Big Idea 5: Earth is the Water Planet is the sixth of 10 short videos explaining what we all should know about the science of the Earth — how the planet's land, water, air, and life systems interact. The American Geological Institute has developed these videos to bring to life the core concepts identified by the U.S. National Science Foundation-funded Earth Science Literacy Initiative (www.earthscienceliteracy.org). For educational activities exploring each of the nine "Big Ideas of Earth Science" illustrated in the videos, visit Earth Science Week (www.earthsciweek.org).
In Why Earth Science?, stunning video sequences and images illuminate the importance of knowing how Earth works and illustrate opportunities for careers in the Earth sciences.
Big Idea 4 Earth Continually Changes is the fifth of 10 short videos explaining what we all should know about the science of the Earth — how the planet's land, water, air, and life systems interact. The American Geological Institute has developed these videos to bring to life the core concepts identified by the U.S. National Science Foundation-funded Earth Science Literacy Initiative (www.earthscienceliteracy.org). For educational activities exploring each of the nine "Big Ideas of Earth Science" illustrated in the videos, visit Earth Science Week (www.earthsciweek.org).
In Why Earth Science?, stunning video sequences and images illuminate the importance of knowing how Earth works and illustrate opportunities for careers in the Earth sciences.
Bolivia includes fifteen ecoregions:  Central Andean dry puna;  Central Andean puna;  Bolivian montane dry forest;  Southern Andean Yungas;  Dry Chaco;  Chiquitano dry forests;  Pantanal;  Cerrado;  Madeira-Tapajós moist forests;  Beni savanna;  Southwest Amazon moist forests;  Bolivian Yungas;  Central Andean wet puna;  Iquitos varzea;  Monte Alegre varzea
Central Andean dry puna
This ecoregion is a very dry, high elevation montane grassland and herbaceous community of the southern high Andes, extending through western Bolivia and northern Chile and Argentina. The vegetation is characteristically tropical alpine herbs with dwarf shrubs, and occurs above 3,500 meters (m) between the tree-line and the permanent snow-line. Dry puna is distinguished from other types of puna by its annual rainfall, or lack of rainfall. This ecoregion receives less than 400 millimeters (mm) of rainfall each year, and is very seasonal with an eight-month long dry season. The Central Andean Dry Puna is a unique ecoregion with flora and fauna highly adapted to the extreme temperatures and altitudes. The region contains forests of Polylepis, the only arborescent genus that occurs naturally at high elevations. Various species of Andean camelids are also found in this region.
The Andean puna has been highly affected by livestock grazing for centuries. The natural vegetation has been severely affected by grazing, burning, firewood collection, and clearance for cultivation. The camelids, goats and sheep in the area degrade the herbaceous vegetation, making the life cycle for the plants difficult to complete. The clearing of Polylepis forest for agriculture, firewood collection, and burning for pasture is an important threat to the endemic fauna, especially birds.
There are some protected areas within this ecoregion; most of them were created as faunal reserves. Eduardo Avaroa Andean Faunal National Reserve in the southwest corner of Bolivia (IUCN category IV) of 714,745 hectares (ha), is an area principally for the protection of birds that inhabit the different lagoons in the Reserve. Several censuses of the flamingo population in this reserve registered 26,600 individuals. Sajama National Park in western Bolivia (IUCN category II) of 100,230 ha, is one of the most diverse Andean Parks in the ecoregion with 25 species of mammals registered. This park includes a forest of Polylepis with trees up to 5-meters high.Central Andean puna
This ecoregion is a high elevation montane grassland in the southern high Andes, extending from southern Peru, though Bolivia, into northern Argentina. Open meadows are dotted with an assortment of rock, bunchgrass, herbs, moss, and lichens. This ecoregion is continuous and transitional between the wet puna to the north and west, and the dry puna to the south. The landscape is characteristically mountainous, with snow capped peaks, mountain pastures, high lakes, plateaus, and valleys.
This ecoregion faces increasing mining activity that is leading to the destruction of its scarce plant cover as well as the contamination of some bodies of water and the soil. In addition, this region has a large number of population centers and highways that cross the Andes, leading to a decline in natural habitat and growing pressures on the existing fauna.Bolivian montane dry forest
This ecoregion is restricted to south-central Bolivia, barely touching northwest Argentina. It is quite restricted, forming a transition between the Yungas and Puna zones in Bolivia. This dry region is characterized by steep hillsides, cliffs, and valleys and contains a number of endemic species of avifauna including the Bolivian recurvebill and Bolivian blackbird. A number of national parks protect a significant area of habitat, however more are needed in order to preserve this region heavily affected by urban expansion.
There are a number of National Parks (NPs) and protected areas in this ecoregion, including: Tariquía National Reserve (2469 kilometers squared) and the slightly smaller Cama Valley Biological Reserve and Toro Toro NP. However, these three sites combined probably do not exceed 6000 km2 and more reserves within this region would be ideal.Southern Andean Yungas
The Southern Andean Yungas are loosely bordered to the east by the Chaco, and tightly interdigitated to the west with Bolivian Montane Dry Forest, spanning southwestern Bolivia and northwestern Argentina. This ecoregion is extremely fascinating from a biogeographic perspective, as it contains what may be the last of the isolated ‘evergreen’ forests resulting from Quaternary glaciations. This region is rich in fauna species, especially avifauna. Many tropical species meet their southern limits of geographic distribution in this region. The forests of Argentina have suffered more damage than Bolivia. A number of national parks protect the forest of this ecoregion including Tariquía National Reserve (2469 km2 in Boloivia.
The extent of deforestation in Bolivia has not been documented with certainty, but there are large areas of degraded land. However, some large and intact regions still persist in Bolivia, such as the forests between the Pilcomayo and Pilaya rivers in Montes Chapeados that span ~1300 km2.Dry Chaco
The Chaco ecoregion as defined herein is generally restricted to the northwestern two-thirds of western Paraguay, and east of the Andes in southeastern Bolivia and northwestern Argentina. The Guarani Indians initially described this region as "Gran Chaco", which implies productive hunting grounds. Today much of the northern Chaco is still abundant with large game mammals, suggesting sustainably harvested populations. However, this is no longer the case in much of the southern Chaco where rampant overgrazing and human population growth has preceded the pristine nature of the Chaco. An important migration route, many species of avifauna can be found in this ecoregion throughout the year. More protected areas are needed in order to save this habitat from overwhelming agricultural development.
Much of the Chaco is in various stages of alteration due to grazing of cattle and goats, the latter especially in the southern Chaco. This development is perhaps least severe around the border of the Paraguayan and Bolivian Chaco, and most extensive in the Argentinean Chaco. Paved road development projects provide easy access to remote sites to hunt game and alter pristine wilderness for agrarian development. A good example of this is the Trans-Chaco highway that connects Paraguay and Bolivia (completed in late 1990s).Chiquitano dry forests
Roughly in the center of the South American continent, most of the Chiquitano forest lies within the eastern lowlands of Santa Cruz, Bolivia, with smaller patches extending into western Mato Grosso, Brazil. This ecoregion is not only a dry forest but a transition zone between the moist Amazonian forests of the north and these dryer forest of the southern Chaco regions. This forest takes its name from the indigenous groups, Chiquitanos, which inhabited them at the time of European colonization. It provided the scenario for most of the Jesuit missionary work during the 17th and 18th century.
This is the largest patch of healthy dry forest ecosystem alive today, and one of the most biologically diverse dry forests in the world. Two large blocks of forest in outstanding conservation condition, comprising 20% of the original ecoregion, remain. Both blocks lie east of San Jose de Chiquitos, split into a north and a south block by a road with ranches along it. Two protected areas Otuquis and San Matias, include important parts of this remnant forest, but linkages between them and effective management are urgent. The Tucavaca Valley is the middle area which needs to be put under protection to provide long-term ecological viability.Pantanal
Located roughly in the center of South America, near the borders of Brazil, Bolivia, and Paraguay, the Pantanal stretches from 16° to 20° S latitude. The majority of the ecoregion occurs in Brazil as a floodplain around the Rio Paraguay and tributaries. The terrain is essentially flat, ranging from 75 to 200 meters (m) above sea level. This elevation coupled with the gentle slope of the rivers in the area, account for the massive flooding during the annual wet season when up to 78% of the area can be submerged.
The Pantanal is the largest wetland in South America, and the largest wetland in the world that has not been substantially modified by humans. While endemism in the area is low, the sheer abundance of large birds, reptiles, and mammals mark its importance as a huge reservoir of biodiversity. Much of the ecoregion remains intact; however, pesticide runoff constitutes a major threat to the watershed of the Rio Paraguay. Also, a project by several governments plans to provide navigable waterway for shipping and dams for hydroelectricity generation, which would drastically alter this pristine habitat.
While cattle ranching is not intense, this type of land use causes some degree of habitat modification. The majority of the Pantanal is in close to pristine condition with most of its biota still extant. Only two dirt roads cross the area from the northern end near Cuiabá, and one road bisects the area between Campo Grande and Corumbá. Less than 3 % of the Pantanal is currently included in protected areas; the remainder of the land is privately owned. The Pantanal National Park covers 1,370 square kilometers (km2) area along the Rio Paraguay, but unfortunately it is dominated by areas completely inundated during the wet season and protects little savanna or forest habitat.Cerrado
Cerrado is the largest savanna region in South America and biologically the richest savanna in all the world. It encompasses Central Brazil (most of Mato Grosso, Mato Grosso do Sul, and Tocantins; western Minas Gerais and Bahia; southern Maranhão and Piauí; all Goiás and Distrito Federal; and small portions of São Paulo and Paraná), northeastern Paraguay and eastern Bolivia. Because of its central position in South America, Cerrado has borders with the largest South American biomes: the Amazon basin (on north), Chaco and Pantanal (on west), Caatinga (on northeast), and Atlantic forest (on east and south).
This ecoregion also contains an amazing about of biodiversity, over 10,400 species of vascular plants are found, fifty of which are endemic. Fauna diversity is very high also with 180 species of reptiles, 113 of amphibians, 837 of birds and 195 of mammals. Major efforts are needed to preserve what is one of the biologically richest savanna in the world, since only one percent of this ecoregion is protected and agriculture development continues to destroy habitat.
Around 67 percent of the Cerrado ecoregion has been already either completely converted or modified in a major way. In contrast, only 1 percent of the total area of the Cerrado Region is protected in parks or reserves. Most of the large-scale human modification in the Cerrado took place in the last 50 years.Madeira-Tapajós moist forests
The Madeira-Tapajós moist forest ecoregion lies in central Amazonia in Brazil south of the Amazon River. It spans the lowland Amazon Basin reaching south to the border with Bolivia. It encompasses portions of three Brazilian states (Amazonas, Rondônia, Mato Grosso) and part of the Bolivian Department of Beni.
This ecoregion is bound on three sides by large rivers, the Solimões (Amazon) to the north, Madeira to the west, and Tapajós to the east, which act as formidable barrier to the distributions of many species.The region includes the large interfluve between the Madeira and Tapajós Rivers, both major tributaries to the mighty Amazon, and extends southward into the headwaters of the Tapajós to the Rio Guaporé Basin. The region encompasses a variety of vegetation types including dense lowland rain forest, dense submontane rain forest, open-canopy submontane rain forest, and woodland savanna.
This region hosts one of the most degraded environments of central Amazonia.Beni savanna
The Beni savannas are located in the lowlands of the southwestern Amazon Basin, extending northeastward from the foot of the Andean ranges. Almost all of the ecoregion lies within Bolivia in the departments of El Beni, Cochabamba, La Paz, Pando, and Santa Cruz, with small areas along the Iténez (Guaporé) River in the Brazilian State of Rondonia and in the Pampas del Heath of the Madre de Dios Department of Peru.
The Beni savannas, also known as the Moxos plains, are the third largest complexes of savannas in South America. This ecoregion has been identified as a plant diversity and endemic center. The abundance of fauna and flora, including threatened species, makes this region highly valuable.
Since the arrival of the Jesuits in the 1680s, the predominant land use of the Llanos de Moxos ecoregion has been cattle ranching on the savannas and wetlands. Anthropogenic fire is used to remove low quality biomass and stimulate regrowth at the end of the dry season. Consequently, few areas remain in their pre-European state. Some forest islands are actually remaining fragments from a previously larger forest stand reduced by human activities; however, historical deforestation in the Moxos region has not yet approached the extent in neighboring regions.
Beni savannas and wetland areas are poorly represented in Bolivia's protected areas system. The Alto Madidi National Park contains areas of these savannas in the north of the La Paz Department. The Manuripi-Heath National Amazonian Reserve of La Paz and Pando contains small islands of savanna. The Beni Biological Station is a UNESCO Biosphere Reserve located in the southwest of this region. It includes 1,350 km2 of flat lowlands, but with little savanna. The Iténez Fiscal Reserve of 15,000 km2 is located on the eastern extreme, but only partially in the Llanos de Moxos ecoregion. Timber extraction is the main activity in this reserve. A national park has been proposed for the savannas and Mauritia palm swamps to the south of the Iténez Fiscal Reserve. A large portion of the southern savannas and wetlands are located with the Multi-ethnic Indigenous Territory and the Isiboro-Sécure Indigenous Territory/National Park. Land tenure and management issues in these territories, however, remain uncertain. The Sirionó Indigenous Territory occupies a portion of the forest-savanna mosaic approximately 60 km east of the Mamoré River. The Ríos Blanco and Negro Wildlife Reserve in Santa Cruz contains a portions of the southern Baures savannas and wetlands.Southwest Amazon moist forests
This ecoregion located in the Upper Amazon Basin, is characterized by a relatively flat landscape with alluvial plains dissected by undulating hills or high terraces.
The biota of the southwest Amazon moist forest is very rich because of these dramatic edaphic and topographical variations at both the local and regional levels.
This ecoregion has the highest number of both mammals and birds recorded for the Amazonian biogeographic realm: 257 with 11 endemics for mammals and 782 and 17 endemics for birds. The inaccessibility of this region, along with few roads, has kept most of the habitat intact. Also, there are a number of protected areas, which preserve this extremely biologically rich ecoregion.
The Manuripi Heath National Reserve is located in the southernmost area of this region in Bolivia covering 18,900 km2 of dense tropical forest.
Much of the natural habitat of the region remains intact, protected by sheer inaccessibility. People have dwelled along the major rivers for millennia and have subtly altered the forests on a small scale, but around the urban centers development proceeds.Bolivian Yungas
The Bolivian Yungas are restricted to west-central Bolivia and extreme southeastern Peru. The northern, southern, western and eastern boundaries of this ecoregion terminate approximately at the 13° and 17° south latitudes and 69° and 63° west longitudes, respectively.
This ecoregion forms a transition along Andean slope between Amazonian and highland Puna habitat. Habitats range from montane forest and cloud forest, to lowland forest. The high levels of biodiversity and endemism characterizing this unique ecoregion are attributable to its transitional position between highly contrasting habitats, as well as extremely heterogeneic topography. Rare fauna species are present such as the spectacled bear, Geoffroy’s cat, and green-capped tanager. Much of this region is under the protection of national parks, however slash and burn practices threaten most of the unprotected habitat.
