scare you away, humans can save the Chesapeake Bay and the planet.

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Virginia's Chesapeake Bay faces environmental issues

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VIRGINIA BEACH, Va. - The Chesapeake Bay located in the states of Maryland and Virginia is home to 3,600 species of animal and plant life. The largest estuary in the United States has a very complex ecosystem and unfortunately a variety of environmental issues. Issues ranging from agriculture to climate change to bay grasses dying [...]

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They asked the dying Pasco County man about his Navy service a half-century before. He kept talking about the steel barrels. They haunted him, sea monsters plaguing an old sailor.

"We turned off all the lights," George Albernaz testified at a 2005 Department of Veterans Affairs hearing, "and ... pretend that we were broken down and ... we would take these barrels and having only steel-toed shoes ... no protection gear, and proceed to roll these barrels into the ocean, 300 barrels at a trip."

Not all of them sank. A few pushed back against the frothing ocean, bobbing in the waves like a drowning man. Then shots would ring out from a sailor with a rifle at the fantail. And the sea would claim the bullet-riddled drum.

Back inside the ship, Albernaz marked in his diary what the sailors dumped into the Atlantic Ocean. He knew he wasn't supposed to keep such a record, but it was important to Albernaz that people know he had spoken the truth, even when the truth sounded crazy.

For up to 15 years after World War II, the crew of Albernaz's ship, the USS Calhoun County, dumped thousands of tons of radioactive waste into the Atlantic Ocean, often without heeding the simplest health precautions, according to Navy documents and Tampa Bay Times interviews with more than 50 former crewmen.

Albernaz began a battle for his life in 1988 when part of his brain began to die, mystifying doctors who eventually concluded the rare ailment might be linked to radiation. He filed a VA claim for benefits in 2001 that was repeatedly rejected, often with tortured government reasoning.

The VA and Navy told Albernaz he was not exposed to radiation on the Calhoun County, a vessel the Navy ordered sunk in 1963 because it was radioactive. The VA ignored Navy documents discovered by a former congressional aide proving the ship's radioactivity, telling Albernaz they were "unsubstantiated." And the Navy today points to Cold War records that are incomplete and unreliable as proof crewmen were not exposed to dangerous radiation.

The Navy and VA's insistence that atomic waste on the Calhoun County was not dangerous comes 15 years after the VA linked the death of a crewman who served with Albernaz to radiation.

Adequate health safeguards were followed and the crew was not exposed to dangerous radiation, Navy spokesman Kenneth Hess said.

"The Navy did not scuttle the ship because of radioactivity," he said, "but because it was at the end of its useful life."

Up to 1,000 men served on the Calhoun County in the years it dumped radioactive waste, a practice that continued until about 1960 - two years before the ship's decommissioning.

It's impossible to know how many suffered unusual health problems after they left the ship. The VA and Navy never followed up on their health. Some got sick and never filed VA claims. And after more than a half-century, much of the crew has died.

Albernaz died in 2009 of heart failure after his health was ruined by radiation, his wife says. He was 75.

"George believed his own government thought he was lying, like it was all a figment of his imagination," said his widow, Bernice Albernaz, 69, who continues the fight with the VA that her husband began 12 years ago.

She said her husband didn't lie. Sea monsters did troll the depths. They remain there still.

* * *

It was a ship built for war.

LST 519 was launched in early 1944 and quickly put in harm's way. The ship took supplies to North Africa and participated in the D-Day invasion of Normandy, surviving convoy attacks by German airplanes. The name Calhoun County was added in 1955.

LST stands for "landing ship, tank." The ship, nearly as long as a football field, carried tons of supplies that could be disgorged through bow doors on a beach or stored on its large top deck.

With the end of World War II, the ship began dumping the military's old or defective ammunition into the Atlantic from ammunition depots up and down the East Coast, usually in waters at least 6,000 feet deep. But it wasn't long before a second mission was added for the crew of 75 or so men.

The opening of the Atomic Age brought a vexing problem - how to dispose of radioactive waste.

The Atomic Energy Commission, which then managed most aspects of U.S. atomic energy policy, settled on a cheap, convenient fix: ocean dumping. The Calhoun County soon became the only Navy ship on the East Coast dumping radioactive waste.

The containers looked like ordinary 55-gallon steel drums. Nobody on the ship was quite sure what was in them.

They arrived by the hundreds by train and truck at the ship's home port at Sandy Hook Bay, N.J. or the ship picked them up at Floyd Bennett Field on Long Island. Less often, waste was picked up at other ports, including Boston. The hottest waste came from Floyd Bennett. At times, the barrels were marked with color-coded dots or a painted X. The "red dot" barrels were said to be the most dangerous.

Not that it mattered. Few if any of the crewmen, according to interviews, received any special training on handling the waste. They said they handled the "red dot" barrels the same as all the rest.

Much of the waste, which was packed in concrete, came from Brookhaven National Laboratory, a government research facility on Long Island that had a reactor and generated radioactive material.

Several shipments emitted 17 rems per hour of radioactivity even after the waste was encased in concrete, Calhoun County's deck logs show. That is the equivalent of about 1,700 typical chest X-rays.

Two sailors would place each barrel on its side and roll it to the edge of the ship. The Calhoun County, with its flat, shallow bottom, always shifted crazily in the waves, back and forth, a metronome marking time for a dangerous waltz.

As the ship tilted in their direction, the men released their barrel with a push and let gravity help take it overboard.

The ship carried the waste out off the continental shelf several times a year to waters of varying depths, usually 6,000 to 12,000 feet. The designated dumping areas were a full day's trip up to 200 miles out to sea, though several men said in interviews that the ship would dump much closer to the coast when the weather was bad.

After they handled the barrels, the men went below deck to drink coffee or eat.

No documents appear to exist showing what exactly the Navy dumped. Deck logs list dumping coordinates, tonnage handled and drum radiation levels - but often, even that information is missing. And from 1946 to 1953, the Calhoun County's officers were not recording any dumps in deck logs at all.

"We do not have complete historical records that would enable accurate estimates of the exact types or total quantity of radiological waste the Navy disposed of at sea," Hess, the Navy spokesman, said. Still, he insists the waste was "low level."

The Navy says some of the waste included contaminated lab equipment and "potential nuclear fuel sources." In the 1970s, scientists found small quantities of plutonium and cesium had leached from some barrels.

A 1954 government handbook on ocean dumping said precise records were critical. Atomic science was new. Dumping could cause "undesirable consequences" then unforeseen, it said.

* * *

At the Brookhaven lab, workers were advised at length about the safest way to deal with radiation. In 1957, the lab produced a booklet for its employees called ABC's of Radiation.

Radiation, the booklet said, "should be regarded with respect, but it need not be feared. Complete safety is possible, if the necessary rules and procedures are followed. Danger lurks only for the uninformed or careless."

Radioactivity can damage a cell's DNA or chemical bonds in the human body. But sometimes cells are unable to repair themselves, especially as radiation levels rise.

Scientists believe this can lead to cancer or other illnesses.

On the Calhoun County, according to documents and interviews, radiation was neither feared nor respected. "We had no supervision," said Bob Berwick, 82, of Laguna Niguel, Calif., an officer on the ship in 1952 and 1953. "We were on our own."

From the Brookhaven booklet: "To guard against contamination, special protective clothing is available in radiation areas. . . . Clothing worn where radioactive materials are present is specially marked and washed."

None of the crew interviewed for this story recall getting special clothing or gear during dumping operations. An exception were the cotton gloves provided to the crew in the early to mid-1950s.

"We threw the gloves overboard into the ocean when we were done with them," said Richard Tkaczyk, 85, of Buffalo, N.Y., who served on the ship from 1949 to 1951.

Several men said they were told to shower and take off clothing for washing after dumps. But for much of the ship's history, this was not done, according to crewmen.
"The laboratory employs shielding extensively to protect you against . . . radiation."
No special shielding was ever used on the Calhoun County. In fact, some of the ship's crew slept in quarters immediately under the barrels on the main deck. The deck plating was less than an inch thick. Atop that was wooden planking. Radiation still seeped below.

Albernaz told the VA in 2007 he recalled a trip when an AEC worker came through the crew quarters with a Geiger counter.

"It would go off like a machine-gun and he would say to us, 'Okay. Get your pillow, blanket and mattress. We're moving you to the tank deck,' " Albernaz said.

But the tank deck was under barrels, too. "So actually, there was really no place on that ship that was safe," Albernaz said.
"All members of the staff who work in radiation areas are required to wear a small film badge, which is darkened by radiation, or a pocket meter resembling a fountain pen. ... Meters are read daily, badges every week to ensure nobody is overexposed."
At times, the men of the Calhoun County wore both types of radiation detectors. But interviews show they were often missing. Other times, the badges would be handed out immediately before a dump and retrieved immediately afterward. So radiation exposure during the three-day round trip to dumping areas was not documented.

And radioactive barrels might be stored on the ship for days at a time before the ship sailed, continually exposing the crew, according to deck logs.

And even when they had detectors, many of the crew did not take them seriously.

"When the badge turned purple, that meant you had too much radiation," said Andre Vernot, 75, of Columbia, Md., an officer on the ship from 1960 to 1962. "Our rules were, when the badge turns purple, turn it in and get another one."
"Radioactive materials can be harmful if within or on the body. ... This is why eating or smoking is forbidden in some radiation areas."
The barrels loaded on the Calhoun County sometimes leaked, especially in the early days of dumping. William Dillow, 90, of St. Augustine, was an ordnance disposal specialist on the ship from 1957 to 1960. He vividly recalled one shipment.

"They had a leaker and the flatbed [truck] was contaminated," he said. The Navy's solution wasn't elegant. The flatbed was loaded on the ship and tossed in the ocean along with the barrels.

When the dumping was done, sailors washed out bin areas with high-pressure water while others used brooms to sweep out the deck. The men might then track that water, and perhaps radioactive particles, into every part of the ship, according to interviews.

One sailor absently sat on a red-dot barrel for a few minutes during one operation, said Elmer Peter, an 81-year-old Lawrenceville, Ga., resident who was a ship's pipe fitter from 1955 to 1956. There was an apparent delay in reporting the incident, and the sailor went about his business.

"They eventually went to this guy's bunk with a Geiger counter and there was so much contamination, it pegged the counter," Peter said. "They had to destroy everything on the bunk and everything else in the area. I never saw him again."

A Navy spokesman dismissed that the men sleeping under the barrels faced danger.

"Even an eighth of an inch of steel can shield people from many low-level radiological waste materials, and even a distance of one foot provides additional protection," said Hess.

The crew sometimes noticed the civilian dock workers who loaded the waste taking precautions the Navy ignored.

"Once we pulled into Sandy Hook, and the civilian workers who were loading this stuff had exposure suits on, masks and everything," said Vernot. "And we're out there in our shorts, no shirts. That really p----- us off."

* * *

There were jokes, of course, about the entire ship being radioactive and how the barrels would make them all sterile.

But the ship was radioactive.

On June 5, 1956, according to Navy memos, Naval Research Laboratory technicians took radiation readings on the Calhoun County before barrels were loaded on its deck.

Parts of the ship were radioactive, a memo to the Third Naval District commandant said. The ship's captain, Herbert Hern, was ordered to "decontaminate affected areas" as soon as possible.

The discovery prompted a more thorough examination of dumping operations. Navy brass did not like what they found. The ship's handling of this dangerous waste was sloppy, haphazard.

The Navy today says all crewmen were trained in the use of dosimeters, or radiation badges, to ensure none received a dangerous dose.

Readings, the Navy says, were documented.

But on Aug. 30, 1956 - a decade after dumping began - a memo from Navy commanders said Calhoun County "personnel are not familiar with monitoring and decontamination procedures " and "radiological exposure records of personnel are not maintained" properly.

The Navy ordered the ship to inspect barrels before they were loaded to ensure none leaked radioactive material, a particular problem.

Ship's surfaces were washed, sandblasted, repainted. Available records do not say if any of this worked.

The crew didn't worry, but few of them knew their workplace was radioactive.

* * *

George Albernaz, then 22, was excited to be on the Calhoun County as its newest quartermaster. He was born in Fall River, Mass., and had hardly been away from home. He thought he was going to be part of the Navy's storied amphibious force.

He took a diary with him and recounted his adventure in the words of a wide-eyed sailor.

"This is the story of the most fascinating experience of my life ... doing a job I never dreamed existed, serving on a ship whose days as a man of war are but a story in the past but today she is engaged in a service equally important as any fighting ship in the Navy," he wrote.

It wasn't long before Albernaz began keeping a different kind of diary. He titled this new log "Nuclear Waste Dumping Diary."

Jan. 20 1957: "371 tons atomic waste."

Feb. 7, 1957: "368 tons atom waste."

Nov. 13, 1957: "299 (tons) poison gas (and) A.W."

One of Albernaz's last entries was on June 12, 1958: "200 tons. Spec. weapons," or special weapons. That was the day, Albernaz later told his wife, that he helped dispose of an atomic bomb.

The Calhoun County sailed out of Norfolk, Va. with two giant crates. The ship's log noted it dumped "confidential material" at 2:31 a.m.

Albernaz's wife said he told her about that trip. He said the crew was told the crates contained two atomic bombs. Other sailors interviewed said the occasional dumping of disassembled atomic bombs occurred several times in its history.

* * *

On March 10, 1958, one of the Calhoun County's crew, Harvey Lucas, was ordered to a Navy hospital. He was in pain and vomiting a brownish liquid, hospital records show.

Two months later, the ship's muster rolls show, Albernaz was hospitalized for two weeks. His wife said he later told her he had severe nausea. The two men were among a handful that year with long hospitalizations, records show. Albernaz later said doctor's diagnosed them with stomach ulcers.

Michael Gardner, a ship's officer in the early 1960s, said he saw odd stomach ailments.

"I distinctly remember crew members being off the vessel and sent to the hospital," said Gardner, 73, of New York City. "The only reason I remember it is because I had to find ways to cover for certain people when they were taken off the ship."

On March 28, 1958, Rowland Burnham, the Calhoun County's new captain, asked his superiors for $37,000 to replace the wooden deck that held radioactive barrels during dumping operations. The ship, it seemed, was still radioactive.

"Scrubbing, washing or scraping away of some of the wood has not removed all of the contamination," Burnham said in a memo. He said the radiation was low, just 1 millirem. A typical chest x-ray is 10 millirems.

"But the personnel are being continuously exposed to it," the captain said. "It is felt that this condition is a health hazard and should be eliminated."

For more than a year, records show, the Navy did nothing, perhaps because it was thinking of mothballing the ship. It needed major repairs.

Early in 1959, the Navy finally replaced the deteriorating deck. That, however, created a new problem: The debris was radioactive. Civilian workers put it in barrels with concrete - 125 in all.

The Calhoun County then sailed out and dumped part of itself into the sea.

* * *

On Nov. 8, 1962, the Calhoun County was finally decommissioned in a ceremony at the Brooklyn Navy Yard. Crew and family sat in chairs on the ship's contaminated deck. A band played. The crew was reassigned.

The Navy planned to sell the ship, either as is or for scrap. Its scrap value was not insignificant - $62,000. But ultimately, the Navy realized it could not be sold.

A Dec. 13 memo by the chief of the Navy's Bureau of Ships doubted radiation on the Calhoun County could ever be reduced to levels then considered safe. The memo noted the Navy had never been able to decontaminate a radioactive ship.

"Complete paint stripping and sandblasting have failed to accomplish this (on the Calhoun County) and in the cases of ships contaminated in nuclear weapons tests," the memo said.

So the Navy ordered the Calhoun County sunk.

Navy officer George Self, 83, of Pahrump, Nev., got the job to ready the Calhoun County for sinking. The end came sometime in 1963. The Navy roped off several compartments inside the ship, Self said, and posted signs throughout warning of radiation.

The ship left Norfolk Naval Base and a submarine fired two torpedoes at it in a gunnery exercise. One punched a hole near the engine room, but the Calhoun County refused to sink.

The Navy towed it back to Norfolk and tied up at a pier to figure out what to do next. It was only then that the Calhoun County started sinking.

Self got an emergency call at home from Navy brass. They were apoplectic that a radioactive ship was sinking at the base.

Divers plugged the hole. Sea water was pumped out. And the ship was towed to deep water.

Self did not go out on the second trip, so he is unsunsure how the ship met its end. The Navy said demolition charges sent the old LST to the bottom.

* * *

The years after his 1960 Navy discharge were cruel to Calhoun County crewman Harvey Lucas.

Lucas, a Denver man who spent more than three years on the ship, had always been suspicious of the Calhoun County's mission even while still a deckhand. Like Albernaz, Lucas tried to document the ship's work. He stole a radiation badge and took pictures of the barrels.

"He documented everything," said daughter Jeanine Lucas.

His family said he wondered if the work had been far more dangerous than the Navy let on. Those concerns could only have been stoked when his uncle, George Dutcher, who served on the ship with Lucas, died of cancer in the late 1960s still in his 40s.

Lucas left the Navy and developed osteoporosis. It was so severe that a doctor said he had the bones of a 95-year-old, his family told the VA. He and his wife had five children born with birth defects or health problems.

Cancer took Lucas, too. He died on June 17, 1985, at age 47 of leiomyosarcoma, an aggressive soft-tissue cancer. It has been documented in women who in the 1950s and 1960s received radiation treatment for excessive menstrual bleeding.

Damage from the disease was so bad a funeral home couldn't embalm him. Lucas was buried in a body bag.

Lucas, and then his wife after his death, battled the VA for benefits, arguing the radiation caused his cancer and brittle bones. The VA repeatedly denied a link, at first saying the ship hadn't carried radioactive waste.

In 1990, his wife, Barbara Lucas, contacted Karl Morgan, who is sometimes called the "father of health physics." He had been head health physicist at the Oak Ridge National Laboratory for 29 years. He helped set standards for radioactive-waste shipping containers like those on the Calhoun County.

"It is my opinion that the Navy was very irresponsible in not informing those engaged in this hazardous waste operation (of) the inherent danger and the necessity to minimize their radioactive exposure and especially to avoid inhalation or ingestion of any of the loose radioactive waste," Morgan told the VA. "It is impossible to condone the fact that these service men did not at all times wear film badges."

William Kemper, a retired Naval physicist, estimated Lucas had been exposed to radiation five times greater than the legal limit when he served.