Fortunately, most protected areas in this ecoregion are difficult to cultivate due to difficult access, steepness of terrain, and very high rainfall. There are a number of relatively large protected areas covering this ecoregion. In Bolivia are Maididi National Park 19,000 km2, Carrasco National Park – 13,000 km2, Isiboror Sécure National Park – 11,000 km2, Amboro National Park - 1800 km2, and Bellavista Protection Forest Reserve – 900 km2 which equate to over 60,000 km2 of protected area. The distribution of these protected areas within the Yungas is fairly well covered in light of petroleum concessions and habitat alteration.Central Andean wet puna
This ecoregion is a high elevation, wet, montane grassland in the southern high Andes, occurring from northern Peru to eastern Bolivia. Occurring above tree-line, that is to say above approximately 3,500 meters (m) elevation, this regions is composed of bunchgrass communities, wetlands, small shrubs, and trees, and herbaceous plants. The wet puna is bordered on the west by the dry Sechura desert and to the east by the wet Peruvian Yungas, which makes for extreme transitional zones. The landscape is characteristically mountainous, with snow capped peaks, mountain pastures, high lakes, plateaus, and valleys.
In Bolivia, the ecoregion is found in the south of the department of La Paz. The Andes divides into two mountain systems- Cordillera Occidental and the Cordillera Oriental- close to the border of Peru and Bolivia. The Cordillera Oriental is in turn divided into two Cordilleras, the Real and the Central. The Cordillera Real contains various mountain chains, among which are the Cordillera de Apolobamba, Cordillera de Muñecas, Cordillera de La Paz, and Cordillera de Tres Cruces.
The ecoregion contains snow-capped peaks, glacial lakes, and several rivers that originate in the Cordilleras. The biggest lake in the ecoregion is Lake Titicaca, which is the highest lake in the world, at an elevation of 3,800 m.a.s.l. Its main tributaries in Bolivia are the Suches and Tiwanacu rivers.
National Faunal Reserve Ulla-Ulla (IUCN category IV, 150,000 ha) is located on the border of Peru and Bolivia. Ulla-Ulla is a biosphere reserve that protects various animals. The most important is the vicuña (Vicugna vicugna), which has been protected since 1965. The Vicuña population declined significantly due to hunting to get the fine wool fiber, but it has recovered in the past decade. The population of the vicuñas in 1996 was of 6,500 individuals.Iquitos varzea
This ecoregion comprises the low, seasonally inundated river basins of the upper Amazon, Ucayali, Marañon, and Madre de Dios, in Peru and Bolivia, several smaller tributaries to the Amazon in Peru, and the upper Juruá and Purus Rivers in Brazil. A large portion of the region centers around the extensive seasonally flooded plain in northeastern Peru at the confluence of the Marañon and Ucayali Rivers that join to form the Amazon. The Rivers Pacaya and Simiria bisect this plain. The large urban center of Iquitos lies at 100 meters (m) elevation, and the topography, on the whole, is very flat with micro-undulations resulting from river meander.
The várzea, because it lies along water "highways," is a region much affected by human activities, both historically and in the present. Today much of the várzea is used for agriculture and managed forest by smallholder farmers, but their systems tend to be biologically diverse agroecosystems. Hence, much of the forest is managed or unmanaged secondary forest. Nevertheless, this region suffers a high degree of deforestation.Monte Alegre varzea
This ecoregion in Brazil comprises portions of the low, seasonally inundated river basins of the central and lower Amazon, much of the length of the Madeira River Basin, and the mouth of the Purus River where it joins the Solimões (Amazon), as well as several smaller tributaries to these. An isolated patch occurs on the border of Brazil and Bolivia along the Mamoré River.
Biodiversity is extremely high in this flooded forest along the lower Amazon. The region hosts an amazing number of avifauna; there are 681 reported bird species including red-shouldered macaws (Ara nobilis), sun parakeets (Aratinga solstitialis), and green-rumped parrotlets (Forpus passerinus). Over two hundred species of mammals are found here including jaguars (Panthera onca), ocelots (Leopardus pardalis), tapirs (Tapirus terrestris), and a number of primate species. There are few protected areas in this ecoregion, which is threatened by cattle ranching and large scale agriculture.Context
Ecoregions are areas that:
 share a large majority of their species and ecological dynamics;
 share similar environmental conditions; and,
 interact ecologically in ways that are critical for their long-term persistence.
Bhutan has six ecoregions as shown in the figure below (from north to south):
- Eastern Himalayan alpine shrub and meadows (Blue)
- Eastern Himalayan subalpine conifer forests (Aqua)
- Eastern Himalayan broadleaf forests (Light Yellow)
- Himalayan subtropical pine forests (Sky Blue)
- Himalayan subtropical broadleaf forests (Mid-yellow)
- Terai-Duar savanna and grasslands (Dark Yellow)
The transistion from the Himalayan subtropical broadleaf forests (6) ecoregion to the Brahmaputra Valley semi-evergreen forests ecoregion of northern Indian (at the bottom of the figure) approximately follows the southern border of Bhutan.
Eastern Himalayan alpine shrub and meadows
The Eastern Himalayan Alpine Shrub and Meadows represent the alpine scrub and meadow habitat along the Inner Himalayas to the east of the Kali Gandaki River in central Nepal. Within it are the tallest mountains in the world-Everest, Makalu, Dhaulagiri, and Jomalhari-which tower far above the Gangetic Plains. The alpine scrub and meadows in the eastern Himalayas are nested between the treeline at 4,000 meters (m) and the snowline at about 5,500 m and extend from the deep Kali Gandaki gorge through Bhutan and India's northeastern state of Arunachal Pradesh, to northern Myanmar.
The Eastern Himalayan Alpine Shrub and Meadows ecoregion supports one of the world's richest alpine floral displays that becomes vividly apparent during the spring and summer when the meadows explode into a riot of color from the contrasting blue, purple, yellow, pink, and red flowers of alpine herbs. Rhododendrons characterize the alpine scrub habitat closer to treeline. The tall, bright-yellow flower stalk of the noble rhubarb, Rheum nobile (Polygonaceae), stands above all the low herbs and shrubs like a beacon, visible from across the valleys of the high Himalayan slopes.
The plant richness in this ecoregion sitting at the top of the world is estimated at more than 7,000 species, a number that is three times what is estimated for the other alpine meadows in the Himalayas. In fact, from among the Indo-Pacific ecoregions, only the famous rain forests of Borneo are estimated to have a richer flora. Within the species-rich landscape are hotspots of endemism, created by the varied topography, which results in very localized climatic variations and high rainfall, enhancing the ability of specialized plant communities to evolve. Therefore, the ecoregion boasts the record for a plant growing at the highest elevation in the world: Arenaria bryophylla, a small, dense, tufted cushion-forming plant with small, stalkless flowers, was recorded at an astonishing 6,180 m by A. F. R. Wollaston.
The ecoregion has fourteen protected areas that cover more than 11,680 km2, including several-such as Annapurna, Makalu Barun, Sagarmatha, Jigme Dorgi, and Sakteng-that exceed 1,000 km2 (or, as in the case of Annapurna and Jigme Dorji, 2,500 km2). Although the total area protected represents about 30 percent of the ecoregion's area, the reserves are inequitably distributed. Most of the protected areas are in Nepal and Bhutan, whereas the eastern section of the ecoregion, especially in Myanmar, receives little or no formal protection. Because of the high species turnover along the east-west axis, more equitable protection is necessary for better representation of the ecoregion's biodiversity. Moreover, about half of the areas that lie within the existing protected areas represent bare rock and areas covered with permanent ice, not very important habitat for biodiversity conservation.Eastern Himalayan subalpine conifer forests
The ecoregion represents the belt of conifer forest between 3,000 and 4,000 meters, from east of the Kali Gandaki River in Nepal through Bhutan and into the state of Arunachal Pradesh, in India. These forests usually are confined to the steeper, rocky, north-facing slopes and therefore are inaccessible to human habitation and cultivation.
The Eastern Himalayan Sub-Alpine Conifer Forests represent the transition from the forested ecoregions of the Himalayas to treeless alpine meadows and boulder-strewn alpine screes. Their ecological role within the interconnected Himalayan ecosystem, which extends from the alluvial grasslands along the foothills to the high alpine meadows, makes the forests of this ecoregion a conservation priority. Conservation of the Himalayan biodiversity is contingent on protecting the interconnected processes among the Himalayan ecosystems. For instance, several Himalayan birds and mammals exhibit altitudinal seasonal migrations and depend on contiguous habitats that permit these movements. The integrity of the watersheds of the rivers that originate in the high mountains of this majestic range depends on the intactness of habitat, from the high elevations to the lowlands. If any of the habitat layers are lost or degraded, these processes will also be disrupted.
The ecoregion straddles the transition from the southern Indo-Malayan to the northern Palearctic fauna. Here tigers yield to snow leopards, and sambar are replaced by blue sheep. But the ecoregion also has its own specialized flora and fauna, such as the musk deer and red panda, which are limited to these mature temperate conifer forests.Eastern Himalayan broadleaf forests
This ecoregion represents the band of temperate broadleaf forest between 2,000 and 3,000 meters, stretching from the deep Kali Gandaki River gorge in central Nepal, eastward through Bhutan, into India's eastern states of Arunachal Pradesh and Nagaland.
The Eastern Himalayan Broadleaf Forests is one of the few Indo-Pacific ecoregions that is globally outstanding for both species richness and levels of endemism. The eastern Himalayas are a crossroads of the Indo-Malayan, Indo-Chinese, Sino-Himalayan, and East Asiatic floras as well as several ancient Gondwana relicts that have taken refuge here. Overall, this ecoregion is a biodiversity hotspot for rhododendrons and oaks; for instance, Sikkim has more than fifty rhododendron species, and there are more than sixty species in Bhutan.
In addition to the outstanding levels of species diversity and endemism, the ecoregion also plays an important role in maintaining altitudinal connectivity between the habitat types that make up the larger Himalayan ecosystem. Several birds and mammals exhibit altitudinal seasonal migrations and depend on contiguous habitat up and down the steep Himalayan slopes for unhindered movements. Habitat continuity and intactness are also essential to maintain the integrity of watersheds along these steep slopes. If any of the habitat layers, from the Terai and Duar grasslands along the foothills through the broadleaf forests and conifers to the alpine meadows in the high mountains, are lost or degraded, these processes will be disrupted. For instance, several bird species are found in the temperate broadleaf forests of Bhutan where the habitat is more intact and continuous with the subtropical broadleaf forests lower down, but in Nepal where the habitat continuity has been disrupted, these same birds have limited ranges.
The fifteen protected areas that extend into the ecoregion cover about 5,800 kilometers2 (7 percent) of the ecoregion. With the exception of Namdapha, none exceed 1,000 kilometers2. However, there are several very large reserves that overlap across several ecoregions, although only parts of the reserves are represented in this one. Examples include Thrumsing La, Jigme Dorji, and Black Mountains national parks in Bhutan. The Jigme Dorji National Park exceeds 4,000 kilometers2 and sprawls across three ecoregions to include the alpine meadows, sub-alpine conifer forests, and temperate broadleaf forests represented by this ecoregion. Two others, Kulong Chu and Black Mountains, exceed 1,000 kilometers2, and Cha Yu, Makalu-Barun, Mehao, and Thrumsing La are more than 500 kilometers2.
Bhutan recently revised its protected area system to link the existing reserves. Plans to develop similar linkages through conservation landscapes have been proposed in the other areas in the eastern Himalayas. These plans use ecoregions as basic conservation units for representation of biodiversity.Himalayan subtropical pine forests
The subtropical pine forests represented by this ecoregion extend as a long, disjunct strip from Pakistan in the west, through the states of Jammu and Kashmir, Himachal Pradesh, and Uttar Pradesh in northern India, into Nepal and Bhutan. Although Champion and Seth indicate the presence of large areas of Chir pine in Arunachal Pradesh, the easternmost extent of large areas of Chir pine is in Bhutan.
The Himalayan Subtropical Pine Forests are the largest in the Indo-Pacific region. They stretch throughout most of the 3,000-kilometer length of this the world's youngest and highest mountain range. Some scientists believe that climate change and human disturbance are causing the lower-elevation oak forests to be gradually degraded and invaded by the drought-resistant Chir pine (Pinus roxburghii), the dominant species in these subtropical pine forests. Biologically, the ecoregion does not harbor exceptionally high levels of species richness or endemism, but it is a distinct facet of the region's biodiversity that should be represented in a comprehensive conservation portfolio.
More than half of this ecoregion's natural habitat has been cleared or degraded. In central and eastern Nepal, terraced agriculture plots, especially between 1,000 and 2,000 m, have replaced nearly all the natural forest. Other than in the less populated western regions, little natural forest remains in Nepal. Similarly, habitat loss is widespread in Pakistan, Jammu and Kashmir, and Himachal Pradesh and Uttar Pradesh states in India. The few larger blocks of remaining habitat blocks are now found in Bhutan.Himalayan subtropical broadleaf forests
This ecoregion represents the east-west-directed band of Himalayan subtropical broadleaf forests along the Siwaliks or Outer Himalayan Range, lying between 500 and 1,000 meters (m). The ecoregion achieves its greatest coverage in the middle hills of central Nepal, but the long, narrow ecoregion extends through Darjeeling into Bhutan and also into the Indian State of Uttar Pradesh. The Kali Gandaki River, which has gouged the world's deepest river valley through the Himalayan Range, bisects the ecoregion.
The Himalayan Subtropical Broadleaf Forests ecoregion includes several forest types along its length as it traverses an east to west moisture gradient. The forest types include Dodonea scrub, subtropical dry evergreen forests of Olea cuspidata, northern dry mixed deciduous forests, dry Siwalik sal (Shorea robusta) forests, moist mixed deciduous forests, subtropical broadleaf wet hill forests, northern tropical semi-evergreen forests, and northern tropical wet evergreen forests.
The ecoregion also forms a critical link in the chain of interconnected Himalayan ecosystems that extend from the Terai and Duar grasslands along the foothills to the high alpine meadows at the top of the world's highest mountain range. For instance, several Himalayan birds and mammals exhibit seasonal altitudinal migrations and depend on contiguous habitat to permit these movements. Therefore, conservation actions in the Himalayas must pay due attention to habitat connectivity because degradation or loss of a habitat type along this chain will disrupt these important ecological processes.Terai-Duar savanna and grasslands
The Terai-Duar Savanna and Grasslands ecoregion sits at the base of the Himalayas, the world's youngest and tallest mountain range. About 25 kilometers wide, this narrow lowland ecoregion is a continuation of the Gangetic Plain. The ecoregion stretches from southern Nepal's Terai, Bhabar, and Dun Valleys eastward to Banke and covers the Dang and Deokhuri Valleys along the Rapti River. A small portion reaches into Bhutan, and each end crosses the border into India's states of Uttar Pradesh and Bihar.
This ecoregion contains the highest densities of tigers, rhinos, and ungulates in Asia.
One of the features that elevates it to the Global 200 ecoregion is the diversity of ungulate species and extremely high levels of ungulate biomass recorded in riverine grasslands and grassland-forest mosaics.
The world's tallest grasslands, found in this ecoregion, are the analogue of the world's tallest forests and are a phenomenon unto themselves. Very tall grasslands are rare worldwide in comparison with short grasslands and are the most threatened. Tall grasslands are indicators of mesic or wet conditions and nutrient-rich soils. Most have been converted to agricultural use.Context
Ecoregions are areas that:
 share a large majority of their species and ecological dynamics;
 share similar environmental conditions; and,
 interact ecologically in ways that are critical for their long-term persistence.
Scientists at the World Wildlife Fund (WWF), have established a classification system that divides the world in 867 terrestrial ecoregions, 426 freshwater ecoregions and 229 marine ecoregions that reflect the distribution of a broad range of fauna and flora across the entire planet.
Twenty years after the 1992 Earth Summit that led to the establishment of two major environmental conventions (the United Nations Framework Convention on Climate Change and the Convention on Biological Diversity), the author believes that Rio+20 (2012) presents an opportunity for the leaders of the world's governments to re-examine their commitments to—and ability to implement—sustainable development.
This Editorial, authored by Georgina M. Mace*, appeared first in PLoS Biology—a peer-reviewed, open access journal published by the Public Library of Science. The article is a verbatim version of the original and is not available for edits or additions by Encyclopedia of Earth editors or authors. Companion articles on the same topic that are editable may exist within the Encyclopedia of Earth.The Limits to Sustainability Science:
Ecological Constraints or Endless Innovation?
The United Nations Conference on Sustainable Development (Rio+20) takes place in Rio de Janeiro on 20–22 June 2012. Twenty years after the 1992 Earth Summit that led to the establishment of two major environmental conventions (the United Nations Framework Convention on Climate Change and the Convention on Biological Diversity), Rio+20 presents an opportunity for the leaders of the world's governments to re-examine their commitments to sustainable development. An Essay by Burger et al.  in this issue and a Perspective contributed in response by Matthews and Boltz  raise concerns that certainly should be considered in Rio. But it's almost certain they won't be.
Burger et al.  present the case that the macroecology of sustainability is woefully under-represented in sustainability science. Ecological principles must govern sustainability, yet sustainability science is largely concerned with social–environmental interactions and barely considers physical limits on resource use. Escalating rates of resource use per capita, along with an increasing human population and environmental change, must, they argue, lead to limits in the availability of energy and materials on which the world's continuing economic development depends. Matthews and Boltz do not contest the evidence presented by Burger et al., but they are more optimistic that human ingenuity and adaptability will both buy time and provide solutions that will allow human societies to overcome resource limitation and continue to grow. Specifically, they contend that, despite the geometric increase in both population and resource use, a societal transformation is under way based around flexible, green economies that are in turn based in dynamic, variable ecosystems. They further argue that environmental pessimism will have less traction in policy-making than providing positive and creative approaches to these awkward problems.
This discussion is not new. Two issues have continued to be debated over the 20 years since the first Rio Earth Summit. One concerns the concept of sustainability and what it means in practice. A common query that has no easy answer asks about the sustainability of what, for whom, where, and over what time scales? Endless rhetoric about sustainable consumption and sustainable development hardly ever confronts the reality that, in most cases, what is sustainable for one sector of human society at one time and place rarely has no impact on other resources, or on environmental processes separated in time and space. The second theme, now discussed for over 40 years, is about the limits to growth. Any sensible person will agree that growth cannot continue indefinitely in a finite world. Yet over recent decades, the evidence indicates continuing growth, often at close to exponential rates in both population and consumption. How is this possible? Are we borrowing from the future, are we using resources that are far from their limits, or are we adapting creatively through innovation and technologically driven efficiency and replacement? Or, are we actually failing to act responsibly given evidence that certain limits are dangerously close, or even are already transgressed? 
Burger et al. present the argument for macroecological limits based on three inter-related themes and the evidence behind them. First, they describe how the flow of resources from the environment to support human societies must conform to physical laws concerning matter and energy. Therefore, at any spatial scale, flows of energy and nutrients for production and growth must come from somewhere, and a positive balance in one context will be felt as a negative balance somewhere else. Since smaller human systems (e.g., in towns and villages) are embedded in larger environmental systems, these flows and fluxes eventually add up to the global scale, where the finite nature of the biosphere and earth system must ultimately set limits. In fact, for the systems and resources that Burger et al. examine, there is evidence that we may already be reaching these limits. In the case of what is clearly a well-managed salmon fishery, resource flows have significant impacts on other components of the ecosystems (e.g., reduced resources for predators or decomposers). In what is an apparently sustainable urban system, the environmental costs to the surrounding landscape or on ecosystems elsewhere are shown to be substantial. In showing how per capita consumption of many materials and resources is now declining, Burger et al. suggest that their data may be the first evidence that we are approaching limits for some resources such as phosphorous, arable land, and freshwater. Some of this decline may be due to efficiencies, redundancy, and technological replacement of resources by innovative human societies, as Matthews and Boltz describe, but they agree that, ultimately, global constraints exist.
There is no doubt that these are critical issues for the environmental sciences to address. The research questions are difficult to pin down because they are embedded in a complex nexus of issues where ecological and evolutionary sciences, natural resource management, poverty alleviation, equitable and sustainable growth, individual rights and responsibilities, and the governance of the environment all converge. The academic community is increasingly engaged in defining the agenda for new science that will be needed. For example, following the recent Planet under Pressure meeting held in London, scientists sent a declaration to the Rio+20 conference  stressing that society is taking substantial risks by delaying urgent and large-scale action for environmental sustainability, and calling for a new approach to research that is more integrative, international, and solutions-oriented. In a similar vein, the 2012 Royal Society report on People and the Planet  concludes that rapid and widespread changes in the human population, coupled with unprecedented levels of consumption, present profound challenges to human health and wellbeing with important implications for future life on our finite planet.
The difference between ecological pessimism in Burger et al. and technological optimism in Matthews and Boltz is only one of the many ways that the problem can be viewed. Often the focus needs to be on extremes, or on non-linearities and irreversibilities in environmental systems that do not sit easily in standard economic analysis . For example, species and ecosystems may be affected more by increases in the frequency of climate extremes than by shifts in mean values of temperature and precipitation. At a societal level, average rates of growth and development, both within and between countries, hide enormous disparity between the very rich and the very poor. The number or proportion of people living in extreme poverty is the key concern for development, not the average level of development, which is often the statistic of choice for scientific assessment and national reporting. More affluent societies tend to be more unequal, and inequality is itself an indicator of low wellbeing . Similarly, while changes to some environmental resources are reversible with good restorative management, for many more, changes produce outcomes that are hard to predict (e.g., species responses to climate change), incur long time lags to recovery (e.g., recovery of fisheries following over-harvesting), or allow recovery but to an altered state (e.g., freshwater lakes following recovery from eutrophication) . Non-linearities are a particular problem for resource management, where flows of resources that contribute to production, and constitute one element of national accounting via gross domestic product, take no account of the condition of stocks or resources. However, when resources are close to being depleted or exhausted, prices rise, pressures may increase, and complete collapse of the resource becomes more likely . In some other cases, such as the extinction of species or the loss of biomes and biodiversity, the loss is irreversible.
Sustainability science therefore needs much stronger connections with environmental sciences, including macroecology. Green economies, a major focus for Rio+20, similarly need to be embedded in ecological principles and not simply be focused on economic growth based on new, greener production systems. Hopefully, in another 20 years, we can celebrate successful outcomes from the emergence of this integrated science for the environment and people.References
- Burger J. R, Allen C. D, Brown J. H, Burnside W. R, Davidson A. D, et al. (2012) The macroecology of sustainability. PLoS Biol 10: e1001345. doi:10.1371/journal.pbio.1001345.
- Matthews J. H, Boltz F (2012) The shifting boundaries of sustainability science: are we doomed yet? PLoS Biol 10: e1001344. doi:10.1371/journal.pbio.1001344.
- Rockstrom J, Steffen W, Noone K, Persson A, Chapin F. S, et al. (2009) A safe operating space for humanity. Nature 461: 472–475. Find this article online
- Planet under Pressure (29 March 2012) State of the Planet Declaration. Planet under pressure: new knowledge towards solutions. Available: http://www.planetunderpressure2012.net/pdf/state_of_planet_declaration.pdf. Accessed 14 May 2012.
- Royal Society (2012) People and the planet. The Royal Society Science Policy Centre.
- Dasgupta P, Mäler K-G (2003) The economics of non-convex ecosystems: introduction. Environmental and Resource Economics 26: 499–525. Find this article online
- Arrow K, Bolin B, Costanza R, Dasgupta P, Folke C, et al. (2003) Economic growth, carrying capacity, and the environment. Science 268: 520–521. Find this article online
- Courchamp F, Angulo E, Rivalan P, Hall R. J, Signoret L, et al. (2006) Rarity value and species extinction: the anthropogenic allee effect. PLoS Biol 4: e415. doi:10.1371/journal.pbio.0040415.
*Georgina M. Mace, Department of Life Sciences, Imperial College London, London, United Kingdom.
- Citation: Mace GM (2012) The Limits to Sustainability Science: Ecological Constraints or Endless Innovation? PLoS Biol 10(6): e1001343. doi:10.1371/journal.pbio.1001343
- Published: June 19, 2012
- Copyright: © 2012 Georgina M. Mace. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
- Competing interests: The authors have declared that no competing interests exist.
Despite the relative lack of information integrating the health, ecological, and economic impacts of different fish dietary choices, clear and simple guidance is needed to effect wise consumption of wild and domesticated fisheries resources.
This Review article, written by Emily Oken, Anna L. Choi, Margaret R. Karagas, Koenraad Mariën, Christoph M. Rheinberger, Rita Schoeny, Elsie Sunderland, and Susan Korrick* appeared first in Environmental Health Perspectives—the peer-reviewed, open access journal of the National Institute of Environmental Health Sciences.
The article is a verbatim version of the original and is not available for edits or additions by Encyclopedia of Earth editors or authors. Companion articles on the same topic that are editable may exist within the Encyclopedia of Earth.Which Fish Should I Eat?
Fish Consumption Choices Abstract
Background: Diverse perspectives have influenced fish consumption choices.
Objectives: We summarized the issue of fish consumption choice from toxicological, nutritional, ecological, and economic points of view; identified areas of overlap and disagreement among these viewpoints; and reviewed effects of previous fish consumption advisories.
Methods: We reviewed published scientific literature, public health guidelines, and advisories related to fish consumption, focusing on advisories targeted at U.S. populations. However, our conclusions apply to groups having similar fish consumption patterns.
Discussion: There are many possible combinations of matters related to fish consumption, but few, if any, fish consumption patterns optimize all domains. Fish provides a rich source of protein and other nutrients, but because of contamination by methylmercury and other toxicants, higher fish intake often leads to greater toxicant exposure. Furthermore, stocks of wild fish are not adequate to meet the nutrient demands of the growing world population, and fish consumption choices also have a broad economic impact on the fishing industry. Most guidance does not account for ecological and economic impacts of different fish consumption choices.
Conclusion: Despite the relative lack of information integrating the health, ecological, and economic impacts of different fish choices, clear and simple guidance is necessary to effect desired changes. Thus, more comprehensive advice can be developed to describe the multiple impacts of fish consumption. In addition, policy and fishery management inter-ventions will be necessary to ensure long-term availability of fish as an important source of human nutrition.Keywords: advisory, economics, fish, methylmercury, nutrition, ocean ecology, poly-chlorinated biphenyls, poly-unsaturated fatty acid, toxicology.
The public receives fish consumption advice from a variety of perspectives, including toxi-cant, nutritional, ecological, and economic viewpoints. For example, U.S. federal and state agencies that are concerned about exposure to toxi-cants in fish, such as methyl-mercury (MeHg) and polychlorinated biphenyls (PCBs), have issued fish consumption advisories recom-mending that at-risk groups limit consumption of fish [U.S. Environmental Protection Agency (EPA) 2004]. However, national organizations of physicians and nutritionists encourage fish consumption for the entire population as a way to increase dietary intake of the n-3 (omega-3) long-chain polyunsaturated fatty acids (LCPUFAs) that may prevent cardio-vascular disease and improve neuro-logical develop-ment (Kris-Etherton et al. 2002; Kris-Etherton and Innis 2007; Lee et al. 2009). Also, environmental groups have recommended that consumers avoid certain fish on the basis of concerns about species depletion or habitat destruction consequent to farming methods, site of origin, or type of harvesting (Monterey Bay Aquarium 2011). Whether, how much, and what type of fish a person eats are also influenced by economic and market considera-tions (e.g., cost and availability) as well as by taste, cultural tradition, recreational habits, and access to alternative foods.
Thus, the consumer who wants to know “which fish should I eat?” is likely to encounter contradictory advice, especially because much of the available information considers a single perspective, such as maximizing health or minimizing ecological harms. For example, because farm-raised salmon is high in n-3 fatty acids and very low in mercury, it is promoted for its nutritional benefits. However, environmental groups consider it a “fish to avoid” because salmon aqua-culture may adversely affect eco-system integrity and wild fish stocks (Monterey Bay Aquarium 2011), and relatively high levels of PCBs have led to concerns about cancer risk (Hites et al. 2004). Furthermore, it may be difficult for consumers to know whether any given fish is “good” to eat because they often do not have access to the facts they need to make fully informed choices, such as the size of the fish or how or where it was caught.
Recent articles as well as detailed scientific reports have simultaneously addressed both the nutritional and toxicological aspects of fish consumption [Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO) 2011; Mahaffey et al. 2011; Nesheim and Yaktine 2007; WHO/United Nations Environment Program 2008]. We have been unable to identify any review that addresses the full scope of relevant perspectives (toxicant, nutritional, ecological, and economic) and that has a primary focus on the complexity of balancing these four perspectives. The goal of this review was to extend the fish consumption discussion beyond the toxicant harm–nutritional benefit dichotomy that, although clearly of public health importance, neglects a number of critical issues regarding fish consumption, including the sustainability of fish as a food source. In doing so, we highlight areas of overlap and disagreement among the perspectives. Our broader perspective may complicate fish consumption choices but has the potential to benefit all points of view. For example, the economic viability of the fishing industry depends on the maintenance of adequate fishing stocks. Similarly, nutritional recom-mendations to increase fish consumption will be feasible only if sufficient fish supplies are available to meet greater demand.Methods
A group of collaborating authors with complementary expertise in environmental toxicology, nutritional epidemiology, aquatic ecology, economics, and public health practice together defined the outline and scope of this study. We then reviewed published literature as well as guidance disseminated by special interest and professional organizations. We also reviewed experience with previous advisories in the United States.