Kemper told the VA, "it seems most likely that he had ingested some cobalt 90 or other (radioactive) waste in . . . his duties."

In 1998, the VA finally ruled Lucas's death was caused by radiation he was exposed to on the Calhoun County and approved benefits for his widow.

* * *

George Albernaz didn't talk much about his almost two years on the Calhoun County after he was discharged in 1958.

He didn't like discussing the atomic dumping with strangers, his wife recalled. He sensed, when he did talk, folks just assumed he was exaggerating his Navy service.

Bernice and George Albernaz met at a dance hall in Massachusetts in the late 1960s. Everybody liked George. A gentle man, he had been an altar boy until he was 15, was soft-spoken with an open, trusting face. Bernice thought he had kind eyes.

The couple married in 1969, and when their son was born in 1970, they laughed. The barrels hadn't sterilized him after all.

In 1988 at age 54, Albernaz began having troubling symptoms.

He lost weight. He began dropping things with his left hand, which felt weakened. He tripped over his left foot and couldn't hold the newspaper up in the morning. When the couple talked about it, they just brushed away any concern.

"You're getting old," Bernice Albernaz told him.

On Aug. 31, 1988, her husband drove to work as shipping supervisor at a Fall River, Mass., factory curtain outlet. During the day, Albernaz fell, shaking uncontrollably with a seizure. He was rushed to the hospital. His wife thought he might have had a stroke or heart attack.

A brain scan and tests brought the worst news. Doctors diagnosed a brain tumor. They prepped Albernaz for surgery.

But no evidence of a tumor was found during surgery. The tissue in one part of his brain was dying. That explained Albernaz's left-side weakness.

The dying brain tissue mystified doctors, but they discharged Albernaz.

He returned in October for more brain scans. The shadow on his brain had grown. Doctors began to doubt their earlier assurances that it wasn't a brain tumor, medical records show, and Albernaz underwent chemotherapy.

Two additional brain surgeries followed. Biopsies finally ruled out a tumor. But that good news was tempered by a growing weakness on his left side. His arm was becoming useless. His left leg was affected as if the malady was moving down his body like snake venom spreading from a bite.

Doctors were still baffled. Samples of Albernaz's brain were sent to the Centers for Disease Control. He began to tell doctors about those long-ago barrels.

A doctor made a consultation note about Albernaz's description of the Calhoun County's work. "He was on a ship where the work was done with no protection. ... He did not appear to have any radiation consequences at the time. . . . There's the possibility that he got some delayed radiation necrosis effect which can appear many years later."

It wasn't until 2006 doctors began to believe Albernaz's troubles were tied to vasculitis, an inflammation of blood vessels that can limit the blood supply to an organ such as the brain. His doctors told him radiation could cause this. But records indicate they would never be certain of the vasculitis diagnosis.

Albernaz became paralyzed on his left side. Seizures continued. He walked only with a leg brace or cane. By the end of his life, he used a wheelchair. Albernaz couldn't get out of bed without help. His life of bowling, dancing and fishing was over.

Albernaz would never work again.

* * *

In 2001, Albernaz filed a claim for benefits with the VA. He wrote letters and emails to anyone he could find who served on the Calhoun County, asking if they had become ill.

A crewman named George Lindsay responded, telling Albernaz he hadn't been sick.

"(But) I do believe that we were exposed without being told what could happen to us and our families," Lindsay wrote him. "I find the biggest problem is that there is no follow up on any of the crew members. . . . Not even a phone call from anyone in the government to find out if we are well."

Weeks after Albernaz mailed in his benefits claim, he got a letter from a woman who would provide the kind of evidence most veterans never see in years fighting the VA.

Deborah Derrick had been an aide to U.S. Rep. David Skaggs, a Colorado Democrat, in the late 1990s when she heard the Harvey Lucas story. She was mesmerized by his history on the ship.

She began researching the Calhoun County, hoping to write a book. She would hit pay-dirt.

In the National Archives, she found old Navy reports about the Calhoun County's radioactivity. She read about a captain's concerns the radiation was a health hazard for sailors. She was stunned to see reports showing the ship was deliberately sunk because it was contaminated with radioactivity.

She attended ship's reunions and tracked down crewmen. Then she found Albernaz.

With her piles of documents proving the ship's radioactivity, Derrick thought it would be impossible for anyone to deny the Calhoun County hadn't endangered its crew.

"I thought I was going to be the girl riding in on white horse to save the day," said Derrick, 52. "I thought I had incontrovertible evidence."

* * *

One of the VA's first responses to Albernaz, his wife said, was to tell him it could not find records that he served on the ship. But the couple found an old Calhoun County Christmas menu from the ship dated 1956 that listed his name.

In the years that followed, the VA discounted or ignored much of the evidence Albernaz presented. The VA talked of his "alleged involvement" in dumping atomic waste. The VA said Derrick's evidence was "unsubstantiated."

Albernaz submitted the letter from Morgan, the 29-year head of health physics at one of the nation's premier radiation labs who had offered an opinion in the Lucas case. Morgan criticized the Navy's low radiation estimates on the Calhoun County.

The VA told Albernaz it "is not familiar with Mr. Morgan's credentials." A child could become familiar with those credentials after 10 minutes on the Internet, Bernice Albernaz later said.

The VA dismissed an assessment by one of Albernaz's doctors that his necrotic brain tissue was caused by radiation because it "was based upon the history the veteran reported to him."

Though there are numerous documents in government archives showing the Calhoun County carried radioactive material, the government made little effort to substantiate Albernaz's claim.

Albernaz's testimony and evidence, the VA said, was "anecdotal."

The VA asked the Navy to check records to see if they showed Albernaz had been exposed to radiation. The Navy found records from 1958 and 1959 with a list of crewmen who wore radiation badges.

Every man on the Calhoun County, except for officers, handled the barrels. But the Navy said Albernaz was not listed in either year. As for readings in 1957, the Navy could find no records at all.

So the VA ruled in 2006: "Again, U.S. Navy Department confirms that there is no evidence to establish occupational exposure to ionizing radiation for this veteran during his active service."

"How can the Navy confirm that I wasn't exposed to ionizing radiation when I lived, ate and slept on (a) contaminated ship that was ... put out of service because it was contaminated with radioactive waste from all the years this dumping took place?" Albernaz said in a letter to the VA. "I am insulted and disappointed."

The VA and Navy came to accept Albernaz was exposed to radiation on the Calhoun County. But his exposure, they said, was very low.

In 2004 the Albernazes moved to New Port Richey from Massachusetts.

* * *

On July 5, 2007, the Albernazes traveled to Washington, D.C., for a hearing at the Board of Veterans Appeals. Derrick went, too. Albernaz was sicker now, hardly able to travel.

Albernaz cried when he described his illness. He recalled a doctor banging his fist on a table while looking at Albernaz's brain scans and saying, "I would give my right eye to know what that is."

The judge seemed sympathetic.

"This is kind of what happened to the Vietnam veterans ... with Agent Orange," hearing judge Lisa Barnard said then. "Nobody knew at the time, but if it kills everything else around, then that would have been a clue that it probably was not a good idea to spray around human beings."

Barnard tried to reassure Albernaz about obtaining incontrovertible proof linking his illness to the ship. "We don't need 100 percent absolute proof. We don't need somebody coming in saying it's beyond all shadow of a doubt this is what caused this. . . . I will try to do something to fix this and sort the situation out."

A month later, the judge sent the case back to the VA in Seminole so it could get more information from the Navy.

Barnard wrote, "This claim must be afforded expedited treatment."

Albernaz wouldn't live to see a final decision.

In August 2009, Albernaz sat up in bed and told his wife he couldn't breathe. Bernice Albernaz rushed him to the emergency room. He had suffered a heart attack. Doctors said he had just days to live.

He was taken to a hospice. Albernaz told his wife to keep fighting to get VA benefits. He told her never to quit. People had to know he had told the truth. "I want my story told," her husband told her.

Albernaz began reciting, almost inaudibly, a Portuguese prayer with a reassuring rhythm. It's a language he knew from his boyhood. His parents' native Portugal is a land of sailors and ships on the cusp of a great but perilous sea.

Hours later, Albernaz died. It was Aug. 8, 2009.

* * *

His wife kept her promise. She continued the fight.

Today, the VA says that even if Albernaz had been exposed to levels of radiation higher than estimates provided by Derrick in her research, he would not have been in danger.

"Mr. Albernaz's exposure ... was far lower than the threshold dose known to cause damage," the VA said in a statement. "Also, his brain necrosis did not occur near the time of exposure, which is normally the case, but instead it occurred some 31 years later."

The Navy maintains the Calhoun County was a safe ship.

Calculations show that "the level of radiation onboard (the) Calhoun County even at the highest levels of potential exposure would not have led to any long-term negative health impacts, according to our radiation health experts."

The Navy declined to release specific radiation dose calculations from the ship because, it says, that would violate the privacy of crewmen.

The Navy said crewmen wore radiation monitors that showed "no monitored personnel received more than the safe occupational limit."

Bernice Albernaz is still appealing the VA's denial of her husband's claim.

"I'll fight them until the end," she said. "It's not about money anymore. My husband died broken-hearted. They have no clue what he went through. I just want to prove he was on the ship. He did what he said he did. These guys did what they said they did. The ship was radioactive. It all really did happen. This story wasn't made up."

The VA sent a letter to Albernaz earlier this year saying it was still gathering evidence.

"This claim," it said, "must be afforded expeditious treatment."

* * *

Civilian workers at Brookhaven, the lab that packaged much of the waste dumped by the Calhoun County, found it difficult to prove their on-the-job exposure to radiation in the Cold War led to cancers some of them suffered. Records were too incomplete. Some workers were never monitored.

So in 2010, the federal government decided they would no longer have to prove their specific radiation exposure to get financial compensation and medical care. If they worked at the lab at least 250 days from 1947 to 1979 and were diagnosed with one of 22 radiation-related cancers, they qualified.

Congress protects military personnel in much the same way. But none of the men who served on the Calhoun County are eligible for automatic VA benefits for radiation illnesses because they did not participate in underwater or atmospheric atomic tests and related activities, the government says.

Thus, the crewmen do not meet their country's definition of "Atomic Veteran."

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USS Calhoun County sailors dumped thousands of tons of radioactive waste into ocean

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They asked the dying Pasco County man about his Navy service a half-century before. He kept talking about the steel barrels. They haunted him, sea monsters plaguing an old sailor. "We turned off all the lights," George Albernaz testified at a 2005 Department of Veterans Affairs hearing, "and ...

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State of the Beach/State Reports/VA/Water Quality - Beachapedia

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Fairview Beach is especially problematic as there was a persistent human signature at all three VDH sampling locations in 2006, and efforts to determine the sources of it will be a focus at Fairview Beach in 2007.

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Good job!

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Industrial facilities dumped over 18 million pounds of toxic chemicals into Virginia's waterways, the second-most in the nation, according to a new report released today by Environment Virginia. Wasting Our Waterways: Industrial Toxic Pollution and the Unfulfilled Promise of the Clean Water Act also reports that 226 million pounds of toxic chemicals were discharged into 1,400 waterways across the country.

"Virginia's waterways are a polluter's paradise right now. Polluters dump 18 million pounds of toxic chemicals into Virginia's lakes, rivers and streams every year," said Laura Anderson, field organizer with Environment Virginia. "We must turn the tide of toxic pollution by restoring Clean Water Act protections to our waterways."

The New River saw the most toxic pollution in the state, with over 12 million pounds dumped into its waters. More than 1.1 million pounds were discharged into the James River, and over 370,000 pounds were dumped into the Shenandoah River.

"The James river is vital to the history and culture of Richmond and Virginia," said Caroline Kory, state associate with Environment Virginia. "We shouldn't be tarnishing our legacy with toxic pollution."

"The Shenandoah River serves to remind us what happens when industrial sites are allowed to pollute," said Jeff Kelble, Shenandoah Riverkeeper. "Before we had the Clean Water Act in 1972, industries contaminated the river with mercury, PCB and other toxic chemicals. People are still unable to eat fish on over 100 miles of the Shenandoah because these toxic chemicals don't break down or go away."

The Environment Virginia report documents and analyzes the dangerous levels of pollutants discharged to America's waters by compiling toxic chemical releases reported to the U.S. EPA's Toxics Release Inventory for 2010, the most recent data available.

Major findings of the report include:

* Virginia's Upper Roanoke watershed is ranked second-worst in the nation for highest amount of total toxic discharges, with over 12 million pounds discharged in 2010.

* Richmond's James River saw over 1.1 million pounds of toxic pollution in 2010.

* 377,090 pounds of toxic pollution were dumped into the Shenandoah River in 2010. Virginia polluters alone dumped 203,480 pounds into the Potomac River, and other states dumped additional toxic pollution for a total of 402,261 pounds into the Potomac in 2010.

Environment Virginia's report summarizes discharges of cancer-causing chemicals, chemicals that persist in the environment, and chemicals with the potential to cause reproductive problems ranging from birth defects to reduced fertility. Among the toxic chemicals discharged by facilities are arsenic, mercury, and benzene. Exposure to these chemicals is linked to cancer, developmental disorders, and reproductive disorders.

"There are common-sense steps that we can take to turn the tide against toxic pollution of our waters," added Anderson.

In order to curb the toxic pollution threatening Virginia's waters, Environment Virginia recommends the following:

* Pollution Prevention: Industrial facilities should reduce their toxic discharges to waterways by switching from hazardous chemicals to safer alternatives.

* Protect all waters: The Obama administration should finalize guidelines and conduct a rulemaking to clarify that the Clean Water Act applies to all of our waterways - including the 33,778 miles of streams in Virginia and 2.3 million Virginians' drinking water for which jurisdiction under the Clean Water Act has been called into question as a result of two polluter-driven Supreme Court decisions in the last decade.

* Tough permitting and enforcement: EPA and state agencies should issue permits with tough, numeric limits for each type of toxic pollution discharged, ratchet down those limits over time, and enforce those limits with credible penalties, not just warning letters.

"The bottom line is that Virginia's waterways shouldn't be a polluter's paradise, they should just be paradise. We need clean water now, and we are counting on the federal government to act to protect our health and our environment," concluded Anderson.

###

Environment Virginia is a state-wide, citizen-funded environmental group working for clean air, clean water and open space. For more information, please visit www.environmentvirginia.org

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Virginia Second-Worst State for Toxic Chemicals Dumped into its Waterways

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Industrial facilities dumped over 18 million pounds of toxic chemicals into Virginia's waterways, the second-most in the nation, according to a new report released today by Environment Virginia. Wasting Our Waterways: Industrial Toxic Pollution and the Unfulfilled Promise of the Clean Water Act also reports that 226 million pounds of toxic chemicals were discharged into 1,400 waterways across the country.

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The city's Public Health Department is warning people not to swim or wade in the ocean between 8th and 22nd streets - a large swath of the resort strip - because bacteria levels exceed the state water-quality standards.

Recent testing showed bacteria levels in the water were above state water-quality standards, according to a news release from the city's Public Health Department.

Water is tested for enterococci, a group of organisms used to determine the extent of the fecal contamination of recreational waters, according to the release. Water samples are taken weekly from May through September. People swimming or playing in waters with bacteria levels higher than the standard have an increased risk of developing gastrointestinal illness as well as skin, eye and respiratory infections, the release stated.

Signs will be posted at the beach in the affected area to alert the public.

"We encourage the public to protect their health by complying with this advisory," said Heidi Kulberg, the health department's director.

"Typically an advisory of this nature is temporary and will be withdrawn once the bacteria levels have returned to safe levels."

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Swimming prohibited in part of the Virginia Beach Oceanfront because of bacteria levels

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The city's Public Health Department is warning people not to swim or wade in the ocean between 8th and 22nd streets - a large swath of the resort strip - because bacteria levels exceed the state water-quality standards. Recent testing showed bacteria levels in the water were above state water-quality standards, according to a news release from the city's Public Health Department.

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Virginia Department of Health
BEACH Monitoring Program

Margaret Smigo, Waterborne Hazards Program Coordinator
109 Governor Street, P.O. Box 2448
Richmond, Virginia 23219
Phone: 804-864-8128

Eastern Shore Health District Jon Richardson, Environmental Health Manager
32191 Front Street
P.O. Box 177
Accomac, VA 23301
Jon.Richardson@vdh.virginia.gov
Ph: 757-302-4271

Hampton Health District Larry Howard, Environmental Health Specialist
1320 LaSalle Ave.
Hampton, VA 23669
Larry.Howard@vdh.virginia.gov
Ph: 757-727-2573

Norfolk City Health District
Marcia Snyder, Environmental Health Supervisor
830 Southampton Ave., Ste. 200
Norfolk, VA 23510
Marcia.Snyder@vdh.virginia.gov
Ph: 757-683-2713

Peninsula Health District
Gary Hagy, Environmental Health Manager
1126 Professional Dr.
Williamsburg, VA 23185
Gary.Hagy@vdh.virginia.gov
Ph: 757-594-7339 or 757-253-4815

Rappahannock Health District
Tommy Thompson, Environmental Health Supervisor
608 Jackson Street
Fredericksburg, VA 22401
tommy.thompson@vdh.virginia.gov
Ph: 540-288-9018 ext. 107

Three Rivers Health District M.B. Sheppard , Environmental Health Supervisor
2780 Puller Highway
P.O. Box 415
Saluda, VA 23149
mb.sheppard@vdh.virginia.gov
Ph: 804-693-6130

Virginia Beach Dept. of Public Health Brad Delashmutt, Environmental Health Supervisor
4452 Corporation Ln.
Virginia Beach, VA 23462
brad.delashmutt@vdh.virginia.gov
Ph: 757-518-2727

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Local Health Department Contacts for Beach Monitoring

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Virginia Department of Health BEACH Monitoring Program Margaret Smigo, Waterborne Hazards Program Coordinator 109 Governor Street, P.O. Box 2448 Richmond, Virginia 23219 Phone: 804-864-8128 Eastern Shore Health District Jon Richardson, Environmental Health Manager 32191 Front Street P.O. Box 177 Accomac, VA 23301 Jon.Richardson@vdh.virginia.gov Ph: 757-302-4271 Hampton Health District Larry Howard, Environmental Health Specialist 1320 LaSalle Ave.

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Menhaden are little guys among fish. But they're huge to a fleet of trawler fishermen and to workers in a Chesapeake Bay town who help turn the catches into pet food and health supplements.

They're also a big deal to other creatures that love to gobble them. Which makes menhaden mighty important to whale lovers and to fishermen who chase bluefish and striped bass.

Those competing demands have fueled decades of debate over whether menhaden are over-harvested, and the General Assembly has been right in the middle. The little fish are the only marine species that state lawmakers regulate.

That distinction will be put to the test once again this year. It's among a slew of environmental issues that lawmakers will confront in the Assembly session that begins Wednesday.

They'll also wade into the choppy waters of oyster ground leases, help decide how much more money the state will invest toward the Chesapeake Bay's cleanup and consider challenging Gov. Terry McAuliffe's control over how to implement federally mandated cuts in power-plant pollution.

In Hampton Roads, no environmental issue is likely to roil the legislature more, however, than menhaden. A dozen of the region's 30 lawmakers have signed on to sponsor bills in the House of Delegates and Senate that would change the way the fishery is managed. The backers come from both parties.

It's an unprecedented level of support for menhaden-related legislation, said Del. Barry Knight, a Virginia Beach Republican who has been pushing for nearly a decade to rein in menhaden fishing.

Knight is the chief patron of House Bills 150 and 151. The first would put regulation of menhaden into the hands of the Virginia Marine Resources Commission, which oversees all other coastal fisheries in the state. The second would forbid the menhaden fleet from using purse nets within a mile of the shores of the bay and its tributaries and within 3 miles of the Atlantic coastline of Virginia Beach.

Last month at a meeting with recreational anglers, Knight heard complaint after complaint about the menhaden fleet's effect on stocks of striped bass and other fish in and around the bay. Roughly 85 percent of the quota for menhaden along the Atlantic Coast comes from Virginia - about 350 million pounds a year.

Virginia's quota remains disproportionately high despite data showing that the number of young menhaden produced in the bay has remained near all-time lows for more than a decade, said Chris Moore, the Chesapeake Bay Foundation's senior scientist in Virginia.

Omega Protein Corp., whose facility in Reedville "reduces" the menhaden catches into other products, is opposed to both of Knight's bills, said Ben Landry, a company spokesman. He said Houston-based Omega is uneasy about the prospect of the nine-member board of the Marine Resources Commission deciding the fate of a company whose Virginia roots go back more than 100 years.

"We'd prefer there be 140 sets of eyes at the General Assembly who would look at it from all walks of life," Landry said. "It's such a politically charged issue that we think it's better that a larger body" control the fishery's fate in Virginia.

Omega has contributed more than $400,000 to political campaigns across the state since 1997, with about $242,000 going to Republicans and $164,000 to Democrats, according to records kept by the nonprofit Virginia Public Access Project.

Landry said Knight's other bill to push the fishery farther from shore "won't do anything, really, to improve the ecosystem. It's just something to say, 'We don't want to see you in our neighborhood.' "

He said Omega has informally agreed to back off from some coastal stretches at certain times of the year but that the mandate called for by Knight would add to the company's costs and make it harder to achieve its catch goal. Menhaden are "near-shore species," he said. "They don't swim in the open ocean."

Knight, at a Chesapeake Bay Foundation-sponsored public forum on menhaden last week, said, "I don't want to run Omega out of business." He said his proposals are just common sense and would help correct an imbalance in fishery management that unfairly favors the company.

He gave his legislation a 50 percent chance of passing this year, adding that in the past he would have rated it a 15 percent shot at best: "We've got more noise on it this year than we've ever had."

Here's a rundown of some other environmental issues to watch for in the General Assembly this session:

Sen.-elect Bill DeSteph, R-Virginia

Beach, has said he will introduce legislation calling for a study of leases of oyster grounds in the Lynnhaven River watershed. That comes after some homeowners along the river filed protests against new proposed oyster grounds, saying the leases would interfere with their recreational water uses and damage property values. DeSteph wants a moratorium on the issuing or transfer of oyster leases in the Lynnhaven while the study is under way. He has already filed another measure, SB102, that would add a 10th member to the board of the Marine Resources Commission, with that spot reserved for a Virginia Beach waterfront property owner. The commissio

n regulates the leases.

The Bay Foundation is hoping lawmakers approve or add to the roughly $62 million that McAuliffe proposed in his latest two-year budget to help farmers fence cattle away from streams or adopt other practices that reduce runoff, said Peggy Sanner, the group's assistant director for Virginia. It's also backing the $59 million he proposed for sewage plant upgrades, and will ask lawmakers to add $50 million a year to the budget to help cities and counties improve stormwater management. The governor zeroed out a special fund for that program in his budget proposal.

HB2, sponsored by Del. Israel O'Quinn, R-Bristol, would require state regulators to get General Assembly approval of any plan to implement a new federal initiative intended to cut carbon dioxide emissions from power plants. Glen Besa, the Sierra Club's Virginia chapter director, said his group will fight the bill and urge McAuliffe, a Democrat, to veto it if the Republican-controlled legislature passes it. He said the bill's intent is to undermine the federal rule, known as the Clean Power Plan.

HB351, offered by Del. Ron Villanueva, R-Virginia Beach, would require the governor to enlist Virginia in a multistate compact that fosters trading of carbon pollution credits. The bill would set aside half of the $250 million a year that environmental groups have estimated it would generate in Virginia to coastal communities, with the money to be used to address rising seas. Separately, McAuliffe's budget proposal to the Assembly includes nearly $2 million for Old Dominion University and the College of William & Mary to establish a joint center for helping communities deal with sea-level rise.

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Little fish tops big list of local environmental issues facing Virginia lawmakers

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Menhaden are little guys among fish. But they're huge to a fleet of trawler fishermen and to workers in a Chesapeake Bay town who help turn the catches into pet food and health supplements. They're also a big deal to other creatures that love to gobble them.

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By: Emma Diet

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Going Green in 2017: The Business Case for Renewable Energy | Article | EESI

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The environmental benefits of expanding renewable energy are clear. Fossil fuels contribute heavily to climate change, which has already begun to have devastating impacts on Earth's ecosystems. But for many, environmental factors are not persuasive enough to shift the attention away from fossil fuels and towards renewable energy: a lot of resources have been invested into fossil fuels, and many assets could end up stranded in a transition to renewable energy.

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Why Is Biodiversity Important? Who Cares? - Global Issues

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Biodiversity is important, more than just the 'I want my children to enjoy it' reason. For example, the richness of diversity allows medicines and foods to be naturally available. The natural disaster prevention mechanisms in most ecosystems and other free services we all get from the surrounding environment are not easily replaceable or replicable, so maintaining biodiversity is important.

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12 PROS and CONS of Wind Energy on the Environment

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Wind turbines use one of our planets 2 best RENEWABLE natural energy sources. Discover the PROS and CONS of wind energy in our full guide!

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Good job, but go more in depth on the reliability. Tell us more about the author or source.

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Abstract

The Elizabeth River system is an estuary in southeastern Virginia, surrounded by the towns of Chesapeake, Norfolk, Portsmouth, and Virginia Beach. The river has played important roles in U.S. history and has been the location of various military and industrial activities. These activities have been the source of chemical contamination in this aquatic system. Important industries, until the 1990s, included wood treatment plants that used creosote, an oil-derived product that is rich in polycyclic aromatic hydrocarbons (PAH). These plants left a legacy of PAH pollution in the river, and in particular Atlantic Wood Industries is a designated Superfund site now undergoing remediation. Numerous studies examined the distribution of PAH in the river and impacts on resident fauna. This review focuses on how a small estuarine fish with a limited home range, Fundulus heteroclitus (Atlantic killifish or mummichog), has responded to this pollution. While in certain areas of the river this species has clearly been impacted, as evidenced by elevated rates of liver cancer, some subpopulations, notably the one associated with the Atlantic Wood Industries site, displayed a remarkable ability to resist the marked effects PAH have on the embryonic development of fish. This review provides evidence of how pollutants have acted as evolutionary agents, causing changes in ecosystems potentially lasting longer than the pollutants themselves. Mechanisms underlying this evolved resistance, as well as mechanisms underlying the effects of PAH on embryonic development, are also described. The review concludes with a description of ongoing and promising efforts to restore this historic American river.

Much of the research concerned with ecological effects of environmental pollution in natural systems has involved lab dose-response studies to determine environmental concentrations that produce negative impacts on variables such as growth, reproduction, and survival in representative or model species that may parlay into population-level effects. Field studies that directly assess population condition, and measure sublethal effects (biomarkers) that may help inform population level effects, also play important roles. Further, studies addressing underlying mechanisms of toxicities are also useful. In addition to undergirding biomarkers, mechanistic studies inform extrapolations across chemicals in the environment and species that are not feasibly tested directly. These approaches have contributed significantly to our ability (1) to set reasonable criteria for chemicals in the environment, (2) to perform meaningful risk assessments, and (3) generally to protect the environment from chemical contamination.

However, an aspect of long-term environmental pollution that these approaches have limited capacity to address is that of adaptations by exposed organisms over multiple generations that improve the abilities of populations to thrive in polluted ecosystems. Of particular importance in this regard is the phenomenon of pollution-driven genetic adaptation, that is, the potential for pollution to act as a significant selection pressure potentially driving evolution. This phenomenon of "evolutionary ecotoxicology" has important ramifications for environmental science and management, including conservation biology, elucidation of fitness costs, and environmental risk assessment and remediation. For example, a site-specific risk assessment based upon an analysis of a population or community that evolved to resist pollution might lead the assessor to underestimate risks by not taking into account fitness costs, reduced genetic diversity, or other unknown consequences.

This review concerns a particular example, or case study, of this phenomenon, stressing biology but including historical, cultural, and management aspects. This story centers on the impacts of a ubiquitous class of environmental pollutants (polycyclic aromatic hydrocarbons [PAH]) on an ecologically important species of fish widespread along the Atlantic seaboard of North America ( Fundulus heteroclitus, often referred to as mummichog or Atlantic killifish) in an estuary of great historical and commercial importance to the United States, the Elizabeth River, Virginia.

THE ELIZABETH RIVER

History

The Elizabeth River is a tidal estuary in southeastern Virginia (). This river consists of the Western, Eastern, and Southern Branches and the Lafayette River that flow through the towns of Chesapeake, Norfolk, Portsmouth, and Virginia Beach-important communities in the Hampton Roads region of Tidewater Virginia. The Southern Branch is the largest, flowing south to north, connecting to the Atlantic Intracoastal Waterway (ICW) near Great Dismal Swamp (which partially feeds the Southern and Western Branches) at its southern origin. After confluence of three branches, the river enters the James River near the mouth of the Chesapeake Bay, approximately 30 km north of its connection with the ICW (). A detailed and fascinating history of the Elizabeth River was written by Amy Waters Yarsinske ( The Elizabeth River, 2007, The History Press, Charleston, SC) and is the primary source of the following historical information.

Captain John Smith was involved in early explorations (circa 1605) of the river; he was sent by King James I of England to explore the Chesapeake Bay in order to establish a harbor for subsequent commerce. Around that time (exact date is uncertain), the river was named for Princess Elizabeth Stuart, the daughter of King James I and sister of Prince Henry and Prince Charles for whom early colonists named the capes at the entrance to the Chesapeake Bay. Following these early explorations, a major port was established on the river, near the mouth of the Chesapeake Bay; it is said to be at present the largest natural harbor in the world. Due to the existence of this harbor, its location on the Eastern Seaboard, and the abundance of natural resources in the area, the Elizabeth River played important roles in American history, particularly in the context of commerce and military activities.

In the late 18th century, the river was prominent in trade with Europe, Great Britain, and the East Indies for various commodities, including Indian corn, lumber, tobacco, naval stores, and rum (which was distilled in the Hampton Roads area). Prior to the Revolutionary War, a Scotsman, Andrew Sprowel, established the Gosport Shipyard on the Southern Branch, just below Portsmouth; the shipyard was established as a British government facility in 1767. In 1776, Norfolk and Portsmouth were bombarded by the British; this sparked reprisals resulting in confiscation of the shipyard by the Commonwealth of Virginia. Subsequently, numerous battles took place on the river during the Revolutionary War. The federal government leased the Gosport Shipyard after the U.S. Navy was created in 1794; 7 years later, in 1801, the government purchased the land and the facility's name was changed to the Norfolk Naval Shipyard in 1862. The shipyard played a major role in building ships for the U.S. Navy during the War of 1812, the Civil War, and World Wars I and II. During World War II the Norfolk Naval Shipyard also served as the primary location for ship repairs-totaling 6,850 vessels.

Physical Changes and Pollution

While commercial and military activities utilizing the Elizabeth River provided numerous benefits for the region and country, they have also had negative impacts on the health of this estuary. Perhaps the most dramatic effect that occurred during early European settlement and subsequent development was the clearing of old growth forests in the region, including riparian habitats lining the river's branches. During the 1800s the river was dredged to roughly double its depth and filled in to about two-thirds of its original width, resulting in the loss of wetlands and shallows that provide critical habitat for many estuarine organisms. During the 19th and 20th centuries, the area's growth in terms of human population, industrialization, naval activities, and shipping contributed to substantial pollution of this relatively poorly flushed estuary. Nutrients and bacteria largely associated with municipal effluents, pesticides in storm sewer runoff, heavy metals and polychlorinated biphenyls (PCB) from various industries, and creosote from wood treatment facilities are among the pollutants that generated the greatest concern, a concern that really materialized in the latter part of the 20th century. In a 1976 report required by the U.S. Environmental Protection Agency (EPA) and the U.S. Congress, the Virginia State Water Control Board called the Elizabeth River one of the worst water pollution problems in the state (Virginia State Water Control Board 1976). In 1993, the U.S. EPA listed the river as one of three regions of concern in the Chesapeake Bay due to chemical contamination (U.S. EPA, 1994); the other two were Baltimore Harbor and the Anacostia River (in Maryland and Washington, DC).

Among the dominant sources of pollution in the Elizabeth River, and of particular relevance to this story, have been wood treatment facilities, an industry that flourished in the area due to abundant timber resources, demand for wood products such as docks and railroad ties resistant to decay, and an extensive rail and water transportation infrastructure for shipping these and other products (Yarsinke 2007). Creosote derived from coal tar was patented and developed for wood treatment in the 1830s and rapidly became the wood treatment of choice for protecting wood from marine wood borers (e.g., Teredo spp. and Limnoria spp.) and other sources of wood decay (Nicholas 1973); it remains the most widely used wood preservative today ( http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=66&tid=18). As its name implies, this form of creosote is derived from the distillation of coal, a commodity of great importance in Tidewater commerce. In the late 19th century Norfolk became the largest coal exporting port in the United States (Foreso et al. 1985), a position it holds through this day ( http://www.eia.gov/todayinenergy/detail.cfm?id=3830). It is unclear how many wood treatment facilities operated in the Elizabeth River system. However, three major plants employing primarily creosote operated for the bulk of the 20th century, all in the Southern Branch-Atlantic Wood Industries, Republic Creosoting, and Eppinger and Russell () (Merrill and Wade 1985). All ceased operations in the latter part of the century. Atlantic Wood Industries was the last to close, in 1990, the same year it was placed on the National Priorities List (for Superfund sites); it is the only wood treatment plant on the Elizabeth to be so designated.

The chemistry of coal-derived creosote is dominated by PAH, which comprise the class of chemical contaminants that have been, and continue to be, of greatest concern in the Elizabeth River (Clark et al. 2013; Huggett, Bender, and Unger 1987; U.S. EPA 1994). In addition to creosote associated with wood treatment, other sources of PAH contamination in the river include coal and petroleum storage and transport facilities and shipbuilding and repair activities (Walker, Dickhut, and Chisholm-Brause 2004). The toxicological effect of PAH that has by far received the most attention and that underlies human health risk assessments is cancer (Luch 2005). Other important effects demonstrated by animal studies include suppression of the immune system (Kaplan et al. 2013) and perturbed development of the cardiovascular system (Billiard et al. 2008). As discussed in the following sections, all of these effects were observed in Elizabeth River killifish and/or in killifish exposed in lab studies to extracts of Elizabeth River sediments and to PAH present in the sediments. Killifish are a useful model to evaluate effects on other biota in this system, the majority of which are less amenable to field and lab studies.

OVERVIEW OF ELIZABETH RIVER PAH CONTAMINATION AND BIOLOGICAL IMPACTS

Polycyclic Aromatic Hydrocarbons in Sediments

The earliest published report we are aware of that addressed PAH pollution in the Elizabeth River is by Merrill and Wade ( 1985). This study included sediment analyses from five sites in the Southern Branch, including sites near the three wood treatment facilities noted earlier. An important conclusion of their study was that creosote was the major contributor of priority (i.e., carcinogenic) PAH in the river. A report shortly thereafter by Bieri et al. ( 1986) appears to comprise the first comprehensive analysis of PAH in the Elizabeth River system. This study measured PAH in sediment samples from 28 sites in the river, including sites from all three branches as well as the main stem downstream of the confluence of the branches. The highest PAH concentrations were observed in the vicinity of the wood treatment sites, including a maximum of 170 ppm for the sum of 14 pyrogenic PAH measured. (Note: All PAH concentrations in this review are expressed on a dry weight basis, as cited in the papers.) Bieri et al. ( 1986) concluded that creosote spills from wood treatment facilities were the likely source of these PAH. Moreover, a comparison made with data from four other PAH hotspots in the United States indicated that the Elizabeth River sediments contained the highest maximum PAH concentrations among these five sites.

Several studies published since Bieri et al. ( 1986) confirmed the high level of PAH contamination, the importance of wood treatment facilities in the Southern Branch, and added additional information concerning PAH dynamics in the system and impacts on biota in the estuary. Based on data collected in 1983 from 14 sites encompassing approximately 14 km in the main stem and Southern Branch, Huggett, Bender, and Unger ( 1987) concluded that the Elizabeth River was the most polluted estuary in Virginia, and that PAH emissions from wood treatment plants were the primary source of this pollution. This study also observed correlations between higher sediment PAH concentrations at different sites and higher tissue concentrations of PAH in deployed oysters, reduced fish biomass, decreased numbers of individual fish, and an increased occurrence of gross abnormalities in fish (fin erosion and eye lens cataracts). Huggett et al. ( 1992) summarized data from sediment surveys and fish trawls performed during the period of 1980-1989 and covering the entire 28 km of the subestuary (main stem and Southern Branch). Sediment chemistry again indicated a general increase in PAH concentrations as one moved from the mouth of the river to upstream sites near the wood treatment plants. A maximum total PAH concentration of 15 g/kg (1.5% or 15,000 ppm) was observed in sediments adjacent to a wood treatment facility. Results from the fish trawls also noted associations between sediment PAH concentrations and various lesions, similar to those reported by Huggett, Bender, and Unger ( 1987).