We primarily focused on issues relevant to purchasers/consumers of store-bought rather than self-caught fish. Because of regional variability in fish species consumed and their respective profiles, we chose to concentrate on consumption advice and guidelines from the United States, including the federal govern-ment as well as state, tribal, and local governments. However, because modern fish production is largely a multi--national industry, we took a more global perspective on the economic impact of fish. Similarly, fish contaminant toxicities or nutrient benefits are applicable to all populations, although we highlight areas where changes in fish intake might have different impacts, for example, among very low or very high consumers. Given the large scope of this article, we did not attempt a comprehensive review of each topic. Rather, we chose to highlight aspects of each perspective that are particularly likely to create confusion (such as the fact that both nutrients and toxicants in fish may influence the same body systems) or that have attracted the most public attention (such as the widely disseminated pocket cards focused on ecological sustainability) (Monterey Bay Aquarium 2011).Results
Perspectives on fish intake. Toxicant exposure and health risks. Dietary intake of fish and seafood is the dominant source of human exposure to MeHg, a toxicant that can have serious adverse effects on a number of body systems, especially the nervous and cardio-vascular systems. Mercury is a widespread contaminant found throughout the environ-ment [National Research Council (NRC) 2000]. MeHg, an organic form that is converted from inorganic mercury primarily by micro-organisms in the aquatic environment, is biomagnified in aquatic food webs, so the highest concentrations occur in large and long-lived predatory fish and marine mammals at the top trophic levels (NRC 2000).
Community-wide MeHg poisonings in Japan and Iraq highlighted the tragedy of high-dose MeHg exposure as well as the particular sensitivity of the developing fetus (Bakir et al. 1973; Harada 1995). Offspring who were exposed to MeHg in utero were born with serious neuro-logical damage, even if their exposed mothers were virtually unaffected (Harada 1995; Igata 1993). Subsequent epidemiological studies among island populations have found more subtle adverse effects of lower levels of MeHg exposure from habitual fish consumption during pregnancy, which have been extensively reviewed elsewhere (Clarkson and Magos 2006; NRC 2000).
Based on evidence for neuro-developmental toxicity from these birth cohort studies, the U.S. EPA recom-mended a MeHg reference dose (RfD) of 0.1 µg/kg body weight per day (NRC 2000). The RfD is an estimate of a daily oral exposure to the human population (including sensitive subgroups) that is likely to be without an appreciable risk of deleterious effects during a lifetime (Rice et al. 2003). The U.S. EPA also incorporated a 10-fold “uncertainty factor” to allow for differences in susceptibility, distribution, and elimination (Rice et al. 2003). However, recent studies in U.S. populations have found evidence for childhood neuro-develop-mental effects of pre-natal MeHg exposure even below the RfD, as reviewed by Karagas et al. (2012).
In addition to MeHg, many other pollutants can be found in fish, including PCBs and other persistent organic compounds, heavy metals, and “contaminants of emerging concern” such as pharmaceuticals and perfluorinated organic compounds. Many of these compounds have established health effects; for example, PCB exposure has been associated with neuro-development and cancer risk (Knerr and Schrenk 2006; Korrick and Sagiv 2008). However, in contrast to MeHg, fish is typically not the only route of exposure to these other contaminants. Furthermore, because contaminant content often varies regionally, advisories to limit exposure to other pollutants focus on the water source as well as the species of fish (U.S. EPA 2010).
Almost all fish are contaminated, to a greater or lesser degree, with environ-mental pollutants. Therefore, the more fish consumed, on average, the more likely an individual is to be exposed to MeHg and other environmental toxicants. Consumers who eat fish frequently or consume highly contaminated species may exceed exposure thresholds. Data from the National Health and Nutrition Examination Survey (NHANES) suggest that about 5–10% of U.S. women of child-bearing age have blood mercury levels consistent with intake exceeding the RfD (Mahaffey et al. 2004). Although debate is ongoing, older women and men may also be at risk; a somewhat less consistent litera-ture has suggested that MeHg exposure from fish consumption in adulthood may be associated with an increased risk of acute coronary events, cardio-vascular mortality, and neuro-logical symptoms (Karagas et al. 2012; Roman et al. 2011).
Nutrient benefits. Fish is high in protein and low in saturated fats and contains a number of other healthful nutrients such as vitamin D, selenium, and iodine. In particular, fish is the primary dietary source of n-3 LCPUFAs, including docosahexaenoic acid (DHA) and eicosa-pentaenoic acid. Because n-3 fatty acids are essential nutrients and because metabolism of the parent n-3 fatty acids to the more biologi-cally active long-chain versions is insufficient in some populations (Mahaffey et al. 2011), dietary intake from fish or from enriched foods and/or supplements is necessary to obtain adequate levels.
Much of the research examining the possible adverse health effects of suboptimal dietary n-3 LCPUFAs has focused on either develop-mental outcomes associated with peri-natal exposure or cardio-vascular risks among older adults. Other outcomes have been also associated with n-3 LCPUFAs (McManus et al. 2009), but in this study we focused on these two end points because of their parallel susceptibility to both nutrient intake and MeHg exposure.
DHA is a necessary structural component of the brain and eye, and the pre- and post-natal periods are likely a critical period for incorporation into these neural tissues (Innis 2000). These anatomic observations have been supported by findings from animal and some human studies (Anderson GJ et al. 2005; Anderson JW et al. 1999; Brion et al. 2011; Innis 2000; Kramer et al. 2008). However, meta-analyses of randomized trials have not found evidence of persistent bene-ficial effects of LCPUFA supplementation of formula milk on the physical, visual, and neuro-develop-mental outcomes of term or pre-term infants (Simmer et al. 2008a, 2008b). Limited evidence from randomized trials of fish oil supplements in pregnancy supports a cognitive bene-fit for offspring (Dunstan et al. 2008), although other trials found no bene-ficial effects (Helland et al. 2008; Makrides et al. 2010).
Cohort studies in the Faroe Islands, Seychelle Islands, and New Zealand focused on associations between pre-natal mercury levels and child develop-ment (NRC 2000). More recent cohort studies that have examined the relation-ship of pre-natal fish consumption with these outcomes have been generally consistent in showing either no adverse effects or improved neuro-develop-ment among children whose mothers ate more fish in pregnancy (Budtz-Jørgensen et al. 2007; Gale et al. 2008; Hibbeln et al. 2007; Lederman et al. 2008; Oken et al. 2005, 2008a, 2008b). Thus, available data suggest that maternal intake of fish and perhaps, although less convincingly, n-3 LCPUFA supplements has modest beneficial effects on neuro-develop-mental and cognitive outcomes of offspring. However, the conclusions that can be based upon these data are limited by a number of factors, including the potential for other neuro--protective nutrients in seafood (e.g., selenium and iodine) to be relevant, and the extent to which confounding (e.g., seafood intake as a marker of healthy lifestyle) explains observed results.
A larger and more consistent body of evidence supports a beneficial role of n-3 LCPUFAs in preventing cardio-vascular disease. Observational studies have found that higher habitual fish intake and higher blood levels of n-3 LCPUFAs are associated with lower risks for congestive heart failure, myocardial infarction, sudden cardiac death, and stroke, as reviewed by Mozaffarian and Rimm (2006).
Although empirical evidence is lacking for the optimal amount of daily n-3 LCPUFAs intake, consensus guidelines recommend DHA intake of about 100–300 mg/day in pregnancy (Akabas and Deckelbaum 2006; Koletzko et al. 2007) and 250–1,800 mg/day for primary prevention of cardio-vascular disease (Kris-Etherton et al. 2002; Mozaffarian and Rimm 2006). Most people consume much less; for example, among U.S. adults in the 1999–2002 NHANES, mean combined intake of DHA plus eicosa-pentaenoic acid was 103 mg/day (Nesheim and Yaktine 2007). Nutritionists and these consensus guidelines have encouraged people to increase their intake of fish to achieve recommended n-3 LCPUFA intake. However, different fish types provide very different amounts of n-3 LCPUFAs. For example, weekly consumption of 6 ounces of shrimp, pollock, or salmon provides an average of 35, 100, and 350 mg/day DHA, respectively (U.S. Department of Agriculture 2009).
Integration of health risks and benefits of fish consumption. Confusion regarding which fish are healthful to eat likely resulted from the fact that early studies assessing the health risk of toxicants found in fish (e.g., MeHg, PCBs) did not incorporate the potential health bene-fits of co-occurring nutrients, and vice versa. Several analyses have attempted to calculate the net health effects of different fish types using estimates of both toxi-cant and nutrient influences (Burger and Gochfeld 2005; Cohen et al. 2005; Ginsberg and Toal 2000; Mahaffey et al. 2011; Stern 2007; Stern and Korn 2011; Tsuchiya et al. 2008). Additionally, a few recent studies, including cohorts focused on child neuro-development (Lynch et al. 2010; Oken et al. 2008b) and adult cardio-vascular disease (Mozaffarian et al. 2011), estimated intake or measured levels of both MeHg and n-3 LCPUFAs.
These analyses will contribute to a clearer picture of the interactions of MeHg and n-3 LCPUFAs on health outcomes, which will allow for guidance to the public that minimizes apparently confusing and conflicting messages about the health effects of fish consumption. However, ecological and economic perspectives, which are generally not considered in analyses weighing possible harms and benefits for health, may result in fish consumption advice or choices antagonistic to recommendations based solely upon human health.
Ecological concerns. Although fish consumption may directly influence human health, human influences, including the harvesting of wild or farmed fish, can profoundly affect the health of the oceans. The rapid decline in large migratory fish species such as tuna, swordfish, and shark has been well documented (Baum et al. 2005; Myers and Worm 2005; Pauly et al. 2002; Worm et al. 2009). Abundance of wild fish stocks is expected to decline further in the future with the added stress imposed by climate variability and habitat alteration, particularly for heavily over-fished stocks that are more sensitive to climate variability (Worm and Myers 2004).
Globally, the volume of fish production has increased 8-fold since 1950, from about 15 to 120 million tons/year (Figure 1) (FAO 2010b). In part because opportunities for additional harvests of wild fish stocks are limited (i.e., additional harvest could result in species collapse from over-fishing), aqua-culture has grown at a rate of 7–9% per year in the past decade, making it the fastest growing food production industry in the world (FAO 2008). Presently, farmed fish account for 23% of the fish consumed (FAO 2010b). Only one-third of total aqua-culture production is used directly for human consumption, with the remainder used for meal in other farming operations (Rice and Garcia 2011).Figure 1. Click for Larger Image.
World fish use and supply from 1950 to 2008. Reproduced from FAO (2010b) with permission from the Food and Agriculture Organization of the United Nations.
Pauly et al. (2002) estimated that global fishing efforts exceeded the maximum sustainable yield by a factor of 3–4. Future needs will likely be even more over-whelming. An estimated 50% increase in fish production is needed by 2050 to meet the basic protein requirements of a growing human population and ensure global food security (Rice and Garcia 2011). If people try not only to meet their protein needs but also to ingest the recom-mended amount of n-3 LCPUFAs from fish, an even greater increase in fish consumption would result.
Creative solutions are needed to resolve the predicament of increasing human demand for fish protein and nutrients amid growing concerns about the global viability of wild fish stocks. Aquaculture has received negative attention because of concerns about the escape of exotic or genetically modified farmed fish species, infection of wild fish stocks with parasites that thrive in farming operations, trophic inefficiencies, enhancement of fish contaminant content, and farm-induced organic enrichment of coastal eco-systems that disrupts their natural functioning (Carniero 2011; Greenberg 2010; Hargrave et al. 1997; Hites et al. 2004; Vanhonacker et al. 2011). However, fish-farming operations can be improved with proper situation of cage sites in estuaries with the appropriate physical conditions (flushing rates and oxygen status) and a focus on lower-trophic-level species such as catfish and tilapia to maximize productivity (Rice and Garcia 2011). Because markets, trade, and consumption patterns strongly influence the activities of the aquaculture community, consumer awareness and demand for sustainable farming practices and quality products can help shape this industry in the future (Khan 2010; Subasinghe et al. 2009).
Economic perspectives on fish consumption. Fisheries are big business on a national and global scale. Indeed, this industry, as well as related industries such as restaurants and grocery purveyors, are key determinants of the amount, type, and form of fish that people consume by affecting the cost, availability, and desirability of different fish.
The United States is one of the world’s largest exporters of seafood products and the world’s second largest seafood importer (Brooks et al. 2009). Over the past half-century, total global production of seafood products has continued to increase, reaching 142 million tons in 2008; the total value of global aquaculture production was estimated at $98.4 billion in 2008 (FAO 2010a). It is obvious from these figures that fish consumption choices have a broad economic impact on the fishing industry, and therefore it is not surprising that this industry seeks to influence the public debate surrounding the harms and benefits of fish intake.
One example of this type of industy influence is canned tuna, a longtime staple in the American diet and the second most commonly consumed type of seafood in the United States; it is also the top dietary contributor to MeHg intake (Groth 2010). There has been an on-going debate regarding whether canned albacore tuna should be listed as a high-mercury fish. The U.S. Food and Drug Administration (FDA) did not include tuna among the high-mercury fish named in its 2001 mercury advisory. Subsequently, a non-profit organization filed a Freedom of Information Act request to access the documents related to the advisory (Nestle 2006). These documents revealed that the FDA had planned to list albacore tuna among the high-mercury fish but dropped the warning after meeting with representatives of the fishing industry. This example illustrates how the interests guiding a fish advisory are not necessarily limited to public health concerns. In fact, the FDA’s regulatory mission is to balance consumers’ health risks against industry interests, such as maintaining demand for popular fish. These issues are not unique to the United States. Although the bluefin tuna used in sushi is high in mercury and ecologically fragile, a recently proposed international ban on bluefin fishing failed after it was vetoed by a number of countries, including Libya, Cyprus, Malta, Spain, France, and Italy, all of which border the Mediterranean and have a stake in the trade of this highly profitable fish (Abend 2010).
As another example, Chilean sea bass has emerged as one of the most popular and profitable fish in U.S. restaurants (Cascorbi 2006). This fish was formerly inaccessible because of its habitat deep in the seas surrounding the Antarctic shelf, as well as being somewhat unappealing when labeled with its official name, the Patagonian toothfish. The rapid expansion of the toothfish fishery in the early 1990s has been linked to the introduction of new fishing techniques as well as aggressive marketing, especially by restaurants, where > 40% of sales occur (Cascorbi 2006). U.S. imports of toothfish, which account for almost half of the worldwide catch, doubled in quantity and tripled in value from 1998 to 2003, from $10 million to > $30 million (Cascorbi 2006). This expansion occurred despite the fact that toothfish are high in mercury (Environmental Defense Fund 2008), vulnerable to overfishing, and caught with methods that result in substantial damage to the seafloor and bycatch of marine birds (Cascorbi 2006).