Walker and Dickhut ( 2001) used isomer ratios of selected PAH and molecular weight fractions to track PAH sources in the river (main stem and Southern Branch), using samples collected in 1999. Data showed that creosote from wood treatment plants was the predominant source, but that coal and/or coal gasification plants were also important in some areas. They noted interesting differences between the two plants that were focused on-Eppinger and Russell, and Atlantic Wood. Sediments adjoining Eppinger and Russell displayed higher total PAH concentrations (approximately 10× for maximal values) than those associated with Atlantic Wood. However, Atlantic Wood samples were more enriched in high-molecular-weight compounds (more associated with cancer than low-molecular-weight PAH). It is also noteworthy that despite the lower levels of PAH near Atlantic Wood, evidence indicated that this facility was a more important contributor of PAH into the main channel of the river, perhaps due to differences in hydrology. Similar conclusions were made by a subsequent report by Walker et al. ( 2005) that incorporated principal component analysis into the data analysis. It was also noted that historical and/or current coal transport and use were likely important sources of PAH at some sites in the river.

A related report by Walker, Dickhut, and Chisholm-Brause ( 2004) involved the analysis of sediment samples collected in 1998-1999 (perhaps overlapping samples from the studies already described), including samples from near the mouth of the river (near Craney Island) to 22 km south of the mouth (which is several kilometers south of the wood treatment facilities; ). Again, the highest total PAH concentrations were found in samples for shoal areas near Atlantic Wood (740 ppm maximum) and Eppinger and Russell (1730 ppm maximum). The highest level observed in the main stem (just north and downstream of the confluence of the Southern and Eastern Branches) was 52 ppm, and was suspected to be due to a coal gasification plant. Included in this study was a comparison of these data with findings collected in 1983 (Huggett, Bender, and Unger 1987), about 15 years earlier. Sediment concentrations for most of the 10 PAH compared had declined at most sites, with calculated half-lives from 5 to 25 years. However, no significant decreases occurred for most PAH at 4 of 13 sites compared. At one site (between Eppinger and Russell and Atlantic Wood), increases were noted for three PAH with no change in the remaining 7. Notably, higher-molecular-weight PAH, including carcinogenic compounds, generally displayed slower removal rates. Walker, Dickhut, and Chisholm-Brause ( 2004) also compared their Elizabeth River findings with data from 16 other sites globally, including several PAH hotspots. Total PAH in shoal areas near wood treatment facilities in the Elizabeth River (740-1730 ppm) exceeded the highest levels reported for other contaminated sites including Tokyo Bay (˜300 ppm), Sidney Harbor (˜400 ppm), and Boston Harbor (˜400 ppm). Non-source-specific areas in the river's channel (˜60 ppm) were below these three locations, but greater than most other sites included in the comparison. For example, PAH concentrations in the nearby York River were ˜3 ppm ().

Two reports by Vogelbein and Unger (2003; 2008) to the Virginia Department of Environmental Quality provided extensive data for various sites in the Elizabeth River system, including the three branches, the Lafayette River, and sites proximate to former wood treatment facilities. Average total PAH concentrations for selected sites () from the 2003 and 2008 reports are included in . Note that samples for the 2003 and 2008 reports were collected in 2001 and 2007, respectively, and the 2008 report added several sites in the vicinity of Money Point. The Money Point area includes sites that were impacted by the Eppinger and Russell facility (on land now owned by Hess Corporation) that are presently undergoing remediation. These reports also include observations of fish pathology surveys that are described later. Sediment data () demonstrate continued highly elevated PAH concentrations near wood treatment facilities years to decades after cessation of plant operations. Moderate to low levels were reported in the Southern Branch downstream of the facilities, in the Western and Eastern Branches, and in the Lafayette River. Generally low concentrations were observed upstream of the facilities in the Southern Branch. Sediment PAH data provided by Clark et al. ( 2013) for samples collected in 2008 are not directly comparable due to differences in sampling sites and chemical analyses, but demonstrate a similar spatial distribution. It is also noteworthy that collectively data from Vogelbein and Unger (2003, 2008) did not indicate widespread declines of PAH levels in this system over this time frame. There are apparently no more recent sediment data available.

TABLE 1.

Biological Responses Associated With Pollution

In addition to these studies addressing chemical contamination of the Elizabeth River, numerous studies examined biological responses potentially associated with pollution in the river. The vast majority of investigations described in this section, as well as those assessing sediment chemistry described earlier, was carried out by scientists at the Virginia Institute of Marine Science (VIMS), a component of the College of William and Mary. The earliest reports of biological effects that were available are those by Hargis, Roberts, and Zwerner ( 1984) and Weeks and Warinner ( 1984). The former study involved exposures of spot ( Leiostomus xanthurus) from an uncontaminated estuary (Ware River, VA) to sediments from a creosote-contaminated location in the Southern Branch of the Elizabeth River. Compared to control fish, exposed spot exhibited severe skin, fin, and gill erosion, reduced hematocrits, and pancreatic and liver lesions. Several other early field investigations also noted various internal and external lesions in a variety of species captured in the Elizabeth River (Huggett, Bender, and Unger 1987; 1992; Thiyagarajah, Zwerner, and Hargis 1989). A lab study by Sved, Roberts, and VanVeld ( 1997) exposed spot to sediment amended with low- or high-molecular-weight fractions of creosote (both PAH primarily) and concluded that the high-molecular-weight fraction accounted for lesions and mortality.

Several investigations addressed immune function in Elizabeth River animals. In a companion study to Hargis, Roberts, and Zwerner ( 1984), Weeks and Warinner ( 1984) collected from the Elizabeth and Ware rivers spot and hogchokers ( Trinectes maculatus), from which they collected kidney macrophages and assessed phagocytosis. Phagocytic activity was reduced in both species from the Elizabeth River following exposures, but rebounded after several weeks in clean water. These observations were consistent with those of a subsequent paper (Faisal et al. 1991) that found suppressed phagocytic activity by leukocytes from killifish captured in the Elizabeth River compared to killifish from a reference site in the York River. Chu and Hale ( 1994) and Chu et al. ( 2002) examined the effects of Elizabeth River sediment extracts on several aspects of immune function in the eastern oyster ( Crassostrea virginica), including susceptibility to the protozoan parasite Perkinsus marinus (dermo). These studies demonstrated enhanced disease expression in exposed oysters, which may be of importance in light of the long-standing concerns for this disease in the Chesapeake Bay region.

Perhaps the disease of greatest concern that is associated with chemical pollution, particularly by PAH, in the Elizabeth River is cancer. Killifish, particularly fish collected from near the Atlantic Wood Industries site, have been the focus of this phenomenon. The first report in this vein appears to be by Hargis et al. ( 1989), who reported a 2% incidence (among 398 fish necropsied) of exterior neoplasms, mainly in the mouth area. This also appears to be the earliest publication concerning pollution effects on Elizabeth River killifish, the focus of this review. Vogelbein et al. ( 1990) found that effects on liver tissue were more severe. Of the 60 killifish collected from the Atlantic Wood Industries site, 93% exhibited grossly visible liver lesions and 35% displayed frank hepatocellular neoplasms (i.e., liver cancer). Subsequently, Stine et al. ( 2004) provided detailed information concerning the nature of these lesions. Rose et al. ( 2000) observed highly elevated levels of hydrophobic DNA adducts in hematopoietic tissues (liver, kidney, spleen) and blood in killifish from this site, whereas none were detected in reference site fish. These adducts, likely derived from PAH, provide a plausible link between PAH exposures and cancer in these fish. Further, Vogelbein and Unger (2003, 2008) described findings that appear to be the most extensive and most recent surveys of liver pathologies in the Elizabeth River system. These reports include fish collected from 16 sites covering all three of the branches of the Elizabeth River and the Lafayette River. Evidence in the 2008 report indicated that overall the incidence of liver disease, including cancer, had not changed significantly from the previous survey, and that the environmental quality of the system remained significantly impaired. These studies support the utility of liver disease in killifish as an effective measure and bioindicator of estuarine contamination, at least for PAH.

In apparently the earliest report of biochemical effects, Roberts, Sved, and Felton ( 1987) measured activities of superoxide dismutase (SOD) and aryl hydrocarbon hydroxylase (AHH) in livers of spot, again collected over several months from the Elizabeth and Ware rivers. SOD is an antioxidant enzyme, while AHH was an early assay for cytochrome P-450 (CYP1A) activity, a key part of the aryl hydrocarbon receptor (AHR) pathway that is described later (, shown later). For both activities, Roberts et al. (1987) noted significant but inconsistent elevations in Elizabeth River fish relative to Ware River fish. Using more advanced techniques for measuring CYP1A, a seminal paper by Van Veld and Westbrook ( 1995) examined killifish from several sites, including Atlantic Wood Industries, and showed that while field-collected fish had higher basal activities than reference-site fish, they were remarkably recalcitrant to enzyme induction by a potent inducer. This study and a VIMS master of arts thesis (Williams 1994) demonstrated the resistance of offspring of this same population to acute toxicity induced by Atlantic Wood Industries sediments, which was the original motivation for the subject of this review: pollution-driven evolution in Elizabeth River killifish.

THE ATLANTIC KILLIFISH OR MUMMICHOG (Fundulus heteroclitus)

Basic Biology

The Atlantic killifish is a small teleost fish found in estuarine ecosystems along the Atlantic coast of North America from New Brunswick to Florida (Shute 1980). This species has a lifespan of about approximately 3-4 years, is sexually dimorphic, and reaches sexual maturity at less than 1 yr old (Abraham 1985) (). It is among the most abundant intertidal fish and a major component of estuarine food webs (Yozzo et al. 1994; Teo and Able 2003a). Killifish are omnivorous feeders; reported food sources include plant detritus, macroalgae, grass shrimp, crabs, annelids, and other fish (Kneib 1986; Kneib and Stiven 1978; Allen et al. 1994; McMahon, Johnson, and Ambrose 2005; Able et al. 2007). In turn, killifish are prey for birds, fish, and invertebrates (Post 2008; Nemerson and Able 2003; Kneib 1982). In general, killifish spawn near the high tide line on a semilunar schedule concurrent with tidal changes (Taylor et al. 1979).

In addition to their important role in estuarine ecosystems, killifish have a number of attributes that make them a unique and popular research species for environmental research (Burnett et al. 2007). Killifish are tolerant of significant variation in environmental conditions, including salinity, temperature, oxygen, and pH (Gonzalez, Mason, and Dunson 1989; Dunson, Fricano, and Sadinski 1993; Wood and Marshall 1994; Smith and Able 2003; Stierhoff, Targett, and Grecay 2003; Nordlie 2006). They are easy to capture and maintain, amenable to manual spawning, and highly fecund, with a single female able to produce up to several hundred eggs at once. Eggs (about 1-2 mm in diameter) have a transparent chorion that facilitates observation of development and stages of embryonic development and organogenesis that are well known (Armstrong and Child 1965). Despite wide distribution, individual killifish have relatively small home ranges (Lotrich 1975; Skinner et al. 2005) and are ideal for studying impacts of local contamination and other stressors (Mulvey et al. 2002, 2003; Burnett et al. 2007; Eisler 1986; Teo and Able 2003b, 2003a). Further, their tolerance to a wide variety of environmental conditions such as variations in salinity, dissolved oxygen, and temperature has made them an extremely useful model to investigate adaptation to environmental changes.

Role of Killifish in Environmental Adaptation Research

Osmoregulation

Killifish have played an important role in the study of osmoregulation and continue to be an important model in this field. Tolerance to an extreme range of salinity from freshwater to hypersalinity as high as 120‰ (Griffith 1974), has made them a valuable tool for studying accommodation to both fresh and salt water, yielding critical contributions to the understanding of teleost osmoregulation (Evans 2008; Evans, Piermarini, and Choe 2005; Burnett et al. 2007). Of particular importance was their contribution to the development of the model of NaCl excretion in what are now known as mitochondria rich cells (MRC) but were formerly known as chloride cells. Karnaky and coworkers (1976) localized the Na⁺,K⁺-ATPase responsible for Na⁺ excretion in killifish MRC and also showed the role of the same cells in Cl- excretion (Degnan, Karnaky, and Zadunaisky 1977; Karnaky, Degnan, and Zadunaisky 1977). Later, Marshall et al. ( 1995) identified the channel responsible for Cl- excretion, and Singer et al. ( 1998) cloned the channel, which is a homologue of the mammalian cystic fibrosis transmembrane conductance regulator. These discoveries helped to complete the model of NaCl secretion in marine teleosts that is still used today.

Hypoxia response

Killifish thrive in areas with variable and often low dissolved oxygen (O ₂) concentrations. A number of studies showed that killifish survive exposure to dissolved O ₂ levels as low as 1 mg/L (Stierhoff, Targett, and Grecay 2003; Smith and Able 2003; Wannamaker and Rice 2000). In fact, killifish may be more tolerant of hypoxia than other common estuarine fish, including Cyprinodon variegatus (sheepshead minnow), Lucania parva (rainwater killifish), and Menidia beryllina (inland silverside) (Smith and Able 2003). In addition, unlike other estuarine species, killifish did not exhibit avoidance of water with low dissolved O ₂ in lab choice experiments (Wannamaker and Rice 2000). One important behavior that helps killifish greatly in low O ₂ conditions is utilization of the more air-saturated surface of the water, which is known as aquatic surface respiration (ASR) (Stierhoff, Targett, and Grecay 2003; Wannamaker and Rice 2000; Greaney et al. 1980).

To cope with chronic exposure to low O ₂ conditions, killifish undergo a number of physiological changes. Their hematocrit and hemoglobin O ₂ affinity increase to augment the O ₂-binding capacity in blood (Stierhoff, Targett, and Grecay 2003; Greaney et al. 1980; Greaney and Powers 1977). In addition, killifish shift toward anaerobic metabolism, via glycolysis, to supplement energy production during O ₂ tension. This is reflected in increased blood and tissue concentrations of lactate observed in this species under O ₂ stress (Cochran and Burnett 1996; Greaney et al. 1980). In addition, increases in the activity of multiple glycolytic enzymes have been documented in killifish exposed to chronic hypoxia (Kraemer and Schulte 2004; Greaney et al. 1980).

Temperature adaptation

In addition to tolerating a wide range of salinity and O ₂ conditions, killifish populations are distributed in habitats along a thermal gradient that covers approximately 12°C. This has resulted in adaptive differences between populations at the extremes of this range and made killifish an important model for study of molecular evolution and environmental adaptation (Schulte 2001). In a series of studies from the late 1970s through the early 1990s, Powers at Stanford University and colleagues investigated the mechanisms underlying this adaptation. Examination of genetic variation among killifish populations along this temperature gradient showed that there are distinct northern and southern genotypes of killifish (Bernardi, Sordino, and Powers 1993). In particular, research focused on the glycolytic enzyme heart-type lactate dehydrogenase (Ldh-B), which was found to exist as two predominant allozymes that had significant differences in enzyme activity at different temperatures (Place and Powers 1979). Specifically, Ldh-B associated with northern populations exhibited a higher reaction rate at lower temperatures, whereas Ldh-B associated with southern populations exhibited a higher reaction rate at higher temperatures. In addition, northern populations possess significantly higher overall levels of Ldh-B transcription (Crawford and Powers 1989; 1992). Eventually, the observed differences in transcription were attributed to differences between populations in the sequence of the promoter region (Schulte, GomezChiarri, and Powers 1997; 2000). These findings were strongly correlated to whole organism performance tests. Individuals homozygous for the northern Ldh-B allele were found to swim faster at lower temperatures than individuals homozygous for the southern allele (DiMichele and Powers 1982).

Recent development as a molecular model

Because killifish successfully inhabit and tolerate a wide variety of environmental conditions, they have great potential for investigation of genome-environment interactions (Burnett et al. 2007). In addition to the advantages of studying wild populations that face significant daily variation in environmental stressors such as temperature, salinity, and dissolved O ₂, killifish may be compared to their diverse relatives in the family Fundulidae or to other popular fish models, such as zebrafish ( Danio rerio). Further, the killifish genome has now been fully sequenced; it is currently being assembled and annotated, but is already available to the community in its current form ( https://my.mdibl.org/display/FGP/Home). Utilizing the newly sequenced genome, resequencing of individuals from the major adapted killifish populations is underway in multiple labs to identify the genomic signatures of pollution adaptation. However, significant progress has already been made using transcriptomic and other molecular approaches to study pollutant responses in killifish.

Several studies used differential display or subtractive hybridization to examine gene expression in response to contaminants. Meyer et al. ( 2005) employed this approach to identify genes differentially expressed in PAH-tolerant and -susceptible populations. Suppressive subtractive hybridization was used to develop "fingerprints" of exposure to the PAH anthracene and pyrene (Peterson and Bain 2004; Roling, Bain, and Baldwin 2004) and to discern the impact of arsenic exposure on gene expression in offspring (Gonzalez et al. 2006). Other studies used cDNA arrays to investigate the effects of chromium, both in lab exposures and in fish from contaminated sites (Roling et al. 2006; 2007; Roling and Baldwin 2006). In addition, multiple researchers compared gene expression among populations from a series of polluted and reference sites; several of these studies included the Elizabeth River population and are discussed later.

Killifish microarrays have also been used to investigate evolution of regulation of gene expression (Crawford and Oleksiak 2007; Whitehead and Crawford 2006b). Studies in killifish enable investigators to compare variation in expression among individuals within distinct populations, between populations, and across related Fundulidae. Several studies demonstrated a high degree of variation in gene expression among and within populations and between taxa that is likely to be evolutionarily important (Whitehead and Crawford 2006a; Oleksiak, Churchill, and Crawford 2002; 2005).