Fish consumption advisories and advice. U.S. Federal governmental fish consumption advisories and their effects. After an NRC review of the health effects of MeHg (NRC 2000), federal and state agencies established fish consumption guidelines based on species-specific mercury levels. In January 2001, the FDA disseminated a consumer advisory on mercury in fish directed at groups considered to be at highest risk: women who might become pregnant, women who are pregnant, nursing mothers, and young children (FDA 2001). The advisory recommended avoiding the four most contaminated fish species (shark, swordfish, king mackerel, and tilefish) and limiting overall consumption of fish and shellfish to ≤ 12 ounces/week (FDA 2001). In 2004, the FDA and the U.S. EPA jointly published a revised advisory that emphasized the nutritional benefits of fish, added a suggested restriction in consumption of canned white (albacore) tuna, and included examples of specific species that are low in MeHg (U.S. EPA 2004). These changes were welcome because many consumers may have been more aware of the content and effect of harmful substances in fish than of the nutrients (Bloomingdale et al. 2010; Verbeke et al. 2005).
Several investigators have taken advantage of existing data sets to estimate effects of the U.S. federal government mercury advisories on fish consumption. In a cohort study of well-educated pregnant women in Massachusetts that straddled dissemination of the FDA advisory (FDA 2001), women reported consuming less dark meat fish, canned tuna, and white meat fish after publication of the advisory (Oken et al. 2003). Using a panel of nearly 15,000 U.S. households, Shimshack and Ward (2010) studied fish purchases from 2000 through 2002, finding that households with pregnant women or young children reduced both their mercury and n-3 LCPUFA intakes after the 2001 advisory. The n-3 LCPUFA decline occurred everywhere along the distribution of intakes, including among those with the lowest intake. Results were driven by a broad-based decline in consumption of all fish. On average, consumers, even those with a college education, did not differentially avoid high-mercury fish, nor did they substitute away from high-mercury species into low-mercury, high-omega-3 species. However, less educated households showed no advisory-induced reduction in mercury (Shimshack and Ward 2010).
In contrast, NHANES data indicated that blood mercury decreased from 1999 through 2004, without a concomitant decrease in fish consumption (Mahaffey et al. 2009). Although the cause for this decrease remains unclear, the authors speculated that the findings suggested a more discerning series of choices in type of fish eaten rather than an overall reduction in fish consumption (Mahaffey et al. 2009)
Most recently, an analysis using pooled nationally representative 2001 and 2006 food safety surveys indicated an increase in U.S. consumers’ awareness of mercury as a problem in fish (69% in 2001 to 80% in 2006), especially among parents of young children (Lando and Zhang 2011). However, women of child-bearing age were less aware and knowledgeable about this information than other women.
U.S. local government fish consumption advisories and their effects. Individual U.S. states and tribes collect data and issue advisories on mercury in fish caught from local bodies of water. Some states and localities provide advice for commercial fish consumption as well (U.S. EPA 2010). Their recommendations may include information on species that are of particular relevance to the local population but not necessarily included in nation-wide U.S. advisories. Advisories differ from state to state based on a number of variables. For example, most advisories target children, pregnant women, and women of child-bearing age, and a few states also provide advice for the general population (Scherer et al. 2008). Although most advisories are based on the U.S. EPA’s RfD for MeHg established in 2000 (NRC 2000), a few are based on the FDA action level established in 1979, which is approximately four times higher (Tollefson and Cordle 1986). A few states (e.g., Alaska) have derived their own health assessments and used these in formulating advice.
Approximately 80% of U.S. fishing advisories are, at least in part, related to mercury contamination. The most recent data indicated that across all 50 states, as of 2010, there were ≥ 4,500 fish consumption advisories (i.e., advice to limit or avoid consuming fish from a given water body because of contaminant risk) (U.S. EPA 2010). These advisories cover 4 of every 10 river miles, almost 79% of contiguous coastal waters, and 40% of all fresh-water surface area in the United States, not including the Great Lakes, 100% of which are under advisories. In contrast, in 2010 only 2% of the nation’s river miles and 9% of the nation’s lake acres had safe-eating guidelines in effect (i.e., an indication that fish from the body of water was safe for consumption) (U.S. EPA 2010).
Awareness of regional fish consumption advisories in the United States is generally low, ranging from 8% to 32% (Anderson et al. 2004; Gliori et al. 2006; Knobeloch et al. 2005). Furthermore, results from several surveys suggest that awareness of regional fish advisories is not more common among higher-risk sub-groups, such as pregnant women, nor does awareness necessarily predict lower mercury levels or less frequent consumption of higher-mercury fish (Burger and Gochfeld 2009; Karouna-Renier et al. 2008; Knobeloch et al. 2005; Silver et al. 2007). Challenges to communicating effectively with high-risk groups have included language barriers, educational and literacy status, income level, cultural differences, and difficulty reaching racial/ethnic minority groups (Imm et al. 2007; Kuntz et al. 2009; Silver et al. 2007). In addition to these challenges, many consumers simply do not want any more information. For example, although most surveyed fishers in the New York Bight did not have accurate knowledge on harms and benefits of fish consumption, well over one-third of them did not feel they needed more information (Burger and Gochfeld 2009).
Other resources. In addition to advice issued by the U.S. federal government and states, not-for-profit and other non-govern-mental organizations also provide information on mercury in fish directly to consumers. In Table 1, we summarize a number of fish consumption recommendations for U.S. populations, by target audience and messages that are conveyed. For example, the Natural Resources Defense Council and the Turtle Island Restoration Network provide online mercury calculators that allow consumers to calculate whether their mercury intake exceeds the U.S. EPA RfD, based on their body weight and combinations and amounts of fish species consumed. In Table 2 we list several web sites that link to valuable sources of information for the public regarding fish consumption. Other groups, such as Physicians for Social Responsibility (2004) and the Environmental Working Group (2012), provide lists of fish species with higher and lower mercury concentrations, along with consumption guidelines.
Summary of major seafood consumption guidelines or advisories targeted at North American populations.
Table 2. Click for Larger Image.
Selected web sites with links to seafood guides.
Other guides incorporate information advocating ocean conservation and warning of the environmental hazards associated with certain types of seafood consumption. Popular guides such as the Monterey Bay Aquarium Seafood Watch (Monterey Bay Aquarium 2011) combine information about the sustainability of fisheries and catch methods with information on contaminant burdens and nutrients in different species.
Challenges for fish consumption choice. Considerable uncertainty exists regarding the actual toxicological, nutritional, ecological, and/or environmental harms and benefits of consuming any given fish. Among the hundreds of species of fish available for consumption, characteristics are highly variable. Even within species, nutritional, contaminant, and ecological attributes can vary widely depending on the size or variant or where the fish is harvested or farmed. For example, shrimp can be rated as an ecological “best choice,” “good alternative,” or “avoid” depending on its origin (Monterey Bay Aquarium 2011). Similarly, tilefish caught in the Gulf of Mexico is very high in MeHg, whereas tilefish from the Atlantic Ocean is low in MeHg (Sunderland 2007).
Furthermore, there is variation in susceptibility to the benefits or harms of fish consump-tion among individuals by age and other characteristics. Also, the net health effect of a change in intake for each individual (or popu-la-tion) depends on baseline intake: If intake is low, the net harm of a further reduction is likely to be greater than if intake is high (Hammitt 2004).
Incomplete information may result in expert advice that is incorrect or mis-leading. For example, most U.S. commercial fish consumption advisories to limit MeHg exposure are based on mean or median mercury concentrations measured in fish samples collected by the FDA. However, these reference data may be based on a small number of fish and are often not up-to-date, and mercury concentrations may vary widely even within the same species. For example, some samples of high-mercury species such as swordfish may have non-detectable levels of mercury, whereas lower-risk species such as halibut may have levels > 1 ppm (FDA 2011). In a recent study of different eco-labels for farmed fish, Volpe et al. (2011) found no evidence that these certified products are actually environmentally preferable, in part because many of the standards applied in the different labels ignored major environmental impacts.
Once advice is issued, consumers may not respond in ways that result in better outcomes. Economic wisdom holds that improved information enhances welfare because consumers refine and adapt their consumption in response to new information. However, it is not clear whether welfare actually increased after the FDA’s seafood consumption advisories (Blanchemanche et al. 2010; Shimshack and Ward 2010). First, rather than substituting higher-mercury fish for lower-mercury fish to reduce exposure while still obtaining benefits provided from fish, many consumers simply reduced their over-all fish intake, which also resulted in a decreased intake of nutrients obtained from fish. Second, although the FDA’s advice targeted pregnant and breast-feeding women, even non-targeted adults reduced their fish consumption (Shimshack and Ward 2010; Shimshack et al. 2007). These consumers may have incurred a welfare loss because their reduction in fish intake led to a reduced intake of n-3 LCPUFAs and therefore increased cardio-vascular risk (Mozaffarian and Rimm 2006), possibly out-weighing the gains from decreased fish intake (e.g., from decreased MeHg exposure).
Why would people make choices that may actually worsen, rather than improve, their health? Balancing risks is notoriously difficult. When individuals make judgments under uncertainty, they tend to use a limited number of cognitive processes. These processes are efficient but can sometimes lead to errors or biases (Kahneman 2003). People often over-estimate some risks (e.g., the risk of harm from MeHg exposure), whereas they under-estimate others (e.g., the risk of harm from sub-optimal nutrition) (Slovic et al. 2000). They tend to focus on worst-case scenarios (Viscusi 1997). Many consumers are better aware of the content and effects of harmful substances than of nutrients in fish (Verbeke et al. 2005).
Given these uncertainties, consumers are likely to employ a bounded rationality approach to make consumption choices (McFadden 2001). That is, they recognize that the gathering and processing of information comes at a cost in terms of time and cognitive burden. Instead of striving for more information to update their beliefs about the relevant health risks, they eventually adopt simpler heuristics to make consumption choices (Gigerenzer and Goldstein 1996). The fact that consumers not targeted by the FDA’s 2001 mercury advisory (FDA 2001) reduced their fish consumption (even of fish lower in mercury) simply to rule out a food risk is consistent with the bounded rationality assumption.
Messages that are simple or that are targeted at well-known fish species are more likely to be effective (Verger et al. 2007). In focus groups, participants preferred simple messages; however, they did not always respond appropriately (Nesheim and Yaktine 2007). For example, almost all participants reported that they would avoid species desig-nated “do not eat” regardless of whether they were in the targeted audience. Also, responses vary depending on whether “risks” or “bene-fits” are listed first (Knuth et al. 2003; Verbeke et al. 2008).Discussion
The possible combinations of matters related to fish consumption—including toxico-logi-cal, nutritional, ecological, and economic—are many, but few, if any, fish consumption patterns optimize all four of these areas. In Table 3 we summarize these viewpoints and the challenges they present to comprehensive advice.
Challenges to developing comprehensive fish consumption advice.
Individual and market economics can influence seafood consumption decisions in ways that may be largely independent of specific toxicant hazards, nutrient benefits, or eco-system effects. In addition, availability, taste preferences, cultural traditions, and cost affect consumers’ fish intake (Verbeke and Vackier 2005). Ecological and economic impacts of fish choice are perhaps the least “visible” to consumers and therefore the most difficult to incorporate into decision making (Verbeke et al. 2007). Furthermore, when consumers choose not to eat fish, regardless of the reason, the foods eaten instead (e.g., red meat) also may have variable health, ecological, and economic impacts.
The future of fish advisories is a matter of ongoing debate and presents a number of alternative options. Agencies may recommend that populations of highest concern refrain from eating fish with high concentrations of MeHg, similar to the FDA advisory (FDA 2001) and many state advisories. But past experience has shown that this approach excludes many “low-risk” populations that may in fact suffer harm from MeHg toxicity, and also is likely to reduce fish intake indiscriminately, worsening nutrition. An alternative approach is to suggest that people should eat fish, without parsing out the contaminant or ecological harms of different fish types. For example, the 2010 Dietary Guidelines for Americans (USDA 2010) encourage everyone, including pregnant and breast-feeding women, to eat seafood at least twice a week. However, this advice might expose a subset of the population to risk of substantial harm from increased MeHg intake and is likely unsustainable given the projected inadequacy of fish stocks to support population growth, even at current consumption levels.
More comprehensive advice that describes both the potential hazards and benefits of fish consumption can be developed. However, such an approach is constrained by a relative lack of information integrating not only health risks and benefits but also ecological and economic impacts. Furthermore, experience to date suggests that effective communication of multiple competing risks is difficult at best and, at worst, may encumber consumers with irreconcilable risk–risk trade-offs. Additionally, although consumer demand for healthful, sustainably harvested or farmed fish can help shape fishing industry practices, it is unlikely that consumers alone can substantially influence these practices. Policy and fishery management inter-ventions will be necessary to ensure long-term availability of fish as an important source of human nutrition.Conclusion
On an individual level, decisions regarding which fish to eat—and whether to change fish consumption habits—may vary widely across consumers. We have not yet met the challenge of providing consumers with accessible information that includes nutritional, contaminant, ecological, and economic trade-offs associated with fish consumption choices, including guidance to consumers who vary by baseline intake, life stage, and reliance on fish intake because of subsistence needs or cultural traditions.
Based on evidence we present here, fish consumption advice addressed to the general public should be clear and simple to have an impact. We suggest developing a list of fish to eat, and those to minimize or avoid, that considers these multiple perspectives and not solely the health effects of contaminants and nutrients. This list should include links to more detailed resources that can be used by those wanting more information about individual fish types or wishing to optimize one or more parameters. The simple message needs to be provided on a national level but with the cooperation of local and regional partners (e.g., states and non-governmental organizations). Thus, adjustments could be made on a regional level if necessary, as long as the framework can be followed. As further information becomes available, the list of beneficial choices, as well as choices to avoid, could be improved upon. Although simplicity of messaging is paramount, the under-lying paradigm addressing the challenges presented in Table 3 would not be simple. Yet with transparency, an approach on a national level could be developed that provides clear choices protecting public and global health.