Several transgenesis techniques have been employed in killifish, and their use is likely to expand with the sequencing and ongoing annotation of the genome. The feasibility of transgenesis was demonstrated by Winn, Vanbeneden, and Burkhart ( 1995), who developed a model of in vivo mutagenesis in killifish. Further, morpholino gene knockdown was recently adapted for use in killifish. Morpholinos are antisense oligonucleotides that may be used to transiently block translation of targeted mRNAs. They are particularly useful for studying gene function during development in fish. In killifish, morpholino knockdown of CYP1A was used to validate the technique and investigate the synergistic effects generated by AHR agonists and CYP1A inhibition (Matson et al. 2008). Morpholino knockdown was also used to demonstrate which of the two known killifish AHR mediates PAH toxicity during development (Clark et al. 2010). The AHR pathway is illustrated and described in directly after this section, and the subject of AHR-mediated toxicity is expanded upon later. In addition, morpholinos have been used to efficiently block translation of serum glucocorticoid kinase 1 and mitogen activated protein kinase 14-1 in studies of seawater acclimation (Notch et al. 2011; 2012) . Following the completion of genome annotation and assembly, there appear to be no barriers to the extensive use of these and other molecular methods in killifish.

THE POLLUTION-ADAPTED PHENOTYPE

Discovery of PAH Resistance in Elizabeth River Killifish

As described previously, initial studies in and around the Atlantic Wood Industries Superfund Site on the Elizabeth River focused on severe acute toxicity affecting a wide variety of fish; data clearly showed that organisms in the estuary were highly impacted by creosote contamination. After the observation of neoplasia in killifish, further attention was focused on that particular species. Given their relatively nonmigratory nature, the Atlantic Wood killifish population appeared likely to be a stable, persistent population that was exhibiting tumors primarily due to long-term residence in a highly creosote-contaminated habitat. Despite the severity of tumorigenesis in killifish resident at this site, it appeared that Atlantic Wood killifish were somehow capable of circumventing many of the acute toxic effects seen in spot and other fish and managing to thrive despite highly elevated pollutant exposures. Studies in several labs addressed and are continuing to examine this remarkable degree of resistance, including the elucidation of underlying mechanisms.

Evidence of resistance of Elizabeth River killifish to effects of PAH was first published by Van Veld and Westbrook ( 1995). In this study, cytochrome P-4501A (CYP1A) response was compared in adult fish collected from the Atlantic Wood site and two reference sites (Wilson Creek and King's Creek, both north of the mouth of the York River, in Gloucester County, VA). CYP1A is a major enzyme involved in Phase I, oxidative biotransformation of xenobiotics. It is highly inducible by exposure to a wide-range of chemicals, including PAH and other aryl hydrocarbons (). As might be expected, CYP1A levels in freshly caught fish were elevated in Atlantic Wood fish in comparison to reference fish (5-fold in liver, 56-fold in gut). However, following intraperitoneal (ip) injection of the PAH 3-methylcholanthrene (3-MC), hepatic expression of CYP1A protein increased 418-fold in reference (King's Creek) fish but was not significantly changed in Atlantic Wood fish. Van Veld and Westbrook ( 1995) also compared CYP1 activity following 3-MC injection using the ethoxyresorufin O-deethylase (EROD) assay, a fluorescence-based measurement of CYP1 catalysis, and EROD activity followed the same trend as CYP1A protein. Further, when each group was exposed to contaminated Elizabeth River sediments, hepatic CYP1A protein expression and EROD activity were markedly elevated in fish from the reference site compared to levels measured in fish from the Atlantic Wood site. In total, data demonstrated that fish from the Atlantic Wood site exhibited a remarkable recalcitrance to induction of CYP1A by PAH.

Characterization of PAH Resistance in Elizabeth River Killifish

After identification of this striking resistance by Atlantic Wood killifish to one of the major biological responses to PAH exposure, greater attention was focused on characterizing the breadth of PAH resistance of Elizabeth River killifish. Due to the probability of close contact with contaminated sediments and potential for increased sensitivity in early life stages, effects on embryos were, and continue to be, of particular interest. Further, it is likely that heritable PAH adaptation is driven by acute toxicity and early-life-stage effects that might impact reproductive success, rather than chronic conditions such as cancer. Ownby et al. ( 2002) investigated early-life-stage toxicity induced by PAH-contaminated sediments in killifish embryos from populations inhabiting four sites on the Elizabeth River, including the Atlantic Wood site, and a reference population on the nearby York River. Sediment PAH concentrations detected among the Elizabeth River sites ranged from 3.9 ± 3.2 to 264 ± 115 mg/g (ppm, dry weight, sum of select PAH). Field-collected adults were manually spawned in the lab, and tolerance of their offspring to Atlantic Wood site sediment was compared. Embryos obtained from the reference population suffered from a variety of cardiac abnormalities, including tube hearts, reduced circulation, and pericardial swelling, but embryos from Atlantic Wood parents showed a dramatic and near-complete resistance to these effects. The observed cardiovascular defects were similar to the suite of deformities known as blue-sac disease produced by some halogenated aromatic hydrocarbons such as 3,3',4,4',5-pentachlorobiphenyl (PCB-126) and 2,3,7,8-tetrachlorodibenzodioxin (TCDD) (Peterson, Theobald, and Kimmel 1993). (These halogenated compounds that exert toxicity via agonism of the AHR are commonly referred to as "dioxin-like compounds" or DLC. Some PAH including several occurring in the Elizabeth River are also AHR agonists.) Ownby et al. ( 2002) also showed that embryos from other Elizabeth River populations showed an intermediate degree of tolerance to the same effects. The degrees of resistance were roughly associated with sediment PAH concentrations at the sites of collection, perhaps reflecting population exposure histories. In addition, Ownby et al. ( 2002) tested the heritability of tolerance by exposing F2 embryos obtained from lab-reared F1 adults. The F2 embryos exhibited a degree of tolerance similar to that exhibited by F1 embryos, indicating that resistance was heritable.

The resistance of Atlantic Wood killifish to PAH (Meyer, Nacci, and Di Giulio 2002; Meyer and Di Giulio 2003) and PCB-126 (Meyer and Di Giulio 2002) was further investigated. In addition to examining resistance to toxicity from contaminated sediments and PAH, these studies further determined the pattern and heritability of recalcitrant CYP1A response previously observed in adult Elizabeth River killifish by Van Veld and Westbrook ( 1995). Despite sediment contamination dominated by PAH and not DLC including PCBs, F1 Atlantic Wood embryos were highly resistant to cardiac teratogenesis and induction of CYP1 activity generated by PCB-126 exposure (Meyer and Di Giulio 2002). In fact, data indicated that both F1 and F2 Elizabeth River killifish were even more resistant to PCB-126 than adapted killifish from DLC-contaminated sites in Newark Bay, NJ, and New Bedford Harbor, MA (Nacci, Champlin, and Jayaraman 2010). Atlantic Wood F1and F2 embryos were also resistant to developmental abnormalities and mortality observed in reference embryos exposed to Elizabeth River sediment pore water (Meyer, Nacci, and Di Giulio 2002; Meyer and Di Giulio 2003). Typical effects on the developing cardiovascular system observed in reference embryos but not Atlantic Wood embryos are displayed in . In addition, Atlantic Wood F1 embryos were recalcitrant to induction of CYP1A by the AHR agonist-type PAH 3-MC and β-naphthoflavone (BNF).

However, in some studies resistance was not consistently heritable. PCB-126-induced EROD activity in F3 embryos (F2 were not tested) returned to levels similar to those of reference embryos; at the highest doses tested, resistance by F3 embryos to the teratogenic effects of PCB-126 was intermediate between the highly resistant F1 embryos and susceptible reference embryos (Meyer and Di Giulio 2002). Similarly, recalcitrance to CYP induction was largely lost in F3 embryos and F2 larvae dosed with 3-MC, BNF, or sediment pore water (Meyer, Nacci, and Di Giulio 2002; Meyer and Di Giulio 2003). In addition, hepatic EROD activity in adult Atlantic Wood F2 and even F1 adults exposed to Elizabeth River sediments was found to be similar to that of adult reference fish. In contrast to the results of Ownby et al. ( 2002) and Nacci, Champlin, and Jayaraman ( 2010), these studies by Meyer and colleagues (2002) seemed to demonstrate that the resistance was heritable but not fully genetic, and it was proposed that this might be achieved through epigenetic regulation of CYP1A. However, Timme-Laragy et al. ( 2005) found no marked differences between methylation status of CpG sites in the CYP1A promoter of Elizabeth River and reference fish. Interestingly, hybrid embryos generated by crossing Atlantic Wood fish of either sex with reference fish demonstrated a BNF-induced EROD response intermediate between those of reference and Atlantic Wood embryos (Meyer, Nacci, and Di Giulio 2002). In a subsequent study, survival of hybrid larvae exposed to diluted Elizabeth River pore water was intermediate between that of Atlantic Wood and reference larvae (Meyer and Di Giulio 2003). In both cases, the response of the two hybrid lines was nearly indistinguishable, regardless of the sex of the parent from the Atlantic Wood population. These results seem to be more consistent with a hypothesis of genetically heritable resistance, transmitted by both male and female Atlantic Wood fish.

It is difficult to reconcile the results of Meyer and coworkers (2002) with those of Ownby et al. ( 2002) and Nacci, Champlin, and Jayaraman ( 2010), although it is notable that some data obtained by Meyer, Nacci, and Di Giulio ( 2002) supported a conclusion of genetic heritability, but others do not. Further contributing to this complex picture, Clark, Bone, and Di Giulio ( 2014) recently found that while F1 and F2 Atlantic Wood embryos were strongly resistant to teratogenesis induced by several PAH and PCB-126, their resistance to induction of CYP1A, CYP1B1, and CYP1C1 mRNA and EROD activity was reduced in F2 embryos, which suggested that only some aspects of the resistance were genetically inherited. In general, the strongest evidence for full genetic heritability has been observed for resistance to teratogenesis in embryos, while studies of heritable resistance in larvae and adults yielded mixed results. Further, the resistance to toxicity and the refractory CYP response seem to decrease with age or after generations of lab rearing, perhaps indicating that some components of the adaptation are life-stage specific or not genetically heritable. It is also possible that resistant fish are less fit under clean conditions, causing some lab populations to undergo "reverse" selection, yielding less resistant offspring in later generations (Meyer and Di Giulio 2003).

Mechanisms of PAH Resistance in Elizabeth River Killifish

Phase II conjugation enzymes

Multiple studies addressed the mechanisms underlying adaptation of Elizabeth River Fundulus to acute toxicity and teratogenesis produced by PAH mixtures. Early in the study of the Atlantic Wood population, investigators discovered elevated expression of a number of xenobiotic metabolizing enzymes. Phase II enzymes, such as glutathione S-transferases (GST), act to conjugate xenobiotics, increasing their solubility and enhancing their excretion from the body. In an investigation of the hepatic lesions in Atlantic Wood killifish, Van Veld et al. ( 1991) noted that hepatic and intestinal GST activity was elevated three- to fourfold in Atlantic Wood fish with respect to reference fish. Armknecht, Kaattari, and Van Veld ( 1998) postulated that elevation in GST might contribute to the PAH resistance. They confirmed earlier findings (Van Veld et al. 1991) of elevated GST activity in Atlantic Wood fish and also a concomitant rise in protein levels. In both studies, GST elevation was found to be intermediate in fish from a site with intermediate levels of PAH, perhaps indicating that increased GST was a marker of exposure rather than an adaptive change. However, hepatic GST activity was not induced in reference fish fed a BNF-amended diet (Van Veld et al. 1991). Gaworecki, Rice, and Van Den Hurk ( 2004), observed elevated activity of the Phase II enzyme UDP-glucuronosyltransferase (UGT) in Atlantic Wood killifish when compared to reference fish. In addition, a numerical rise in sulfotransferase (SULT) activity was noted, although overall level of activity measurable in killifish was low. Further, Cooper, Vogelbein, and Van Veld ( 1999) demonstrated that the xenobiotic transporter p-glycoprotein (Pgp, some of which are also known as ATP-binding cassette transporters or multidrug resistance proteins) was expressed at levels two- to threefold higher in Atlantic Wood fish than in reference killifish. Pgp, sometimes referred to as Phase III metabolizing enzymes, are membrane transport ATPases that are involved in the efflux of compounds. Although these proteins have been identified in a variety of normal tissues, they are also frequently elevated in multidrug-resistant cell lines and chemotherapy-resistant tumors (Abu-Qare, Elmasry, and Abou-Donia 2003). Thus far, the heritability of these elevated Phase II and III responses has not been investigated. Thus, it is not clear whether Pgp are components of heritable adaptation, acclimatory responses, or simply reflect toxic reactions to PAH exposure.

Oxidative stress

In addition to perturbations in AHR-mediated signaling, PAH produce toxicity via oxidative stress due to metabolism or photo-modification to products that generate reactive oxygen species (ROS) (Arfsten, Schaeffer, and Mulveny 1996). For this reason, Meyer et al. ( 2003a) hypothesized that upregulation of antioxidant defenses might be an important component of resistance to stressors in the Elizabeth River environment. Data demonstrated that exposure to Elizabeth River sediments led to increases in several antioxidant defenses, including total glutathione (GSH), glutathione reductase (GR) activity, and manganese superoxide dismutase (MnSOD) protein, in both Elizabeth River and reference fish. Studies with zebrafish established that, as with Elizabeth River sediments, a mixture of BNF and α-naphthoflavone (ANF) that produced cardiac malformations also induced expression of a battery of antioxidant response genes (Timme-Laragy et al. 2009). To further examine the role of oxidative stress in the synergistic toxicity of BNF and ANF, Timme-Laragy et al. ( 2009) used morpholino knockdown of NF-E2-related factor 2 (Nrf2) expression. Nrf2 is a transcription factor that controls expression of a variety of antioxidant defenses (Kaspar, Niture, and Jaiswal 2009), and knockdown of its transcription resulted in exacerbation of BNF and ANF mixture toxicity.

Given data showing the potential for PAH mixtures to generate oxidative stress, it was not surprising that Elizabeth River killifish differed from reference fish in their response to oxidative stressors ("pro-oxidants"). Elizabeth River F1 and F2 larvae were more resistant than reference larvae to the model pro-oxidant t-butyl hydroperoxide (Meyer et al. 2003a). Compared to reference fish, whole-body homogenates of Elizabeth River F1 or F2 larvae also displayed greater total oxygen scavenging capacity (TOSC), quantitatively elevated total GSH levels, and higher MnSOD protein expression. Total GSH levels were particularly increased in larval liver. In a subsequent study, wild-caught Elizabeth River adults exhibited higher hepatic total GSH and selenium-independent glutathione peroxidase (GPx) activity; however, selenium-dependent GPx activity was higher in reference fish (Bacanskas, Whitaker, and Di Giulio 2004). Mitochondrial lipid peroxidation was elevated in Elizabeth River fish relative to reference fish, despite the observed increases in antioxidant defenses. Overall, these studies suggest that Elizabeth River sediments and PAH mixtures generate oxidative stress and that killifish exhibit a variety of short-term physiological responses to this stress. Further, some antioxidant responses in Elizabeth River killifish appear to be heritable defenses that may contribute to overall resistant phenotype.

Downregulation of the aryl hydrocarbon receptor (AHR) pathway

The most pronounced and consistent biochemical alteration observed in the resistant killifish is marked recalcitrance to induction of Phase I metabolizing enzyme CYP1A (described previously). This conspicuous downregulation, along with the knowledge of the role CYP1 enzymes play in activation of PAH to more toxic and reactive metabolites, led the Di Giulio lab to pursue the hypothesis first proposed by Van Veld and Westbrook ( 1995) that suppression of CYP1A activity was a major component of resistance in Atlantic Wood killifish. To test this hypothesis and investigate the ramifications of exposure to PAH mixtures, reference population (King's Creek) killifish embryos were exposed to AHR agonists while CYP1A activity was suppressed using chemical inhibitors (Wassenberg and Di Giulio 2004a; 2004b; Wassenberg et al. 2005). However, in contrast to reducing toxicity, combined exposure of embryos to an AHR agonist and a CYP inhibitor resulted in an unexpected and dramatic synergistic increase in cardiac teratogenesis. The combination of 11 μg/L of AHR agonist BNF with 100 μg/L of CYP1A inhibitor α-naphthoflavone (ANF) resulted in a near-maximal score on the deformity index used, despite the fact that neither compound elicited any observable teratogenicity on its own (Wassenberg et al. 2005). Comparable results were observed using a variety of AHR agonists (benzo[a]pyrene [BaP], BNF, and PCB-126) and CYP1A inhibitors (ANF, fluoranthene [FL], 2-aminoanthracene, piperonyl butoxide, carbazole, and dibenzothiophene) (Wassenberg and Di Giulio 2004a; Wassenberg et al. 2005). Similar marked enhancement of toxicity was noted when embryos were exposed to a mixture of diluted Elizabeth River pore water and ANF (Wassenberg and Di Giulio 2004b). To further investigate this phenomenon and confirm the role of CYP1A inhibition, targeted morpholino knockdown of CYP1A was performed. Our lab in collaboration with the Hahn laboratory (Woods Hole Oceanographic Institute) developed the morpholino gene knockdown technique for use in killifish and demonstrated that knockdown of CYP1A exacerbated BNF-induced toxicity in killifish (Matson et al. 2008). Collectively, these results have a number of important implications. Clearly, suppression of CYP1A alone is not only insufficient to provide the resistance observed in Elizabeth River killifish but in fact increases toxicity of AHR agonist-type PAH in naive fish. Further, at least with respect to embryotoxicity, data call into question the model of additive toxicity that is commonly assumed for PAH.