Meanwhile, we should continue to urge international organizations, governments, and agencies to promote remediation and, where possible, elimination of sources of fish contamination and to establish policies that promote environmentally responsible and economically viable fishing practices so fish can remain a part of a healthy human diet for future generations.References
- Abend L.. 2010. Why a Proposed Ban on Bluefin Tuna Fishing Failed. Time 18(March). Available: http://www.time.com/time/health/article/0,8599,1973374,00.html [accessed 14 November 2011]
- Akabas SR, Deckelbaum RJ. 2006. Summary of a workshop on n-3 fatty acids: current status of recommendations and future directions. Am J Clin Nutr 83(6): suppl1536S–1538S. Find this article online
- Anderson GJ, Neuringer M, Lin DS, Connor WE. 2005. Can pre-natal n-3 fatty acid deficiency be completely reversed after birth? Effects on retinal and brain biochemistry and visual function in rhesus monkeys. Pediatr Res 58(5):865–872. Find this article online
- Anderson HA, Hanrahan LP, Smith A, Draheim L, Kanarek M, Olsen J. 2004. The role of sport-fish consumption advisories in mercury risk communication: a 1998–1999 12-state survey of women age 18–45. Environ Res 95(3):315–324. Find this article online
- Anderson JW, Johnstone BM, Remley DT. 1999. Breast-feeding and cognitive development: a meta-analysis. Am J Clin Nutr 70(4):525–535. Find this article online
- Bakir F, Damluji SF, Amin-Zaki L, Murtadha M, Khalidi A, al-Rawi NY, et al. 1973. Methylmercury poisoning in Iraq. Science 181(96):230–241. Find this article online
- Baum JK, Kehler D, Meyers RA. 2005. Robust estimates of decline for pelagic shark populations in the Northwest Atlantic and Gulf of Mexico. Fisheries 30(10):27–29.). Find this article online
- Blanchemanche S, Marette S, Foosen J, Verger P.. 2010. “Do not eat fish more than twice a week.” Rational choice regulation and risk communication: uncertainty transfer from risk assessment to public. Health Risk Society 12(3):271–292. Find this article online
- Bloomingdale A, Guthrie LB, Price S, Wright RO, Platek D, Haines J, et al. 2010. A qualitative study of fish consumption during pregnancy. Am J Clin Nutr 92(5):1234–1240. Find this article online
- Blue Ocean Institute 2012. Seafood Guide. Available: http://www.blueocean.org/seafood/seafood-guide [accessed 17 April 2012]
- Brion MJ, Lawlor DA, Matijasevich A, Horta B, Anselmi L, Araujo CL, et al. 2011. What are the causal effects of breastfeeding on IQ, obesity and blood pressure? Evidence from comparing high-income with middle-income cohorts. Int J Epidemiol 40(3):670–680. Find this article online
- Brooks N, Regmi A, Jerardo A 2009. U.S. Food Import Patterns, 1998–2007. Available: http://www.ers.usda.gov/publications/fau/2009/08aug/fau125/fau125.pdf [accessed 14 November 2011]
- Budtz-Jørgensen E, Grandjean P, Weihe P.. 2007. Separation of risks and benefits of seafood intake. Environ Health Perspect 115:323–327. Find this article online
- Burger J, Gochfeld M.. 2005. Heavy metals in commercial fish in New Jersey. Environ Res 99(3):403–412. Find this article online
- Burger J, Gochfeld M.. 2009. Perceptions of the risks and bene-fits of fish consumption: individual choices to reduce risk and increase health benefits. Environ Res 109(3):343–349. Find this article online
- Carniero G.. 2011. Marine management for human development: a review of two decades of scholarly evidence. Marine Policy 35:351–362. Find this article online
- Cascorbi A 2006. Chilean Sea Bass, Final Report. Available: http://www.montereybayaquarium.org/cr/cr_seafoodwatch/content/media/MBA_SeafoodWatch_ChileanSeabassReport.pdf [accessed 15 December 2011]
- Clarkson TW, Magos L. 2006. The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36(8):609–662. Find this article online
- Cohen JT, Bellinger DC, Connor WE, Kris-Etherton PM, Lawrence RS, Savitz DA, et al. 2005. A quantitative risk-benefit analysis of changes in population fish consumption. Am J Prev Med 29(4):325–334. Find this article online
- Dunstan JA, Simmer K, Dixon G, Prescott SL. 2008. Cognitive assessment of children at age 2½ years after maternal fish oil supplementation in pregnancy: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed 93(1):F45–F50. Find this article online
- Environmental Defense Fund 2008. Seafood Selector. Available: http://apps.edf.org/page.cfm?tagID=1521 [accessed 14 November 2011]
- Environmental Working Group 2012. EWG’s Fish List. Available: http://www.ewg.org/safefishlist [accessed 17 April 2012]
- FAO (Food and Agriculture Organization of the United Nations) 2008. Report of the FAO Expert Workshop on Climate Change Implications for Fisheries and Aquaculture. FAO Fisheries Report No. 870. Available: http://www.fao.org/docrep/011/i0203e/i0203e00.htm [accessed 16 April 2012]
- FAO (Food and Agriculture Organization of the United Nations) 2010a. Fishery and Aquaculture Statistics 2008. Rome:FAO. Available: http://www.fao.org/docrep/013/i1890t/i1890t.pdf [accessed 16 April 2012]
- FAO (Food and Agriculture Organization of the United Nations) 2010b. The State of World Fisheries and Aquaculture. Rome:FAO. Available: http://www.fao.org/docrep/013/i1820e/i1820e.pdf [accessed 16 April 2012]
- FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) 2011. Joint FAO/WHO Expert Consultation on the Risks and Benefits of Fish Consumption. Fisheries and Aquaculture Report No. 978. Available: http://www.fao.org/docrep/014/ba0136e/ba0136e00.pdf [accessed 23 November 2011]
- FDA (Food and Drug Administration) 2001. Consumer Advisory: An Important Message for Pregnant Women and Women of Childbearing Age Who May Become Pregnant about the Risks of Mercury in Fish. Available: http://www.fda.gov/OHRMS/DOCKETS/ac/02/briefing/3872_Advisory%203.pdf [accessed 14 April 2012]
- FDA (Food and Drug Administration) 2011. Mercury Levels in Commercial Fish and Shellfish. Available: http://www.fda.gov/Food/FoodSafety/Produ ct-SpecificInformation/Seafood/Foodborne PathogensContaminants/Methylmercury/ucm115644.htm [accessed 14 November 2011]
- FDA (Food and Drug Administration) and U.S. EPA (U.S. Environmental Protection Agency) 2004. What You Need to Know about Mercury in Fish and Shellfish. Available: http://www.fda.gov/downloads/Food/ResourcesForYou/Consumers/UCM182158.pdf [accessed 17 April 2012]
- Fish4Health.net 2009. Fish4Health.net Homepage. Available: http://fn.cfs.purdue.edu/fish4health [accessed 17 April 2012]
- Fishwise 2012. Purchasing Tools. Available: http://www.fishwise.org/science/purchasing-tools/ [accessed 17 April 2012]
- Food and Water Watch 2011. National Smart Seafood Guide 2011. Available: http://www.foodandwaterwatch.org/fish/seafood/guide [accessed 17 April 2012]
- Gale CR, Robinson SM, Godfrey KM, Law CM, Schlotz W, O’Callaghan FJ. 2008. Oily fish intake during pregnancy—association with lower hyperactivity but not with higher full-scale IQ in offspring. J Child Psychol Psychiatry 49(10):1061–1068. Find this article online
- Gigerenzer G, Goldstein DG. 1996. Reasoning the fast and frugal way: models of bounded rationality. Psychol Rev 103(4):650–669. Find this article online
- Ginsberg GL, Toal BF. 2000. Development of a single-meal fish consumption advisory for methyl mercury. Risk Anal 20(1):41–47. Find this article online
- Gliori G, Imm P, Anderson HA, Knobeloch L. 2006. Fish consumption and advisory awareness among expectant women. WMJ 105(2):41–44. Find this article online
- Greenberg P 2010. Four Fish: The Future of the Last Wild Food. New York:Penguin Books.:
- Greenpeace International 2012. Seafood. Available: http://www.greenpeace.org/international/seafood/ [accessed 17 April 2012]
- Groth E III. 2010. Ranking the contributions of commercial fish and shellfish varieties to mercury exposure in the United States: implications for risk communication. Environ Res 110(3):226–236. Find this article online
- Hammitt JK. 2004. Economic implications of hormesis. Hum Exp Toxicol 23(6):267–278. Find this article online
- Harada M.. 1995. Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol 25(1):1–24. Find this article online
- Hargrave BT, Phillips GA, Doucette LI, White MJ, Wildish DJ, Cranston RE. 1997. Assessing benthic impacts of organic enrichment from marine aquaculture. Water Air Soil Pollut 99(1–4):641–650. Find this article online
- Health Canada 2007. Human Health Risk Assessment of Mercury in Fish and Health Benefits of Fish Consumption. Available: http://www.hc-sc.gc.ca/fn-an/pubs/mercur/merc_fish_poisson-eng.php [accessed 17 April 2012]
- Helland IB, Smith L, Blomen B, Saarem K, Saugstad OD, Drevon CA. 2008. Effect of supplementing pregnant and lactating mothers with n-3 very-long-chain fatty acids on children’s IQ and body mass index at 7 years of age. Pediatrics 122(2):e472–e479. Find this article online
- Hibbeln JR, Davis JM, Steer C, Emmett P, Rogers I, Williams C, et al. 2007. Maternal seafood consumption in pregnancy and neuro-developmental outcomes in childhood (ALSPAC study): an observational cohort study. Lancet 369(9561):578–585. Find this article online
- Hites RA, Foran JA, Schwager SJ, Knuth BA, Hamilton MC, Carpenter DO. 2004. Global assessment of polybrominated diphenyl ethers in farmed and wild salmon. Environ Sci Technol 38(19):4945–4949. Find this article online
- Igata A.. 1993. Epidemiological and clinical features of Minamata disease. Environ Res 63(1):157–169. Find this article online
- Imm P, Knobeloch L, Anderson HA. 2007. Maternal recall of children’s consumption of commercial and sport-caught fish: findings from a multi-state study. Environ Res 103(2):198–204. Find this article online
- Innis SM. 2000. Essential fatty acids in infant nutrition: lessons and limitations from animal studies in relation to studies on infant fatty acid requirements. Am J Clin Nutr 71(1): suppl238S–244S. Find this article online
- Institute of Medicine 2006. Seafood Choices: Balancing Benefits and Risks. Available: http://www.iom.edu/Reports/2006/Seafood-Choices-Balancing-Benefits-and-Risks.aspx [accessed 17 April 2012].
- Kahneman D.. 2003. Maps of bounded rationality: psychology for behavioral economics. Am Econ Rev 93:1449–1475. Find this article online
- Karagas MR, Choi AL, Oken E, Horvat M, Schoeny R, Kamai E, et al. 2012. Evidence on the human health effects of low-level methylmercury exposure. Environ Health Perspect 120:799–806. Find this article online
- Karouna-Renier NK, Rao KR, Lanza JJ, Rivers SD, Wilson PA, Hodges DK, et al. 2008. Mercury levels and fish consumption practices in women of child-bearing age in the Florida Panhandle. Environ Res 108(3):320–326. Find this article online
- Khan AS. 2010. The rebuilding imperative in fisheries: clumsy solutions for a wicked problem? Progr Oceanogr 87:641–650. Find this article online
- Kidsafe 2012. Kidsafe Seafood. Available: http://www.kidsafeseafood.org/ [accessed 17 April 2012]
- Knerr S, Schrenk D.. 2006. Carcinogenicity of “non-dioxinlike” polychlorinated biphenyls. Crit Rev Toxicol 36(9):663–694. Find this article online
- Knobeloch L, Anderson HA, Imm P, Peters D, Smith A. 2005. Fish consumption, advisory awareness, and hair mercury levels among women of childbearing age. Environ Res 97(2):220–227. Find this article online
- Knuth BA, Connelly NA, Sheeshka J, Patterson J. 2003. Weighing health benefit and health risk information when consuming sport-caught fish. Risk Anal 23(6):1185–1197. Find this article online
- Koletzko B, Cetin I, Brenna JT. 2007. Dietary fat intakes for pregnant and lactating women. Br J Nutr 98(5):873–877. Find this article online
- Korrick SA, Sagiv SK. 2008. Polychlorinated biphenyls, organochlorine pesticides and neuro-development. Curr Opin Pediatr 20(2):198–204. Find this article online
- Kramer MS, Aboud F, Mironova E, Vanilovich I, Platt RW, Matush L, et al. 2008. Breastfeeding and child cognitive development: new evidence from a large randomized trial. Arch Gen Psychiatry 65(5):578–584. Find this article online
- Kris-Etherton PM, Harris WS, Appel LJ. 2002. Fish consumption, fish oil, omega-3 fatty acids, and cardio-vascular disease. Circulation 106:2747–2757. Find this article online
- Kris-Etherton PM, Innis S. 2007. Position of the American Dietetic Association and Dietitians of Canada: dietary fatty acids. J Am Diet Assoc 107(9):1599–1611. Find this article online
- Kuntz SW, Hill WG, Linkenbach JW, Lande G, Larsson L. 2009. Methylmercury risk and awareness among American Indian women of childbearing age living on an inland northwest reservation. Environ Res 109(6):753–759. Find this article online
- Lando AM, Zhang Y. 2011. Awareness and knowledge of methyl-mercury in fish in the United States. Environ Res 111(3):442–450. Find this article online
- Lederman SA, Jones RL, Caldwell KL, Rauh V, Sheets SE, Tang D, et al. 2008. Relation between cord blood mercury levels and early child development in a World Trade Center cohort. Environ Health Perspect 116:1085–1091. Find this article online
- Lee JH, O’Keefe JH, Lavie CJ, Harris WS. 2009. Omega-3 fatty acids: cardio-vascular benefits, sources and sustainability. Nat Rev Cardiol 6(12):753–758. Find this article online
- Lynch ML, Huang LS, Cox C, Strain JJ, Myers GJ, Bonham MP, et al. 2010. Varying coefficient function models to explore interactions between maternal nutritional status and pre-natal methylmercury toxicity in the Seychelles Child Development Nutrition Study. Environ Res 111(1):75–80. Find this article online
- Mahaffey KR, Clickner RP, Bodurow CC. 2004. Blood organic mercury and dietary mercury intake: National Health and Nutrition Examination Survey, 1999 and 2000. Environ Health Perspect 112:562–570. Find this article online
- Mahaffey KR, Clickner RP, Jeffries RA. 2009. Adult women’s blood mercury concentrations vary regionally in the United States: association with patterns of fish consumption (NHANES 1999–2004). Environ Health Perspect 117:47–53. Find this article online
- Mahaffey KR, Sunderland EM, Chan HM, Choi AL, Grandjean P, Marien K, et al. 2011. Balancing the benefits of n-3 poly-unsaturated fatty acids and the risks of methylmercury exposure from fish consumption. Nutr Rev 69(9):493–508. Find this article online
- Makrides M, Gibson RA, McPhee AJ, Yelland L, Quinlivan J, Ryan P. 2010. Effect of DHA supplementation during pregnancy on maternal depression and neuro-development of young children: a randomized controlled trial. JAMA 304(15):1675–1683. Find this article online
- McFadden D.. 2001. Economic choices. Am Econ Rev 91:351–378. Find this article online
- McManus A, Howieson J, Nicholson J 2009. Review of Literature and Resources Relating to the Health Benefit of Regular Consumption of Seafood as Part of a Healthy Diet. Report 090101. Perth, Australia: Centre of Excellence Science, Seafood and Health, Curtin Health Innovation Research Institute, Curtin University of Technology.