Thus far, the mechanisms by which CYP1A inhibition synergizes PAH toxicity remain to be determined. One hypothesis is that blockage of metabolism by CYP1A prevents degradation of PAH and prolongs its persistence in fish. This may serve to make PAH resemble DLC, perhaps explaining why cardiac teratogenesis generated by PAH mixtures closely resembles that induced by DLC. Another possibility is that inhibition of CYP1A shifts metabolism of the PAH to a different route that results in more toxic metabolites. In an attempt to address this hypothesis, Elizabeth River and reference embryos were exposed to a mixture of BaP and the CYP1A inhibitor PAH FL from 24 h post fertilization (hpf) to 120 hpf, at which point the presence of parent BaP and specific metabolites were measured (Wills et al. 2009). Coexposure to FL exerted minimal effects on the rate of BaP metabolism in either population; Elizabeth River embryos retained numerically more parent BaP. In addition, more of the only metabolite detected, BaP-9,10-dihydrodiol, was measured in Elizabeth River embryos. Because 9,10-dihydrodiol and its subsequent metabolite, 9,10-diol,7,8-epoxide, are less mutagenic than the alternatives (Stegeman and James 1985; Peltonen and Dipple 1995), Wills et al. ( 2009) postulated that this shift in metabolism might contribute to resistance in Elizabeth River killifish. Increased production of 9,10-dihydrodiol may be indicative of a rise in the ratio of epoxide hydrolase activity relative to CYP1A (Kleinow et al. 1998; Oesch 1988; Bauer et al. 1995; James and Little 1983). However, it should be noted that the Wills et al. ( 2009) study was hampered by detection limits for most BaP metabolites measured.

Given the results of the effect of blocking CYP1A on PAH toxicity, it appears likely that the refractory CYP1A response in Elizabeth River killifish might be part of a broader downregulation of the entire AHR pathway. The critical role of AHR in toxicity of both DLC and some PAH makes it a likely target for development of resistance. Other populations of fish, including killifish, were identified that are resistant to DLC (Wirgin and Waldman 2004), and several demonstrated resistance to both PAH and DLC. As indicated previously, Elizabeth River killifish are resistant to PCB-126 and to PAH (Meyer and Di Giulio 2002; Nacci, Champlin, and Jayaraman 2010). Killifish from New Bedford Harbor, MA are resistant to high levels of PCB at the site and also to PAH (Bello et al. 2001; Nacci et al. 1999; 2002) While tomcod ( Microgradus tomcod) from the Hudson River, New York, are resistant to high levels of PCB contamination, their CYP response is refractory to induction by PCB but not by PAH (Roy et al. 2002). However, they are less susceptible to DNA damage by BaP than reference-site tomcod (Sorrentino et al. 2004). One hypothesis to explain development of resistance to different but related classes of contaminants in multiple populations and species is through modification of a single conserved gateway, such as the AHR.

Further evidence that PAH resistance in Elizabeth River killifish occurs through modification at the top of the AHR pathway was provided by analysis of transcriptional expression of hepatic CYP1A, AHR1, AHR2, ARNT2, and AHRR in adult fish treated with BNF (Meyer et al. 2003b). CYP1A, AHRR, and AHR2 expression were induced in reference fish, but not in Elizabeth River fish; AHR1 and ARNT2 were not differentially expressed. Data suggest suppression at the level of the AHR, since both CYP1A and AHRR are AHR regulated. It is also notable that there were no marked differences between populations in basal levels of expression of any genes examined, which implies that a difference in initial mRNA expression of AHR pathway genes does not confer resistance. Further, it is noteworthy that AHR2 was inducible in reference but not Elizabeth River fish. Although there is debate as to whether AHR is inducible by chemical treatment, one might expect that if it were, Elizabeth River fish direct from the field might display elevated basal levels due to PAH exposure in situ. This lack of induction of AHR2 in Elizabeth River fish, coupled with statistically indistinguishable basal levels of expression, may indicate that resistance is conferred through an insensitive or noninducible AHR2 in Elizabeth River fish. It is important to note, however, that expression of AHR2 was increased detectably in male fish from the Elizabeth River, indicating that these changes may have a sex-specific component. Thus far, these comparisons have only been made at the level of mRNA, not protein. Recent assessment in the Di Giulio lab of PAH-induced CYP mRNA expression in larvae and embryos provides further evidence that alterations occur prior to transcription of individual AHR-responsive genes. CYP1A, CYP1B1, and CYP1C1 were all induced by BaP exposure in larval reference but not Elizabeth River larvae (Wills et al. 2010b), and Elizabeth River embryos were also resistant to expression of the three CYP after exposure to multiple PAH and PCB-126 (Clark, Bone, and Di Giulio 2014). It is more likely that alterations at the level of AHR might be responsible for the observed changes in expression of various AHR pathway genes, rather than separate changes for each gene.

Morpholino knockdown studies provide evidence supporting the potential of modulation of AHR for conferring resistance to PAH and PAH mixtures. In zebrafish, morpholino knockdown of AHR2 was protective from synergistic cardiac toxicity induced by a mixture of BNF and ANF (Billiard et al. 2006) and by high doses of pyrene or benz[a]anthracene (Incardona et al. 2005; 2006). Further, work in the our lab showed that AHR2 knockdown in zebrafish protects from teratogenesis due to PAH mixtures, including BaP + FL, and benzo[k]fluoranthene (BkF) + FL (Van Tiem and Di Giulio 2011; Garner and Di Giulio 2012). Similarly Clark et al. ( 2010) demonstrated that knockdown of AHR2, but not AHR1, protected killifish from cardiac teratogenesis due to BNF, BkF, and PCB-126.

Mechanisms by which AHR mediates developmental toxicity of some PAH in fish, including killifish and zebrafish, are largely unknown. This phenomenon has received significantly more attention in the context of DLC, particularly TCDD. These studies suggested interactions between the AHR and other signaling genes and pathways involved with development, including Sox9b (Hofsteen et al. 2013), the COX2-thromboxane pathway (Teraoka et al. 2014), and the Wnt pathway (Schneider, Branam, and Peterson 2014). This remains an active area of research. It is likely that mechanisms revealed for DLC are relevant to PAH that are AHR agonists. A recent microarray study in our lab exploring PAH synergy, described earlier in this article, suggested a connection between the AHR pathway and perturbed calcium homeostasis affecting heart muscle contractility as a potential target (Jayasundara et al. 2015). Additional studies in this vein are underway.

However, there is also evidence that some of the components of PAH mixtures may produce cardiac toxicity independent of the AHR pathway. In particular, studies investigating the mechanisms underlying oil-mediated embryotoxicity found that some three- and four-ring PAH present in both oil and creosote mixtures (i.e., phenanthrene, dibenzothiophene, and pyrene) produced cardiac and circulatory abnormalities in zebrafish (Incardona, Collier, and Scholz 2004; 2005; 2006) . In one such study, morpholino knockdown of AHR2 blocked developmental cardiac toxicity induced by exposure to 5 μ M pyrene, but not that produced by exposure to 28 μ M phenanthrene (Incardona et al. 2005). Further, low-molecular-weight PAH are a major component of contamination in Elizabeth River sediments (Clark et al. 2013; Fang et al. 2014). Although the role of AHR-pathway-independent toxicity in the adaptation of Elizabeth River killifish has not been comprehensively examined, a recent effect-directed analysis of Elizabeth River pore water showed that in addition to toxicity induced by fractions containing high-molecular-weight PAH, a fraction dominated by low-molecular-weight PAH was also toxic to zebrafish embryos (Fang et al. 2014). A simplified mixture meant to simulate the relative concentrations of the dominant chemicals from that fraction (dibenzothiophene, phenanthrene, FL, pyrene, 1,2-benzofluorene, 1,2-benzanthracene, and chrysene) resulted in similar toxicity, but a mixture that matched the concentrations of the two most dominant compounds in the fraction (phenanthrene and FL) failed to produce an effect. In contrast, Brown et al. ( 2014) showed that exposure of zebrafish embryos to 6 μ M phenanthrene alone did not produce cardiotoxicity, but damage to the heart occurred when embryos were co-exposed to 6 μ M phenanthrene and 2.5 μ M FL.

Fitness Trade-Offs and Cross-Resistance in PAH-Adapted Killifish

Although evolutionary theory predicts that rapid adaptation to single stressors is likely to be accompanied by concurrent fitness costs to populations, not all studies confirm that (Kinnison and Hairston 2007). Strong and rapid selection is thought to reduce overall population genetic variation and fitness following a population bottleneck. However, even relatively rapid development of resistance to chemical pollution may occur via a series of changes in populations, potentially avoiding such bottlenecks and their associated costs. Little evidence for the classical fitness costs of adaptation, that is, reduced fecundity, growth rate, and survival, has been identified in Elizabeth River killifish, but a broader interpretation might also include greater sensitivity to other stressors-chemical, physical and biological. Despite the significant PAH resistance exhibited by Elizabeth River killifish, they are not wholly adversely unaffected by contamination. As described previously, Elizabeth River killifish suffer from a variety of hepatic and extrahepatic neoplasms (Vogelbein et al. 1990; Fournie and Vogelbein 1994). These fish also seem to be more susceptible to diseases and have documented alterations in immune function (Meyer et al. 2005; Weeks, Warinner, and Mathews 1988; Faisal et al. 1991a; Meyer and Di Giulio 2003; Frederick, Van Veld, and Rice 2007; Kelly-Reay and Weeks-Perkins 1994). This may also be a direct effect of PAH exposure, as there is evidence that PAH exert a variety of effects on the immune system of fish (Reynaud and Deschaux 2006). Some of these effects are clearly an effect of long-term persistence in a heavily polluted environment, but others may be costs of adaptation.

To explore the consequences and fitness costs of adaptation, Meyer and Di Giulio ( 2003) compared responses of Elizabeth River and reference killifish to several stressors and to clean conditions. In clean conditions, survivorship of Elizabeth River F1 larvae was significantly lower than for reference larvae after 9 months. Interestingly, survivorship of F2 larvae was no different than for reference fish. A similar trend was observed for growth. In addition, reference larvae tolerated phototoxicity mediated by combined exposure to FL and ultraviolet (UV) light for longer than Elizabeth River larvae. However, Elizabeth River F1 larvae still survived longer when exposed to Elizabeth River sediments, regardless of UV exposure. In addition, Elizabeth River F1 and F2 larvae tolerated low O ₂ (0.5 mg/L) conditions for significantly less time than reference larvae in short-term acute exposures

Taking a nontargeted approach, Meyer et al. ( 2005) used suppressive subtractive hybridization to generate a differential display of genes expressed in livers of Elizabeth River killifish and a reference population. Some of the genes that were most strikingly decreased in the Elizabeth River fish were related to immune function, including Factor XI, a clotting factor also involved in complement activation, and complement components C3 and C9. Further, expression of UDP-glucose pyrophosphorylase was lower and expression of glucose 6-phosphatase was higher in Elizabeth River fish, suggesting impairment of aerobic energy metabolism and a shift away from energy production in mitochondria. This result is consistent with reduced tolerance of Elizabeth River killifish to hypoxia.

A series of studies by Jung and coworkers further explored the effect of PAH and of PAH adaptation on mitochondria of Elizabeth River and reference killifish. While the bulk of CYP1A protein and activity occurs in the endoplasmic reticulum of cells, it also is present in mitochondria. Jung and Di Giulio ( 2010) isolated killifish mitochondrial CYP1A and showed that it was induced by BaP in reference fish but not in Elizabeth River killifish. Using long-amplicon polymerase chain reaction (PCR), Jung and coworkers ( 2009a; 2009b) demonstrated that wild-caught Elizabeth River adults exhibited significantly greater levels of both mitochondrial DNA (mtDNA) and nuclear DNA (nDNA) damage in liver, brain, and muscle than reference fish.

Although wild-caught Elizabeth River killifish exhibited a higher basal level of DNA damage, they may actually be less susceptible to induction of DNA damage by PAH. Jung et al. ( 2009a) found that intraperitoneal (ip) injection of BaP resulted in a two- to sevenfold increase in DNA damage in reference fish, but less than twofold rise in Elizabeth River. This fits with the observations of Wills et al. ( 2009) indicating that Elizabeth River fish might be shifting metabolism of BaP away from the formation of DNA-damaging metabolites. Further, this correlates strongly with Wills et al. ( 2010a) showing that Elizabeth River killifish are less susceptible to BaP-induced liver toxicity and carcinogenesis. Data suggest that while Elizabeth River killifish display elevated rates of liver cancer due to living in an environment highly enriched in carcinogens, they are nonetheless more resistant to this PAH-mediated cancer than naive killifish. A reasonable hypothesis for this is that the downregulation of the AHR pathway in Elizabeth River killifish that confers resistance to acute toxicity of PAH also results in reduced activation of PAH to their ultimate mutagenic metabolites. However, it is conceivable that resistance to the acute effects, which readily parlay into effects on population dynamics, is the evolutionary driver for adaptations, not resistance to cancer, which is less tied to population dynamics.

In another investigation, Clark and Di Giulio ( 2012) determined whether PAH adaptation had trade-offs for Elizabeth River fish exposed to contaminants for which the mode of action (MOA) differed from that of PAH but that were known to interact with components of the AHR pathway. Larvae were challenged with neurotoxic insecticides, including those for which the adaptive suppression of the AHR pathway would be beneficial (chlorpyrifos; activated by CYP to the more toxic chlorpyrifos-oxon) and detrimental (permethrin; degraded by CYP to less toxic metabolites). Surprisingly, the Elizabeth River larvae were more resistant than reference larvae to both chlorpyrifos and permethrin, suggesting that other aspects of adaptation were contributing to resistance. Although some chemicals affect Elizabeth River fish equally, a chemical challenge to which Elizabeth River fish are more susceptible than reference fish, other than FL in combination with UV exposure, has not yet been tested (Bryan Clark, unpublished data).

Key aspects of the "Elizabeth River phenotype" described in the forgoing sections are presented in .

POPULATION GENETICS AND ADAPTATION

Thus far, much of the work reviewed here focused on the nature and underlying mechanism of PAH tolerance in Elizabeth River killifish. However, the existence of the adapted Elizabeth River population along with contaminant-adapted killifish populations in New Bedford Harbor, MA, and Newark Bay, NJ, provides unique opportunities for investigating the effects of pollutants on selection and genome-level responses to environmental contaminants.

There are several explanations for the persistence of a killifish population in the highly contaminated Atlantic Wood Superfund site. One is that they have developed heritable adaptations that enable their survival; much of the work described previously supports that conclusion. Alternately, the Atlantic Wood subpopulation may suffer a high rate of mortality, but continually replenish via immigration from nearby subpopulations. Various investigations used allozyme frequency (Mulvey et al. 2002) and mtDNA haplotype diversity (Mulvey et al. 2003) to test these possibilities. In these studies genetic diversity was compared among subpopulations throughout the Elizabeth River estuary and reference populations in the nearby York River. The Elizabeth River subpopulations were located in sites that varied in degree of sediment PAH contamination. In both studies, data demonstrated that fish from the Atlantic Wood site were genetically distinct from the other subpopulations investigated. Fish from a second, moderately contaminated Elizabeth River site were less distinct from other subpopulations. Overall, genetic distance between subpopulations was not correlated with geographic distance but rather with degree of PAH contamination at the site of collection. Thus, immigration from subpopulations does not appear to be a significant mechanism for supporting continued existence of the AW population. There is evidence, however, indicating that such immigration might occur with DLC-adapted populations (Roark et al. 2005; McMillan et al. 2006).

Recently, Clark et al. ( 2013) compared the level of resistance to a variety of aryl hydrocarbons among Elizabeth River killifish subpopulations from throughout the estuary, most of which were collected in or near the sites used by Mulvey and coworkers ( 2002; 2003). Unlike the Atlantic Wood population, some of the subpopulations exhibited a high degree of AHR pathway activation, as measured by EROD activity, but were also resistant to aryl hydrocarbon-induced teratogenesis. Further, various subpopulations exhibited unique patterns of response to the differing hydrocarbons tested. The varied patterns of resistance to teratogenesis and AHR pathway activation suggest that PAH adaptation in the Elizabeth River killifish meta-population is multigenic, with highly resistant Atlantic Wood fish exhibiting all aspects of resistance and various subpopulations only sharing some of the resistance mechanisms.

Further, the degree of aryl hydrocarbon resistance was not highly correlated with the level of PAH at the subpopulation collection site. These unique patterns of subpopulation response and lack of correlation to contaminant level are also notable given the previous observations of strong correlations between PAH level and genetic distance (Mulvey et al. 2002; 2003) and resistance (Ownby et al. 2002). Mulvey et al. ( 2002; 2003) estimated a rate of migration sufficient to maintain significant gene flow among subpopulations; the modeled effective migration rates were 9.6 migrants per generation for juveniles and 17.5 migrants per generation for adults. It was hypothesized that the Atlantic Wood population remains genetically distinct despite the migration rate because immigrants are unable to survive in the harsh conditions. However, it is possible that emigrants from the Atlantic Wood site might be driving the appearance of adaptation at sites with low levels of PAH contamination that was observed. Moreover, the transmission and fixation of only some components of a multigenic adaptation to other subpopulations might explain the unique patterns and incomplete resistance displayed by the individual subpopulations. High migration rates may also serve to help maintain overall genetic diversity, given that strong selection for a particular adaptive parameter might lower overall genetic diversity. Conversely, pollutant stress may reduce genetic variability in populations by reducing population size through loss of sensitive individuals and reduced fecundity. However, Mulvey et al. ( 2002); 2003) noted no marked loss of genetic diversity in either study of Elizabeth River killifish.

In studies comparing aryl hydrocarbon-adapted killifish populations from the Atlantic Wood Industries Superfund site and Superfund sites in New Bedford Harbor, MA, and Newark Bay, NJ, Oleksiak and coworkers searched for transcriptomic loci linked to contaminant exposure and adaptation. Hypothesizing that pollutant exposure would necessitate changes in metabolic gene expression to provide energy for protection against toxicity, a metabolic cDNA array was utilized to compare gene expression in brain (Fisher and Oleksiak 2007) and liver (Oleksiak 2008) between each pollution-adapted population and two nearby matched reference populations. Compared to its reference sites, 5% of the examined genes (13 of 260) were differentially expressed in brains of Elizabeth River killifish, but this was reduced to only one gene after Bonferroni correction. In addition, only two genes were shared among all three Superfund populations (NADH-ubiquinone oxidoreductase AGG subunit precursor, a subunit in oxidative phosphorylation complex I, and thioredoxin, an oxidoreductase that facilitates the reduction of other proteins). In livers of Elizabeth River killifish, 8% of examined genes (20 of 250) were differentially expressed compared to reference populations; this reduced to 2 of 250 after Bonferroni correction. Again, a small number of genes were identified that were differentially expressed in all three aryl hydrocarbon-adapted populations (acyl-coenzyme A [CoA]-binding protein, the MNLL subunit of NADH-ubiquinone oxidoreductase, and thioredoxin). However, none of these genes exhibited consistent expression patterns among the polluted populations. Evidence indicated that the relative lack of overlap among the gene expression patterns of the three aryl hydrocarbon-adapted populations reflects different routes of adaptation and different pollutant exposure. However, previous studies found a great deal of overlap in the adaptive responses of the three populations (Wirgin and Waldman 2004); thus, it is also possible that the limited number of genes or the sensitivity of the array was unable to fully capture the adaptive changes. In contrast, Whitehead et al. ( 2012; 2010) observed convergent transcriptomic responses in comparisons of PCB-126 embryotoxicity exhibited by several DLC-adapted populations (the Elizabeth River population was not tested). In these studies, embryos from tolerant and sensitive populations were exposed to PCB-126 and at 10 d postfertilization were assessed for both phenotypic and transcriptomic responses. Among the major transcriptomic responses in the sensitive populations were a decrease in expression of cardiovascular-system-related genes (Whitehead et al. 2010) and an increase in expression of genes associated with the AHR pathway (Whitehead et al. 2010; 2012); these responses were absent in the adapted populations. Finally, similar to Mulvey et al. (2002; 2003), Oleksiak et al. (2002; 2005) also did not observe any reduction in variance in gene expression due to contaminant adaptation.