- Mercury Policy Project 2010. Mercury and Fish: The Facts. Available: http://www.mercuryfactsandfish.org/ [accessed 17 April 2012]
- Monterey Bay Aquarium Seafood Watch 2011. Seafood Watch. Available: http://www.montereybayaquarium.org/cr/seafoodwatch.aspx [accessed 14 November 2011]
- Monterey Bay Aquarium Seafood Watch 2012. Seafood Recommendations. Available: http://www.montereybayaquarium.org/cr/cr_seafoodwatch/sfw_recommendations.aspx?c=ln [accessed 17 April 2012]
- Mozaffarian D, Rimm EB. 2006. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA 296(15):1885–1899. Find this article online
- Mozaffarian D, Shi P, Morris JS, Spiegelman D, Grandjean P, Siscovick DS, et al. 2011. Mercury exposure and risk of cardio-vascular disease in two U.S. cohorts. N Engl J Med 364(12):1116–1125. Find this article online
- Myers RA, Worm B. 2005. Extinction, survival or recovery of large predatory fishes. Philos Trans R Soc Lond B Biol Sci 360(1453):13–20. Find this article online
- National Geographic 2012. The Impact of Seafood. Available: http://ocean.nationalgeographic.com/ocean/take-action/impact-of-seafood/#/seafood-decision-guide/ [accessed 17 April 2012]
- National Oceanic and Atmospheric Administration 2012. Fishwatch: U.S. Seafood Facts. Available: http://www.fishwatch.gov/ [accessed 17 April 2012]
- Natural Resources Defense Council 2009. Sustainable Seafood Guide. Available: http://www.nrdc.org/oceans/seafoodguide/default.asp [accessed 17 April 2012]
- Nesheim M, Yaktine A, eds 2007. Seafood Choices: Balancing Benefits and Risks. Washington, DC: National Academies Press.
- Nestle M 2006. What to Eat. New York:North Point Press:
- NRC (National Research Council) 2000. Toxicological Effects of Methylmercury. Washington, DC: National Academy Press.
- Oken E, Kleinman KP, Berland WE, Simon SR, Rich-Edwards JW, Gillman MW. 2003. Decline in fish consumption among pregnant women after a national mercury advisory. Obstet Gynecol 102(2):346–351. Find this article online
- Oken E, Østerdal ML, Gillman MW, Knudsen VK, Halldorsson TI, Strøm M, et al. 2008a. Associations of maternal fish intake during pregnancy and breastfeeding duration with attainment of developmental milestones in early childhood: a study from the Danish National Birth Cohort. Am J Clin Nutr 88(3):789–796. Find this article online
- Oken E, Radesky JS, Wright RO, Bellinger DC, Amarasiriwardena CJ, Kleinman KP, et al. 2008b. Maternal fish intake during pregnancy, blood mercury levels, and child cognition at age 3 years in a US cohort. Am J Epidemiol 167(10):1171–1181. Find this article online
- Oken E, Wright RO, Kleinman KP, Bellinger D, Amarasiriwardena CJ, Hu H, et al. 2005. Maternal fish consumption, hair mercury, and infant cognition in a U.S. Cohort. Environ Health Perspect 113:1376–1380. Find this article online
- Pauly D, Christensen V, Guenette S, Pitcher TJ, Simaila UR, Walters CJ, et al. 2002. Toward sustainability in world fisheries. Nature 418:689–695. Find this article online
- Physicians for Social Responsibility and Association of Reproductive Health Professionals 2004. Healthy Fish, Healthy Families. Available: http://www.psr.org/assets/pdfs/hfhf_english.pdf [accessed 17 April 2012]
- Rice DC, Schoeny R, Mahaffey K. 2003. Methods and rationale for derivation of a reference dose for methylmercury by the U.S. EPA. Risk Anal 23(1):107–115. Find this article online
- Rice JC, Garcia SM. 2011. Fisheries, food security, climate-change, and biodiversity: characteristics of the sector and perspectives on emerging issues. ICES J Mar Sci 68(6):1343–1353. Find this article online
- Roman HA, Walsh TL, Coull BA, Dewailly É, Guallar E, Hattis D, et al. 2011. Evaluation of the cardio-vascular effects of methyl-mercury exposures: current evidence supports develop-ment of a dose-response function for regulatory benefits analysis. Environ Health Perspect 119:607–614. Find this article online
- Scherer AC, Tsuchiya A, Younglove LR, Burbacher TM, Faustman EM. 2008. Comparative analysis of state fish consumption advisories targeting sensitive populations. Environ Health Perspect 116:1598–1606. Find this article online
- Shedd Aquarium 2012. Conservation. Available: http://www.sheddaquarium.org/3163.html [accessed 17 April 2012]
- Shimshack JP, Ward MB. 2010. Mercury advisories and household health trade-offs. J Health Econ 29(5):674–685. Find this article online
- Shimshack JP, Ward MB, Beatty TKM. 2007. Mercury advisories: information, education, and fish consumption. J Environ Econ Manag 53:158–179. Find this article online
- Silver E, Kaslow J, Lee D, Lee S, Lynn Tan M, Weis E, et al. 2007. Fish consumption and advisory awareness among low-income women in California’s Sacramento-San Joaquin Delta. Environ Res 104(3):410–419. Find this article online
- Simmer K, Patole SK, Rao SC. 2008a. Longchain poly-unsaturated fatty acid supplementation in infants born at term. Cochrane Database Syst Rev ((1):CD000376.; doi:10.1002/14651858.CD000376.pub2 [Online 8 October 2008] Find this article online
- Simmer K, Schulzke SM, Patole S. 2008b. Longchain poly-unsaturated fatty acid supplementation in preterm infants. Cochrane Database Syst Rev ((1):CD000375.; doi:10.1002/14651858.CD000375.pub3 [Online 8 October 2008] Find this article online
- Slovic P, Fischoff B, Lichtenstein S 2000. Facts and fears: understanding perceived risk. In: The Perception of Risk (Slovic P, ed). London:Earthscan, 137–154.
- Star Chefs 2004. Loving our Seafood to Death?. Available: http://starchefs.com/features/food_debates/html/sustainable_seafood.shtml [accessed 17 April 2012].
- State of Connecticut Department of Public Health 2012. Connecticut’s Fish Consumption Advisory and the Safe Eating of Fish Caught in Connecticut. Available: http://www.ct.gov/dph/cwp/view.asp?a=3140&Q=387460 [accessed 17 April 2012]
- Stern AH. 2007. Public health guidance on cardio-vascular bene-fits and risks related to fish consumption. Environ Health 6:31.; doi:10.1186/1476-069X-6-31 [Online 23 October 2007] Find this article online
- Stern AH, Korn LR. 2011. An approach for quantitatively balancing methylmercury risk and omega-3 benefit in fish consumption advisories. Environ Health Perspect 119:1043–1046. Find this article online
- Subasinghe S, Soto D, Jia J.. 2009. Global aquaculture and its role in sustainable development. Rev Aquacult 1(1):2–9. Find this article online
- Sunderland EM. 2007. Mercury exposure from domestic and imported estuarine and marine fish in the U.S. seafood market. Environ Health Perspect 115:235–242. Find this article online
- Tollefson L, Cordle F.. 1986. Methylmercury in fish: a review of residue levels, fish consumption and regulatory action in the United States. Environ Health Perspect 68:203–208. Find this article online
- Tsuchiya A, Hardy J, Burbacher TM, Faustman EM, Marien K. 2008. Fish intake guidelines: incorporating n-3 fatty acid intake and contaminant exposure in the Korean and Japanese communities. Am J Clin Nutr 87(6):1867–1875. Find this article online
- Turtle Island Restoration Network 2012. Got Mercury?. Available: http://www.gotmercury.org [accessed 17 April 2012].
- USDA (U.S. Department of Agriculture) 2009. USDA National Nutrient Database for Standard Reference, Release 24. Available: http://www.ars.usda.gov/nutrientdata [accessed 16 April 2012]
- USDA (U.S. Department of Agriculture) and Department of Health and Human Services 2010. Dietary Guidelines for Americans. 7th ed. Available: http://www.health.gov/dietaryguidelines/dga2010/DietaryGuidelines2010.pdf [accessed 17 April 2012]
- U.S. EPA (Environmental Protection Agency) 2004. FDA/EPA Consumer Advisory: What You Need to Know about Mercury in Fish and Shellfish. Available: http://www.epa.gov/ost/fishadvice/factsheet.html [accessed 14 November 2011]
- U.S. EPA (Environmental Protection Agency) 2010. Fish Advisories. Available: http://water.epa.gov/scitech/swguidance/fishshellfish/fishadvisories/index.cfm [accessed 18 April 2012]
- Vanhonacker F, Altintzoglou T, Luten J, Verbeke W.. 2011. Does fish origin matter to European consumers? Insights from a consumer survey in Belgium, Norway and Spain. Br Food J 113(4):535–549. Find this article online
- Verbeke W, Sioen I, Pieniak Z, Van Camp J, De Henauw S.. 2005. Consumer perception versus scientific evidence about health benefits and safety risks from fish consumption. Public Health Nutr 8(4):422–429. Find this article online
- Verbeke W, Vackier I.. 2005. Individual determinants of fish consumption: application of the theory of planned behaviour. Appetite 44(1):67–82. Find this article online
- Verbeke W, Vanhonacker F, Frewer LJ, Sioen I, De Henauw S, Van Camp J. 2008. Communicating risks and benefits from fish consumption: impact on Belgian consumers’ perception and intention to eat fish. Risk Anal 28(4):951–967. Find this article online
- Verbeke W, Vanhonacker F, Sioen I, Van Camp J, De Henauw S.. 2007. Perceived importance of sustainability and ethics related to fish: a consumer behavior perspective. Ambio 36(7):580–585. Find this article online
- Verger P, Houdart S, Marette S, Roosen J, Blanchemanche S.. 2007. Impact of a risk-benefit advisory on fish consumption and dietary exposure to methylmercury in France. Regul Toxicol Pharmacol 48(3):259–269. Find this article online
- Viscusi WK. 1997. Alarmist decisions with divergent risk information. Econ J 107:1657–1670. Find this article online
- Volpe JP, Gee J, Beck M, Ethier V 2011. How Green Is Your Eco-label? Comparing the Environmental Benefits of Marine Aquaculture Standards. Victoria, British Columbia, Canada:University of Victoria.:
- Washington State Department of Health 2011. Fish - Eat Fish, Be Smart, Choose Wisely. Available: http://www.doh.wa.gov/ehp/oehas/fish/default.htm [accessed 17 April 2012]
- WHO (World Health Organization)/United Nations Environment Program 2008. Guidance for Identifying Populations at Risk from Mercury Exposure. Available: http://www.chem.unep.ch/Mercury/IdentifyingPopnatRiskExposuretoMercuryFinalAugust08.pdf [accessed 23 November 2011]
- Worm B, Hilborn R, Baum JK, Branch TA, Collie JS, Costello C, et al. 2009. Rebuilding global fisheries. Science 325(5940):578–585. Find this article online
- Worm B, Myers RA. 2004. Managing fisheries in a changing climate. Nature 429(6987):15.. Find this article online
Belgium has two ecoregions:
- Atlantic mixed forests
- Western European broadleaf forests
Atlantic mixed forests
The Atlantic mixed forests ecoregion includes coastal vegetation formations of dunes and heathlands with vegetation that thrives in salty soil. Sand dune systems occur along the southwestern coast of France, the region known as Les Landes, covered by both natural and planted forests of maritime pine (Pinus pinaster). They are rich in plant life, and home to a number of endemics. Bird diversity is particularly high--over 440 species have been recorded in the Netherlands alone. Most of the ecoregion’s mammals are widespread in other parts of Europe. Several are listed on the International Union for Conservation of Nature and Natural Resources Red List, including otter, European mink, and several species of bat. Only fragments of natural vegetation remain in this ecoregion, as most of the area was converted long ago into intensive agriculture or pasture.Western European broadleaf forests
The south is included within the Western European broadleaf forests ecoregion. This region includes the middle of France, extending into Germany. Warm, moist air from the Atlantic Ocean dominates this inland ecoregion. Small mountains (no higher than 5,000 feet [1,500 m]), hills, and valleys are found throughout the area. Yearly temperatures are steady, precipitation is fairly evenly distributed throughout the year, and frosts occur for one to three months. This ecoregion maintains healthy bird populations, but most of the larger mammals are in decline and have been extirpated from many areas. Throughout this ecoregion, the landscape is dominated by urbanization and agriculture, including vineyards and other monocultural plantings. Most streams have been altered for use in irrigation, and many valleys are flooded by dams constructed for increasing power and water supplies.Context
Ecoregions are areas that:
 share a large majority of their species and ecological dynamics;
 share similar environmental conditions; and,
 interact ecologically in ways that are critical for their long-term persistence.
Bangladesh has five ecoregions:
- Sundarbans mangroves
- Sundarbans freshwater swamp forests
- Lower Gangetic Plains moist deciduous forests
- Mizoram-Manipur-Kachin rain forests
- Myanmar coastal rain forests
The ecoregion lies in the vast delta formed by the confluence of the Ganges, Brahmaputra, and Meghna rivers. The maze of mangrove channels extends across southern Bangladesh and India's West Bengal State.The Sundarbans Mangroves ecoregion is the world's largest mangrove ecosystem.
Named after the dominant mangrove species Heritiera fomes, locally known as sundri, this is the only mangrove ecoregion that harbors the Indo-Pacific region's largest predator, the tiger (Panthera tigris).
Unlike in other habitats, here tigers live and swim among the mangrove islands, where they hunt scarce prey such as chital deer (Cervus axis), barking deer (Muntiacus muntjak), wild pig (Sus scrofa), and even macaques (Macaca mulatta). Quite frequently, the people who venture into these impenetrable forests to gather honey, to fish, and to cut mangrove trees to make charcoal also fall victim to the tigers.
But the ecoregion's importance is not based solely on its role as a priority tiger conservation area. Mangroves are a transition from the marine to freshwater and terrestrial systems. They provide critical habitat for numerous species of fishes and crustaceans that are adapted to live, reproduce, and spend their juvenile lives among the tangled mass of roots, known as pneumatophores, that grow upward from the anaerobic mud to get the trees' supply of oxygen.
Bangladesh supports one of the world's highest human population densities. About half of this ecoregion's mangrove forests have been cut down to supply the fuelwood and other natural resources extracted from these forests by this large population. Despite the intense and large-scale exploitation, the ecoregion still is one of the largest contiguous areas of mangroves in the world.
There are seven protected areas that cover almost 2,700 square kilometers (km2), or 15 percent of the ecoregion (table 2). Despite the high proportion of the ecoregion being within the protected area system, only one of these, Sajnakhali, is large enough to support a space-dependent species such as the tiger. Many of the protected areas also lack trained and dedicated personnel and infrastructure to adequately manage them.Sundarbans freshwater swamp forests
This ecoregion represents the brackish swamp forests that lie behind the Sundarbans Mangroves where the salinity is more pronounced. The freshwater ecoregion is an area where the water is only slightly brackish and becomes quite fresh during the rainy season, when the freshwater plumes from the Ganges and Brahmaputra rivers push the intruding salt water out and also bring a deposit of silt. Like the vast mangrove ecoregion, the freshwater swamp forest ecoregion also straddles the boundary between Bangladesh and India's state of West Bengal.
The Sundarbans Freshwater Swamp Forests ecoregion is nearly extinct. Hundreds of years of habitation and exploitation by one of the world's densest human populations have exacted a heavy toll of this ecoregion's habitat and biodiversity.