Subsequently, Williams and Oleksiak ( 2008) compared allele frequencies of amplified fragment length polymorphisms (AFLP) among the same pollutant-adapted and paired reference populations used in the gene expression studies. The goal was to identify genomic loci with large differences in allele frequency between the aryl hydrocarbon-adapted and reference populations, but that were not also highly different between the pair of reference populations; these outlier loci might be involved in adaptation and pollutant responses. Three percent (9 of 299) of the loci scored were identified as outliers in comparison of the Elizabeth River killifish to two reference populations. Of these, six were found in individual comparisons of the Elizabeth River population to each reference population that were not found in comparison of reference populations to each other. The Elizabeth River population shared two outlier loci with the New Bedford Harbor fish and two with the Newark Bay fish. No outliers were shared among all three adapted populations; rather, most of the identified loci were unique to each adapted population. This may be attributed to linked loci dragging different polymorphisms to fixation in each population, even if the locus driving selection was actually the same in each population, or the adaptation might differ among the populations. However, as indicated previously, populations are faced with similar contaminant profiles and exhibit many similar adaptive responses, so it is surprising that more shared loci were not identified. Williams and Oleksiak ( 2008) also postulated that other selective pressures, such as predation or food availability, may drive differences among populations. It is interesting to consider that these differences may also be secondary effects arising from differing effects of the contamination in each ecosystem.

Because of the multiple lines of evidence pointing to the AHR pathway as a target for adaptation, Proestou et al. ( 2014) compared the pattern of genetic variation in single nucleotide polymorphisms (SNP) in 42 AHR pathway genes in 4 DLC-tolerant killifish populations and nearby reference sites. Pairwise comparisons of geographically close tolerant and sensitive populations uncovered differences in allelic composition at AHR1 and 2, cathepsin Z, CYP1A and CYP3A30, and the NADH dehydrogenase subunits, but variation in AHR2 and CYP1A was strongest across all of the tolerant versus sensitive population pairings, supporting a role for alterations of the AHR pathway in the adaptive response of multiple populations. Further, Proestou et al. ( 2014) did not find any marked reduction in overall genetic variation in the pollutant-adapted populations, in agreement with multiple previous studies.

CONCLUDING REMARKS

This review is by no means the first discovery concerning pollution driving animal evolution. The phenomenon of industrial melanism in populations of the peppered moth ( Biston betularia) in England and Wales is perhaps the iconic example of pollution (in this case, soot emitted by coal burning) affecting evolution (Cook 2003). In this case, natural selection favored the dark, melanic phenotype (carbonaria) over the normally lighter, "peppered" phenotype (typica), apparently due to reduced avian predation due to the camouflage afforded against the dark, soot-covered tree trunks the moths utilized. Following control of emissions, the carbonaria phenotype gradually declined in relative abundance (Cook 2003). There are numerous reports of insects evolving resistance to insecticides, including mechanisms associated with different classes of insecticides. In recent years, this has garnered particular attention in relation to mosquito control, in part due to the key role these insects play in malaria transmission (Lenormand et al. 1999; Wondji et al. 2008). As alluded to earlier, there are other examples of pollution tolerance in fish populations, some of which appear to be inheritable and thus of evolutionary significance. These include DLC-resistant killifish populations in New Jersey, Massachusetts, and Connecticut (Prince and Cooper 1995; Nacci, Champlin, and Jayaraman 2010), resistance to DLC and PAH in Gulf killifish ( Fundulus grandis) in Texas (Oziolor et al. 2014), resistance to methylmercury, also in New Jersey killifish (Weis et al. 1981), and resistance to cadmium in lab-reared least killifish ( Heterandria formosa) (Xie and Klerks 2003). The subject of chemical toxicity resistance in fish was reviewed by Van Veld and Nacci ( 2008); however as they point out, most examples of this phenomenon did not include studies to determine whether observed adaptations were genetically based.

The Elizabeth River story of pollution-driven evolution in killifish is compelling for several reasons. The degree of resistance exhibited by the Atlantic Wood Industries population is striking and has garnered attention of numerous investigators over the years; thus, there is a wealth of information concerning this population gathered from a number of perspectives, including toxicology, ecology, genomics, physiology, risk assessment and management. Other subpopulations in the river have also been identified that reveal varying degrees of adaptation, and that, together with the Atlantic Wood population, provide fertile grounds for studying pollution-driven evolution, underlying mechanisms, fitness costs, and impacts of remediation. Regarding remediation, two of the former creosote sites (Atlantic Wood Industries and Eppinger and Russell) are undergoing active remediation, and remediation of the third, Republic Creosoting, is planned. Thus, these sites, together with other sites in the river not associated with wood treatment, provide excellent opportunities for examining how specific subpopulations change during and post remediation. Also noteworthy is the chemical class at the center of this story-PAH. While the major source of PAH in the Elizabeth River is creosote that apparently is no longer used for wood treatment in the area, PAH are ubiquitous environmental contaminants that appear to be gradually increasing due to the use of fossil fuels and concomitant population growth and urbanization (Van Metre and Mahler 2005). In addition, these compounds are the chemicals of greatest concern following oil spills such as the 2010 Deepwater Horizon explosion in the Gulf of Mexico, the impacts of which included effects on the Gulf killifish (Dubansky et al. 2013). Thus, the gradient of PAH contamination present at specific sites in the Elizabeth River provides a powerful platform on which to understand organismal and population-level effects of these chemicals in a real-world ecosystem.

Work to date in this system has yielded several significant findings, and raised important questions. Demonstrating that the resistance was genetically based and thus evolutionarily meaningful is important; perhaps not surprisingly, there are relatively few clear examples of pollution driving evolution in free-living vertebrates. Interestingly, several of the other demonstrations of this also were observed in the Atlantic killifish, supporting the utility of this species as sentinel for Atlantic coast estuaries; the closely related Gulf killifish has a similar utility on that coast. Considerable insight has been gained concerning mechanisms underlying the resistance, which in turn provides a unique opportunity to address mechanisms of PAH-mediated toxicity. Among mechanisms observed, downregulation of the AHR in the Atlantic Wood populations has been the most pronounced and consistent signal. This is similar to observations of DLC-adapted killifish in the northeastern United States. Mechanisms that underlie this downregulation and those by which the AHR mediates toxicity in nonadapted killifish (and other animals) remain important subjects of inquiry.

The observation that the most sensitive endpoint to exposures to extracts from the Atlantic Wood site and to simple PAH mixtures in nonadapted killifish (and also to zebrafish) was embryonic development of the cardiovascular system was a significant finding; this effect is postulated to be the evolutionary driver of resistance in the Atlantic Wood population. At the time of first observing this (approximately 2000), this effect was somewhat surprising, as it was not a "textbook" effect of PAH, as opposed, for example, to cancer (upon which human risks for PAH are based). The only previous example of a PAH perturbing cardiovascular development we are aware of is that of retene (7-isopropyl-1-methylphenanthrene, associated with pulp and paper mills) in zebrafish and rainbow trout (Billiard, Querbach, and Hodson 1999); retene also induced CYP1A activity (Brinkworth et al, 2003), suggesting that it is an agonist for the AHR.

A related and striking finding emanating from the Elizabeth River killifish studies was the unanticipated finding of the potent synergy between PAH that are AHR agonists (e.g., BaP) and those that are inhibitors of CYP1A (e.g., FL); these two representatives are among the most prevalent PAH at the Atlantic Wood site. This synergy has important ramifications for PAH risk assessments. Risk assessments for classes of chemicals often assume additivity; that is, the toxicity of a mixture of a given class may be predicted based on adding the relative toxic potencies and concentrations in the mixture, with potencies of component chemicals based on a well-characterized representative of high potency. This is referred to as the toxic equivalency approach and has been widely used in risk assessments of DLC in which TCDD serves as the reference compound (Van Den Berg et al. 2006). Risk assessments for PAH do not appear as formalized at present, but approaches implicitly assume additivity, which is explicitly assumed for DLC. For human risk assessments of PAH, cancer is the key endpoint and BaP is often the reference compound (U.S. EPA 2010). For ecological risks there appears to be no reference compound but the toxicities of individual PAH generally based on acute toxicities are added after adjusting for relative concentrations in the mixture of concern (Wu et al. 2011). Studies based on Atlantic Wood sediments suggest that this approach likely greatly underestimates risks posed by some PAH mixtures, particularly those with relatively high proportions of higher molecular weight AHR agonists-typical of pyrogenic PAH mixtures. This may be less true for petrogenic mixtures in which lower molecular weight PAHs appear to dominate toxicity, as in the case of oil spills (Incardona, Collier, and Scholz 2004).

The phenomenon of genetic adaptations to pollution that decreases sensitivity to exposures has other implications for risk assessment and environmental management. An argument could be made that free-living organisms with relatively short generation times may evolve to thrive in the face of chronic pollution that is of a consistent nature (as is the case for the Elizabeth River). However, evolutionary theory posits that genetic adaptations to a potent driver of natural selection will reduce genetic diversity and incur fitness costs in the adapted population (Ribeiro and Lopes 2013). While it is unclear whether pollution in the river reduced genetic diversity, genetic structure was altered in several subpopulations, and, importantly, fitness costs were incurred in the only subpopulation that was examined intensively in this regard to date (Atlantic Wood). This subject merits additional scrutiny and is an active area of investigation currently; preliminary results suggest fitness costs in other subpopulations of Elizabeth River killifish, with degree of costs roughly tracking degree of pollution resistance. In any event, to base risk assessments or management decisions on the observation that organisms evolve to survive pollution seems inappropriate. Other important considerations are the likely complex ramifications that evolved adaptations in the killifish have for other members of the community and the ecosystem overall. For example, one would predict that the adapted killifish accumulate greater amounts of PAH due to reduced metabolism, thereby increasing exposure to their predators.

A question that arises from this review is that of potential implications for human health. Given the long generation time of humans versus killifish, the relevance of the evolutionary component appears limited. However, the observed effects of PAH, including synergistic mixtures, on vertebrate development may be relevant in consideration of the ubiquity of this class of chemicals and their importance as air pollutants (Boström et al. 2002). However, there are important differences between fish embryos and human fetuses as targets for PAH. For fish embryos, PAH exposures are likely to occur either directly from the water column, or via vitellogenin, the yolk protein synthesized in the maternal liver that was shown to transfer BaP to killifish eggs (Monteverdi and Di Giulio 2000). Human fetal exposures would likely occur from maternal blood flow via the placenta. Thus, in the case of humans, there would be greater opportunity for PAH to be metabolized before they reached the fetus than in the case of fish embryos. Moreover, there are no apparent reports of PAH exposures to fetuses (carried by mothers that are smokers, for example) having effects on the developing cardiovascular system. This would be a more difficult consequence to observe in humans versus fish. However, studies by Columbia University investigators following a cohort of children born to nonsmoking mothers in New York City revealed strong associations between cord blood concentrations of PAH during pregnancy and subsequent adverse intellectual and behavioral outcomes in young children (Perera et al. 2012). These studies suggest an effect of PAH on human neurodevelopment. Current studies at Duke University are investigating behavioral effects in killifish and zebrafish at exposures below those producing frank cardiovascular effects. Thus, these human and fish studies appear to have relevance for one another.

Finally, while this story revolves around the degradation of an estuarine ecosystem due to human activities, it is important to conclude with the good news of ongoing efforts to restore the Elizabeth River. Coordinated efforts including, among others, the U.S. EPA, U.S. Army Corps of Engineers, National Oceanic and Atmospheric Administration (NOAA), the Virginia Department of Environmental Quality, and area towns (Chesapeake, Norfolk, Portsmouth, and Virginia Beach) and industries, are making significant progress in removing and limiting inputs of pollutants into the system, restoring habitats including wetlands, and increasing public awareness of the value of a restored Elizabeth River. Many of these efforts are being coordinated by the Elizabeth River Project, a non-profit organization incorporated in 1993 (website: http://www.elizabethriver.org). The project's goal is to make the Elizabeth River swimmable and fishable by the year 2020; it also is involved with projects on the Lafayette River. Among the notable projects overseen by the Elizabeth River Project is the revitalization of Money Point, an area that includes the former creosoting facility operated by Eppinger and Russell (). This ambitious project includes removal of hotspots of PAH contaminated sediments, prevention of future upland inputs of contaminants, enhancing the co-existence of industrial, community and ecological health, and the restoration of wetlands and other wildlife habitats. This project is well underway; contaminated sediments have been removed from the Eppinger and Russell site (with the assistance of the current landowner, Hess Corporation) and wetland restoration there is in progress (). Also, a retaining wall surrounding the most contaminated sediments adjoining the former Atlantic Wood Industries Superfund site was recently completed (summer, 2014; ), and related restoration activities are planned.

Thus, there is good reason for optimism for the health of the Elizabeth River, an attitude not present several decades ago when a spokesman for the Virginia State Water Control Board stated, "It is questionable whether or not this body of water can be restored" (Yarsinke 2007, 330). Among other approaches, the Atlantic killifish provides a powerful sentinel for gauging the success of revitalization efforts in this historic American river.

FUNDING

Portions of the research described in this review were supported by the National Institute of Environmental Health Sciences (NIEHS)-supported Duke University Superfund Research Center (P42ES010356) and Duke Integrated Toxicology and Environmental Health Program (T32ES07031).

Funding Statement

Portions of the research described in this review were supported by the National Institute of Environmental Health Sciences (NIEHS)-supported Duke University Superfund Research Center (P42ES010356) and Duke Integrated Toxicology and Environmental Health Program (T32ES07031).

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The Elizabeth River Story: A Case Study in Evolutionary Toxicology

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The Elizabeth River system is an estuary in southeastern Virginia, surrounded by the towns of Chesapeake, Norfolk, Portsmouth, and Virginia Beach. The river has played important roles in U.S. history and has been the location of various military and industrial ...

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Economic And Environmental Impacts Of Climate Change In Virginia

Virginia's climatic changes have been thoroughly documented over recent decades. The overwhelming weight of scientific evidence predicts that climate change will continue and may accelerate unless strong action is taken to reduce global greenhouse gas emissions. Climate change threatens serious harm to Virginia's economy, its people and its treasured natural resources. Virginia's political leaders should promote vigorous state, national and international policies to halt global warming. Virginia's current leadership, both in government and in the private sector, should take up this mission.

Although Virginia has experienced a relatively moderate rate of climate change compared to many other parts of the country over the past century as a whole, the speed and scale of climatic changes has gained momentum and has been accelerating throughout the last 50 years. Warming has occurred across the state, mostly during the winter months, when average temperatures rose about one degree C.1 Precipitation patterns also changed: summer rainfall declined on average by 0.50mm/day but in the fall months, precipitation increased by about the same amount.2 Correspondingly, there were more days of intense precipitation and precipitation became more variable, with greater frequency of both wet and dry periods, including the pronounced drought of 2010.3

All regional climate models project rising temperatures over coming decades. Annual average temperatures are expected to rise by three to four degrees centigrade over this century and possibly much more if emission levels continue to grow rapidly, with corresponding increases in both maximum and minimum temperatures. Overall precipitation is expected to increase by about ten percent and some models forecast that most of the increase will occur during the summer. The number of hot and humid days and the corresponding "misery index" will climb substantially. There are likely to be more heat waves like the one that Virginia suffered in the summer of 2011.4 Virginia's seasons will change: spring will come earlier, summer will last longer into the fall and winters will be milder.

INCREASED STORM SURGES AND SEA LEVEL RISE

The combination of land subsidence, sea level rise, flat and low tidewater topography and intensive coastal real estate and infrastructure development puts southeastern Virginia, namely the Virginia Beach/Norfolk/Hampton Roads region, at extreme risk from storm surges. Past tropical storms, such as Hurricane Isabel, did extensive damage from storm surge. An analysis based on catastrophe models developed by RMS, a risk management firm, identified this region as the 10th most vulnerable in the entire world to flooding from storm surges and in the United States, second only to Miami.5 Some of those at risk have already taken notice. The US Navy and Air Force, which have spent many millions of dollars to harden their facilities against flooding, are taking climate change into account in plans for the future of their bases in the region.6 Insurance companies have realized the potential for serious losses. CoreLogic, a real estate data firm, estimates that in the event of a major storm more than one-third of the houses in the Hampton Roads region would suffer flood damages7.

Most property and casualty insurers operating in the mid-Atlantic area now refuse to insure businesses and primary residences in the coastal region.8 Many industry members believe it will soon become too costly to cover many of these potentially high-risk properties, even with higher premiums. Some insurers have begun to refuse coverage for vacation homes. Limited insurance coverage puts property owners at great risk. Less than one-quarter of homes in the Hampton Roads area now have flood insurance, even in the highest flood risk areas. Insurance coverage for losses from storms is less than 25 percent of actual losses.9 Though that area will bear the brunt, these storm surge risks extend far into Chesapeake Bay and up Virginia's rivers as far as Richmond and Alexandria. The National Weather Service estimates that a Category 3 storm making landfall in the Carolinas could produce a 13-foot surge as far north as Baltimore and 14-16 foot surges further south in the Bay.10

Climate change will make the situation much worse. The pace of sea level rise at Norfolk is the highest on the East Coast because the shoreline is subsiding and global warming is increasing the rate of sea level rise, both because of thermal expansion and the melting of land ice.11 The lower tidewater area around Virginia Beach and Norfolk, as the result of climate change, will lose 19 percent of undeveloped dry land, 79 percent of beaches, and a third of brackish and freshwater marshes. An extensive analysis based on catastrophe modeling and 10,000 simulated storm tracks super-imposed on shoreline characteristics found that the mid-Atlantic region is more at risk than even the Gulf Coast or Atlantic Florida.12

The analysis considered only flood damages to above-ground structures, not in-ground infrastructure, but did include losses to building contents and interrupted use. Wind damages were not considered. Tests of the model showed that estimated losses compared closely with actual losses in past storms. The analysis considered three levels of risk: 1) losses at the current sea level height; 2) losses at the predicted higher sea level; and 3) losses at the higher sea level combined with warmer sea surface temperatures, which increase the intensity of tropical storms. Warmer sea surface temperatures significantly increase the number of hurricane-strength storms making landfall along the Atlantic coast.13

At the predicted level of sea level rise, expected annual losses exceed those at current sea levels by about 20 percent because storm surges would be higher and would extend further inland and up the estuaries. However, the combination of higher sea level and warmer sea surface temperatures elevated expected annual losses by roughly 55 percent above current levels because of the higher probability of intense storms making landfall. A particularly intense storm, one with a 50-year return period, would raise expected damages by 25 percent above current levels with only a higher sea level but by about 95 percent with both sea level rise and higher sea surface temperatures, almost four times as high as the current expected losses. The study concludes that the risks to coastal property from global warming are greatest in the mid-Atlantic region.14

Although these studies serve as serious warnings, they badly underestimate the actual risks. First, they consider only damages from storm surges, ignoring damages from high winds or from flooding caused by intense rainfall. Second, the analysis considered damages only to property that exists now but did not consider that population and construction in the coastal area will increase even as global warming continues, so future risks and damages will be considerably higher. Third, these studies consider only property damage, not potential injuries or loss of life and not the disruption that such storms bring to businesses and households. In the aftermath of a severe storm, these disruption losses alone are estimated to be equivalent to about a week's worth of total income, which is currently about $1.5 billion just for the Hampton Roads area. In only measuring a fraction of the absolute damage wrought by such storms, these analyses diminish the true scale of devastation that would result from storms that are more common and more powerful.

HURRICANES AND EXTREME STORMS

The effects of climate change on hurricane frequencies and intensities have been the subject of considerable scientific research and discussion. As they generate power from warm, moist air over warm ocean waters, hurricanes are becoming more intense as climate change continues to increase ocean temperatures. The current scientific understanding is that sustained warming will result in the more intense hurricanes becoming more frequent in Virginia's latitudes and the less intense hurricanes growing less frequent.15 With climate change driven by increasing emissions, the frequency of the most intense Category 4 and 5 storms would be expected to increase by 80 percent by 2080, or by roughly one percent per year. Over the same period the frequency of the less intense Category 1-3 hurricanes will diminish by 38 percent.

These changes are unlikely to be steady trends, since the most intense hurricanes strike the mid-Atlantic region only rarely and the effects of global warming will be superimposed on considerable short-term variability. Historically, no Category 4 or Category 5 hurricane has ever struck in Virginia but climate change is making it more likely that one will eventually do so. The implication is that overall hurricane risks are increasing because historically Category 4 and 5 hurricanes have caused 86 and 48 percent of recorded hurricane damages respectively, even though they represented only 24 and 6 percent of hurricane landfalls in the United States.16 Higher winds cause more devastation, persist longer at damaging levels and generally affect a wider area.

ECONOMIC DAMAGES FROM HURRICANES

In 2003, Hurricane Isabel did an estimated $5.5 billion dollars in damages to the Hampton Roads region, even though the region was not directly hit.17 A recent analysis carried out by a risk management firm, First American Corporation, estimated that if the least intensive hurricane, a Category 1 storm, made landfall in Southeast Virginia, it would probably cause $7.4 billion in damages, in 2010 prices.18 Another firm, CoreLogic made a similar estimate of $10 billion in damages to residential properties.19 Moreover, while the probabilities of more intense hurricanes are increasing, Virginia's economy is changing in ways that put more people and value in harm's way. Population and commercial and real estate development are again increasing in the coastal zone after the great recession of 2008-2010. The potential loss from any given storm is expected to double in each decade.20 Without a vigorous adaptation effort, Virginia is becoming more vulnerable to the effects of climate change.

When these projections of rising sea levels and storm surges, more frequent intense hurricanes, and increasing values at risk are brought together in an integrated analysis, using numbers that represent the best current scientific estimates, the results are ominous. The findings from such an integrated analysis for the coastal Virginia area are presented below.21

The National Hurricane Center, part of NOAA, estimates hurricane probabilities in each vulnerable region by fitting probability curves to historical data. Until now, the Center has neither estimated the effects of past climate change on hurricane frequencies nor predicted future effects. Nonetheless, the following table accepts the Center's estimates of hurricane return periods for 201022 and uses the scientific predictions discussed above to show the changing return periods from 2000 through 2060 of tropical storms and Category 1 through 5 hurricanes striking the Norfolk/Virginia Beach region. As the following table shows, though the probabilities of tropical storms and less intense hurricanes decline, the probabilities of major hurricane strikes increase by 50 percent over the period. By 2060 the hundred-year storm would be a Category 4 or 5 hurricane.

A study by Yale Economics Professor William Nordhaus, based on all recorded previous hurricanes striking the United States, found that damages increase exponentially as the maximum wind speed increases.23 In order to construct an overall risk analysis, these return periods, expressed as annual probabilities, were combined with the damage function estimated by Nordhaus and the estimate of a $7.4 billion dollar loss from a Category 1 hurricane. Damage estimates also factored in the effects of rising sea levels and the increase in coastal population and value at risk.24 Consequently, the damages to be expected from hurricanes striking the region increase dramatically over time, as the following table shows.

Expected losses are the damages that would be suffered from a storm of each intensity, multiplied by the probability of such a storm occurring, and then added up for all possible storms. These losses represent the actuarially fair value of hurricane damages to the region - the amount that insurers would have to collect in premiums (without overhead) to break even over time. As seen below, they rise dramatically, more than doubling in each decade because of the combined effects of global warming on hurricane intensities and sea level, along with the increase in value at risk. This perfect storm of heightened vulnerability and amplified risk will put Virginia's insurance sector under great pressure. Private insurers will have to raise rates dramatically or more will withdraw from the market. Coastal residents and communities also face an increasingly perilous future.

Another illustration of the increasing economic risks is to make use of loss exceedance curves, which are widely used in the insurance and other financial industries to measure risk exposure. A loss exceedance curve is the probability that a loss will be incurred that is equal to or greater than some amount. Loss exceedance curves for each decade from 2010 through 2060 for the Norfolk/Virginia Beach area are plotted in the following graph. Two things are immediately evident. First, the curves "flatten out" as loss amounts rise. Though probabilities of occurrence decline as maximum wind speeds rise, this is offset by the exponential increase in damages, so the probabilities of loss - combining the two - hardly fall. By 2050 there will be a 1 in 10 chance of a loss in coastal Virginia exceeding $9 billion dollars. Second, the loss exceedances rise rapidly over time. For example, the probability of damages exceeding $5 billion dollars rises from about 1 in 40 in the year 2010 to about 1 in 8 by the year 2050. The likelihood of even much greater losses rises almost as rapidly.

The implication of these estimates, when put together, is that climate change is sharply amplifying the risks to Virginia's economy and citizens and substantially increasing the likelihood of a natural disaster.

IMPACTS ON VIRGINIA'S NATURAL ENVIRONMENT

Degradation of Chesapeake Bay and loss of its economic value

Among climate change's many environmental impacts, Virginians must be especially concerned about the consequences for Chesapeake Bay and other estuaries, which are incredibly valuable recreational and economic resources. Attempts to put an overall economic value on these resources, which include not only its fisheries and recreational uses but also its many ecological functions, are necessarily speculative though the billions of dollars and tens of thousands of jobs in fishery-related and recreational activities have been documented.25 Nonetheless, the Chesapeake Bay Blue Ribbon Finance Panel put an overall value on the Bay in excess of a trillion dollars.26 Economists in Delaware estimated that a mere one percent of the Chesapeake Bay watershed generated economic benefits of $20 billion over a decade, which gives a perspective on the value of Virginia's much larger share.27 Climate change will not only impair this value but also negate the billions of dollars currently being spent to rehabilitate the Chesapeake Bay resource.

Over the course of this century, scientists predict that the CO2 content of Bay waters will increase by 50-150 percent, leading to higher acidity. Water temperatures will rise by two to six degrees C and water levels will increase by 0.7 to 1.6 meters and possibly much more if emissions grow rapidly.28 Storm intensities in the watershed and some seasonal inflows from higher precipitation and runoff are likely to increase as well. The consequences are likely to be profound even though they are hard to predict due to the complex ecology of the Bay.

More than 50 percent of estuarine beaches and 25 percent of ocean beaches on Virginia's eastern shore will disappear. One consequence will be a loss of nesting areas for already endangered loggerhead and Kemp's ridley sea turtles.29 The Chesapeake Bay could lose 50-80 percent of its tidal wetlands and marshes to inundation. An estimated 66 percent of the region's commercial

fish species depend on these marshes for nursery and spawning grounds, including menhaden, bluefish, flounder and rockfish. The sport-fishing industry, which generates more than $1.5 billion dollars per year in expenditures, will be seriously affected. Salinity levels will increase, adversely affecting eelgrass, other aquatic plants and associated fish and shellfish species. Some of these changes are potentially irreversible, once ecological tipping points are reached.30

Seagrass losses will be particularly devastating for duck species that depend on submerged aquatic vegetation for food, such as redhead, pintail, widgeon, black duck and canvasback. Duck hunting on the Eastern Shore, a popular activity for residents and visitors, will suffer. More intense storms will wash more non-point-source pollutants into the Chesapeake Bay, increasing turbidity and eutrophication. The occurrence of harmful algal blooms and oxygen deficits in Bay waters will increase.31 Parasites that have helped to destroy oyster and crab populations will proliferate.32 There are likely to be substantial changes in the mix of fish and shellfish species to be found in Chesapeake Bay waters and the productivity of the Bay, already severely impaired, is likely to be affected. The extent of these changes will be determined largely by the pace and degree of climate change.

Loss of Fish Stocks and Decreased Forest Productivity

Ecological impacts will not be limited to the coastal zone. In the upper reaches of Virginia's rivers and streams, warmer waters will reduce habitat for brook trout by up to 90 percent and reduce population numbers by more than half.33 Brook trout cannot tolerate water temperatures higher than 70 degrees F. The numbers of fly fishermen will correspondingly decline. Virginia's forests will experience significant changes. Red spruce and balsam fir will almost disappear and the red maples, yellow poplars, and chestnut oaks will decline, to be replaced by loblolly and shortleaf pine. Forest pests will proliferate, such as the hemlock woolly adelgid, which is likely to eliminate all eastern hemlocks from Virginia's forests. Drought will encourage outbreaks of pine bark beetles and gypsy moths.34 Whether overall forest productivity will rise or fall will depend on the balance between positive forces, such as CO2 fertilization, longer growing seasons and milder winters, and negative forces, such as more frequent droughts, fires, pest outbreaks and intense storms.

IMPACT ON HEALTH AND RELATED COSTS

￼Air Quality

The higher summer and fall temperatures are expected to affect air quality adversely. Release of pollen and other airborne allergens will increase with the changing seasons. Ozone and smog formation is likely to increase because higher temperatures heighten the underlying chemical reactions in the atmosphere and also increase volatile organic compounds released from trees and vegetation.35 Atmospheric ozone exacerbates bronchitis, asthma and other lower respiratory tract diseases, which are among the leading causes of death in Virginia. Climate change will also raise concentrations of fine particulates, which are even more damaging to health.36 The aggravated air pollution that typically accompanies heat waves especially harms children as they have a higher risk of developing asthma, lungs that are still developing and growing, and higher exposure because they breathe at a higher rate than adults do and often play outdoors.

National air quality standards for ozone are to be tightened eventually because of continuing health effects at the current level of standards. Recent EPA assessment concludes that allowable levels for fine particulates should be significantly lowered.37 During 2011, Virginia's air monitoring systems recorded numerous violations of current ozone standards in the Richmond and Hampton Roads areas and across northern Virginia.38 In addition, virtually all of northern Virginia violated the fine particulate standards in 2011.39

Climate change will make it even more difficult for Virginia to meet future air quality standards, particularly because hotter summers will increase summer peak electricity use, necessitating an escalation in the nitrogen oxide emissions that contribute to both ozone and particulate formation. Dominion Power is already scheduled to invest $500 million by 2015 in projects to reduce emissions from its coal-fired power plants in the state and will probably have to spend even more in the future. These amounts will be passed along in higher rates to electricity consumers in Virginia.

Health Impacts

These changes in climate will have significant impacts on the health and well being of Virginia's people, especially on the elderly and the very young, who together comprise nearly 20 percent of the population. For example, over the coming decades, Lyme disease, now confined to just one region, will spread across the state.40 The seasonal feeding cycle of the main carrier of Lyme disease, ticks, is heavily influenced by climatic changes and warmer temperatures will result in more severe tick infections in Virginia and the propagation of Lyme disease in the state. Lyme disease can be extremely debilitating, affecting every tissue and every major organ system in the body and can even be fatal in severe cases. Studies have found that almost two-thirds of Lyme disease patients still experience significant symptoms months or years after the infection was treated, including persistent severe fatigue and pain.

The burden on the medical system from increased cases of Lyme disease alone will be substantial. A survey of over 2,000 people who had tested positive found that roughly 26 percent had been on disability or public support, with a majority receiving support for more than two years and 37 percent for more than five years.41 Over half had visited an emergency room as a result of their illness, 15 percent had done so three to five times, and nine percent had done so six or more times. More than half of patients saw seven or more physicians to obtain a diagnosis; over a third saw 10 or more physicians.

In addition, three of the four leading causes of death in Virginia, heart disease, stroke, and chronic diseases of the lower respiratory tract, will be significantly exacerbated by climate changes. Episodes of extreme heat lead to increases in both illness and death.42 Heat waves result in more heart attacks, strokes, and asthma attacks.

A recent study found that "heat wave mortality risk increased 2.49 percent for every one degree F increase in heat wave intensity and 0.38 percent for every 1-day increase in heat wave duration. Mortality increased 5.04 percent the first heat wave of the summer versus 2.65 percent in later heat waves, compared with non-heat wave days."43

In Virginia's cities, "heat island" effects will be intensified by higher nighttime temperatures. Elderly people, who are becoming a higher and higher percentage of the population, are particularly vulnerable because they are less able to effectively regulate body temperature, and often live alone without air conditioning. People who are obese, 25 percent of Virginia's population, are also at higher risk.

Adverse health effects of climate change will also add to Virginia's fiscal pressures. Health-related expenditures account for 30 percent of the state's budget, second only to education. 44 The largest category of spending is on Virginia's Medicaid program, serving children, the elderly and people with disabilities. Despite some of the most stringent eligibility criteria in the nation, the program's budgetary impact is growing, with the elderly and people with disabilities being responsible for the heaviest fiscal burden, largely because of the prevalence of chronic problems, such as heart disease and stroke.

CLIMATE CHANGE'S IMPACT ON TOURISM

Another important sector of the economy that will suffer from these environmental impacts is the tourism and travel industry, which is Virginia's 5th largest employer. Counting direct and induced employment, the industry generated 287,700 jobs in 2010 and more than $7.5 billion in payrolls. Total expenditures by tourists in 2010 exceeded $31 billion, more than seven percent of the state's gross domestic product.45 The leading travel and tourist destinations are in Northern Virginia in Arlington, Fairfax and Loudoun counties, near the nation's capital. Of leisure travelers, 90 percent visited historic sites and battlefields and 84 percent visited beaches, national and state parks, or engaged in other nature-related activities, including hunting, fishing and bird- watching.46

This industry is at risk as climate change threatens many vacation destinations. Historic Jamestown Island could be completely inundated and popular Chincoteague could be battered and lose 80 to 90 percent of its beaches.47 Most tourists arrive in the summer months and their travel plans will be affected by higher heat and humidity, more frequent heat waves, and more frequent intense storms. Families walking with children around urban sites in 100 degree heat and humidity do not greatly enjoy their sightseeing experience. One out of five families whose beach vacations are interrupted by heavy storms cancels their plans to return in the following year.48

THE WAY FORWARD

Near the end of 2007, then Governor Tim Kaine formed a broadly based Climate Change Commission to consider the potential impacts of climate change on the state and to recommend specific actions both to mitigate and to adapt to those impacts. The Commission consulted widely among public, industry and scientific groups and put forward a Climate Change Action Plan in December 2008.49 It contained many well- founded recommendations for cost-effective actions to improve energy efficiency, to mitigate and sequester greenhouse gas emissions and to promote effective adaptation.

The Action Plan recognized that despite these opportunities for action within Virginia, climate change is a problem that requires national and international action as well as state and local participation.50 The succeeding administration has shown little interest in implementing those recommendations. According to a very recent report in the Roanoke Times, "This week, the Virginia secretary of natural resources said Gov. Bob McDonnell has no interest in reviving a climate-change commission created by his predecessor, Gov. Tim Kaine."51

The rising risks to Virginia's economy, its people and its irreplaceable natural resources cannot be avoided simply by denying that they exist. Virginia's leaders should recognize the increasing dangers that global warming poses and support implementation of the useful recommendations made by the Climate Change Action Plan or adopt equally effective policies of their own. In particular, Virginia's leaders should follow the example of former Republican Senator John Warner and support strong state, national and international action to reduce greenhouse gas emissions.

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Economic And Environmental Impacts Of Climate Change In Virginia

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Virginia's climatic changes have been thoroughly documented over recent decades. The overwhelming weight of scientific evidence predicts that climate change will continue and may accelerate unless strong action is taken to reduce global greenhouse gas emissions. Climate change threatens serious harm to Virginia's economy, its people and its treasured natural resources.