Because it sits in the vast, productive delta of the Ganges and Brahmaputra rivers, the annual alluvial deposits make the ecoregion exceptionally productive. Therefore, most of the natural habitat has long been converted to agriculture, making it almost impossible to even surmise the original composition of the ecoregion's biodiversity.
This ecoregion is nearly extinct, the victim of large-scale clearing and settlement to support one of the densest human populations in Asia. There are two protected areas that cover a mere 130 square kilometers (km2) of the ecoregionLower Gangetic Plains moist deciduous forests
The Lower Gangetic Plains Moist Deciduous Forests lie along the confluence of two of Asia's largest rivers, the Ganges and Brahmaputra rivers, which run the length of the Himalayan foothills and drain its breadth. It once harbored impressive populations of tiger (Panthera tigris), greater one-horned rhinoceros (Rhinoceros unicornis),Asian elephant (Elephas maximus), gaur (Bos gaurus), swamp deer (Cervus duvaucelli), and Bengal florican (Eupodotis bengalensis). Today, the ecoregion supports one of the densest human populations on Earth, and the fertile alluvial plains have been cleared and intensely cultivated. The human activities that date back thousands of years have taken a very heavy toll on the natural biodiversity of the ecoregion, and many of these species have disappeared from the ecoregion.
Despite hundreds of years of human settlement, much forest still remained until the early twentieth century. Since then deforestation has accelerated, and now the ecoregion's natural habitat borders on the verge of extinction. Only about 3 percent of the ecoregion is now under natural forest, and only one large block of intact habitat (south of Varanasi) remains in this ecoregion. Although more than forty protected areas are represented in the ecoregion, they cover only about 3 percent of the ecoregion, and more than half of these protected areas are small, being less than 100 km2 in areaMizoram-Manipur-Kachin rain forests
This large ecoregion represents the semi-evergreen submontane rain forests that extend from the midranges of the Arakan Yoma and Chin Hills north into the Chittagong Hills of Bangladesh the Mizo and Naga hills along the Myanmar-Indian border, and into the northern hills of Myanmar. It divides the Brahmaputra and Irrawaddy valleys, through which two of Asia's largest rivers flow.
The Mizoram-Manipur-Kachin Rain Forests has the highest bird species richness of all ecoregions that are completely within the Indo-Pacific region. (The only ecoregions that have more birds are the Northern Indochina Subtropical Forests and South China-Vietnam Subtropical Evergreen Forests that extend into China.) Except the pioneering explorations of Kingdon-Ward (1921, 1930, 1952) and Burma Wildlife Survey made by Oliver Milton and Richard D. Estes (1963), few scientific surveys have been made in this ecoregion. Once exception has been the recent Wildlife Conservation Society (WCS) and Smithsonian Institution's reptile survey in northwestern Myanmar. Therefore these rugged mountains' biodiversity remains largely unknown.
Almost half of this ecoregion's natural habitat is still intact, especially in the eastern areas within Myanmar. There are fifteen protected areas that cover about 3,700 km2 (3 percent) of the ecoregion (Table 3). Nonetheless, several other intact habitats should be incorporated to create a more comprehensive and representative protected area network that includes the diverse habitats and biodiversity contained within this ecoregion.Myanmar coastal rain forests
This ecoregion represents the lowland evergreen and semi-evergreen rain forests of the western side of Arakan Yoma and Tenasserim ranges along the west coast of Myanmar. A small area extends into southeast Bangladesh.
The Myanmar Coastal Rain Forests are a diverse set of climatic niches and habitats that include flora and fauna from the Indian, Indochina, and Sundaic regions. Though low in endemism, this ecoregion has a tremendous species diversity. However, the forests have been increasingly destroyed to make way for agriculture, and poaching has become the dominant threat to the remaining wildlife populations.
Most of the seasonal evergreen forest and almost all the freshwater swamp of this ecoregion has been cleared for agriculture, especially along the fertile, densely populated plains of the Irrawaddy. Heavy degradation is evident around Myeik (Mergui) and Dawei (Tavoy). Further north, large tracts of forest have been cut, including the gorges of the Thanlwin (Salween) River where it enters the Andaman Sea at Mawlamyine, an area that once harbored many local or endemic species of orchids, begonias, and other herbs. This ecoregion is inadequately protected; there are five proposed protected areas that cover about 2,700 km2 (4 percent) of the ecoregion area (Table 2). Of these one, Pegu Yomas, shared with Irrawaddy moist deciduous forests accounts for almost 2,500 km2. Along Myanmar's western coast, extensive areas of forest remain that are worthy of conservation and should be brought under protection and managed effectively to increase representation in this diverse ecoregion.Types and Severity of Threats
The continued development of flat, lowland areas for irrigated paddy rice and subsistence crops such as hill rice, cassava, yams, and vegetables on hilly ground will be a major threat in the future. Forests are being exploited extensively for timber because the country is hungry for foreign currency.
Wildlife trade and poaching are a major threat to the rapidly declining large mammals and medicinal plants in both regions of Arakan and Tenasserim coasts. Tigers are almost extinct in the northern part of the ecoregion along the Arakan Yoma because of intense demand in China and Thailand.
Ecoregions are areas that:
 share similar environmental conditions; and,
 interact ecologically in ways that are critical for their long-term persistence.
Scientists at the World Wildlife Fund (WWF), have established a classification system that divides the world in 867 terrestrial ecoregions, 426 freshwater ecoregions and 229 marine ecoregions that reflect the distribution of a broad range of fauna and flora across the entire planet.
Linda S. Birnbaum, Ph.D., D.A.B.T., A.T.S., is Director of the National Institute of Environmental Health Sciences (NIEHS) of the National Institutes of Health (NIH), and National Toxicology Program Division. As NIEHS and NTP director, Dr. Birnbaum oversees a budget that funds multidisciplinary biomedical research programs, prevention, and intervention efforts that encompass training, education, technology transfer, and community outreach. The NIEHS supports more than 1,000 research grants.
Dr. Birnbaum has received numerous awards, including the Women in Toxicology Elsevier Mentoring Award, the Society of Toxicology Public Communications Award, EPA’s Health Science Achievement Award and Diversity Leadership Award, and 12 Science and Technology Achievement Awards. She is the author of several hundred peer-reviewed publications, book chapters, abstracts, and reports. Dr. Birnbaum received her M.S. and Ph.D. in microbiology from the University of Illinois, Urbana. A board certified toxicologist, Dr. Birnbaum has served as a federal scientist for 30 years - 19 years with the U.S. Environmental Protection Agency Office of Research and Development, and the first ten years at NIEHS as a senior staff fellow at the National Toxicology Program, then as a principal investigator and research microbiologist, and finally as a group leader for the Institute’s Chemical Disposition Group.
Oil and natural gas production is the United States’ largest industrial source of VOCs, although a smaller source than the nation’s leading overall contributor, gasoline-powered vehicles.
This article, written by Bob Weinhold* appeared first in Environmental Health Perspectives—the peer-reviewed, open access journal of the National Institute of Environmental Health Sciences.
The article is a verbatim version of the original and is not available for edits or additions by Encyclopedia of Earth editors or authors. Companion articles on the same topic that are editable may exist within the Encyclopedia of Earth.The Future of Fracking: New Rules Target
Air Emissions for Cleaner Natural Gas Production
Natural gas is lauded as a cleaner-burning fuel than either coal or oil, but getting the fuel out of the ground can be a dirty process, especially given the widespread adoption of the technology known as hydraulic fracturing (“fracking”). Concerns about toxic air emissions from previously unregulated fracking sites led to the U.S. Environmental Protection Agency (EPA) announcement on 18 April 2012 of new and updated air pollution regulations for these facilities and certain other elements of oil and natural gas production and transmission.1 Compliance with the new regulations is expected to result in major reductions in emissions of methane and volatile organic compounds (VOCs), particularly from new fracked natural gas wells.
The rules were a hot topic nationally, drawing more than 156,000 comments after the proposed version was released in mid-2011. Under the final rules, companies have until January 2015 to fully phase in the control measures needed; by comparison, the initial proposal called for a 60-day phase-in for many major requirements. The EPA says about half of all new wells already use the equipment needed to capture the targeted emissions.2Click for Larger Image. A hydraulic fracturing natural gas drilling rig on the eastern Colorado plains. In 2009 there were more than 38,000 natural gas wells in the state.© 2012 Ed Darack/Science Faction
Many environmental groups consider the new regulations an improvement over the existing situation, but they tend to be disappointed much more wasn’t done. “This is quite a milestone,” says Jeremy Nichols, Climate and Energy Program director for the advocacy group WildEarth Guardians, one of two groups that filed suit against the EPA in 2009 to force action on the issue. “But is the work done? No, of course not. It’s a floor to build on, providing a minimal level of protection.”
The oil and natural gas industry has its own concerns about the new rules but has indicated it can work with them. In a press release issued the day the rules were announced, Howard Feldman, director of regulatory and scientific affairs for the American Petroleum Institute, said, “EPA has made some improvements in the rules that allow our companies to continue reducing emissions while producing the oil and natural gas our country needs.”3Extraction in the United States
Oil and natural gas drilling are getting easier in some ways, as success rates for finding reserves have increased from 75% in 1990 to 90% in 2009. But companies must drill deeper to extract the resources, with oil and gas drilling depths steadily increasing from averages of 4,841 feet in 1990 to 6,108 feet in 2009. Fracking enables drillers to liberate hard-to-reach oil and hydrocarbons from underground deposits. Nevertheless, average natural gas productivity per well, measured in volume, steadily declined by a total of 36% between 1990 and 2009, with oil wells following suit with a drop of 17%.4(Tables 2-4, 2-5, 2-6)
In 2009 there were an estimated 1.02 million onshore oil and natural gas wells in the United States, split roughly evenly between the two types.4 The total is expected to steadily increase by about 17,000–35,000 natural gas wells and 9,000–10,000 oil wells per year between 2012 and 2035.4(Table 2-13) Connecting the wells, processing plants, distribution facilities, and customers are more than 1.5 million miles of pipelines.4(Table 2-8)
A number of primary and secondary pollutants are linked with this web of facilities.4 One of them, methane, is over 20 times more potent a greenhouse gas than carbon dioxide (CO2) when emitted directly to the atmosphere.5 Hydrogen sulfide and VOCs such as benzene, ethylbenzene, toluene, mixed xylenes, n-hexane, carbonyl sulfide, ethylene glycol, and 2,2,4-trimethylpentane are classified by the EPA as hazardous air pollutants, or air toxics.6 Sulfur dioxide, nitrogen oxides, carbon monoxide, fine particulate matter (PM2.5), and ground-level ozone are classified as criteria air pollutants.7 Both classifications of pollutants cause adverse human health effects, but whereas criteria air pollutants are regulated by air quality standards that localities must achieve, hazardous air pollutants are regulated by requiring specific control technologies for the targeted emissions.
Among human health effects that have been associated with these pollutants are cancer; cardiovascular, respiratory, neurologic, and developmental damage; and adverse outcomes such as premature mortality, emergency department visits, lost work and school days, and/or restricted activity days. The pollutants are also associated with reduced visibility, climate change, and/or vegetation damage.4,9
Oil and natural gas production is the United States’ largest industrial source of VOCs, although a smaller source than the nation’s leading overall contributor, gasoline-powered vehicles.8 The industry also emits nearly 40% of the nation’s total methane.4 In 2015, even with the new rules in place, the oil and natural gas industry’s total VOC emissions will fall by only about 15% and its total methane emissions by only about 13%, according to figures provided by an EPA spokeswoman who spoke on condition of anonymity.
Click for Larger Image.
States with Active Natural Gas Production
In some cases, elevated concentrations of pollutants—some of them exceeding existing standards—have been documented around oil and natural gas facilities in states such as Wyoming,10,11 Utah,10 Colorado,12 New Mexico,12 and Texas.13 In many other cases, however, the concentrations of pollutants around these facilities are unknown.
In May 2012 the EPA designated a number of settings around the country as violating the 2008 ground-level ozone standard of 75 ppb—these included Bakersfield, California; Jamestown, New York; multicounty regions around Denver, Dallas, Fort Worth, Pittsburgh, Columbus, and Cleveland; and three counties in southwestern Wyoming. Many of these areas happen to host oil and natural gas operations, but many also have long histories of poor air quality related to other industries, making it difficult to tease out the contribution of oil and natural gas operations. The natural gas boom region of northeastern Utah also is suspected of contributing to local elevations in ground-level ozone, although there aren’t enough data for a formal violation designation.14
Under the Clean Air Act, the EPA is required to review certain regulations every eight years and revise them if necessary. These regulations include New Source Performance Standards, or NSPSs (which apply to specific types of newly built, modified, and reconstructed facilities), and National Emission Standards for Hazardous Air Pollutants, or NESHAPs (which apply to the air toxics emitted from various facilities). The NSPSs applicable to oil and natural gas production had not been updated since 1985, and the applicable NESHAPs had not been updated since 1999. So on 14 January 2009 WildEarth Guardians and fellow advocacy group San Juan Citizens Alliance filed suit to force the agency to act. The parties signed a consent decree 5 February 2010. The EPA issued proposed rules 28 July 2011 and signed the final regulations 17 April 2012.15A New Era
Some of the rules begin to take effect 60 days after they’re published in the Federal Register (which had not yet occurred as this article went to press), with various phase-in periods for other parts of the rules up to 1 January 2015. The rules apply to all relevant onshore facilities that have been constructed, reconstructed, modified, or refracked since 23 August 2011. The main focus of the new rules is most types of new fracked natural gas wells.16
The primary tool for controlling the relevant emissions is equipment that captures and separates the mixed gases, liquids, and other substances that flow from new wells. Completing the well installation process with this kind of pollution-control equipment has been dubbed a “green completion.” Much of the captured material includes resources with substantial market value, including propane, butane, and liquefied natural gas.4
Steady Growth in Natural Gas
The number of natural gas wells nationally has steadily risen from about 269,000 in 1990 to nearly 500,000 in 2010.4(Table2-5) Meanwhile, total oil production has steadily dropped since 1970 and is now at about two-thirds that peak, although there has been an uptick in the past couple of years, driven almost entirely by the oil fracking surge in North Dakota.31
The overall increase in natural gas extraction is being driven in large part by the increase in consumption, which rose 19% between 1990 and 2009.4(Table 2-10) Most of that increase occurred in the electric power sector, with its share of total consumption rising from about 17% in 1990 to about 30% in 2009. Industrial consumption has declined from about 43% of the total in 1990 to about 32% in 2009. Other sectors have remained fairly steady, with residential use at 20–24%, commercial use at 13–14%, and transportation at 3%.4(Figure 2-5)
© 2012 Les Stone/Corbis
Green completions are mandatory for new wells beginning 1 January 2015 and are encouraged on a voluntary basis before that. Larger companies tend to be the ones already using green completions, Feldman says. In some cases, companies have opted not to use green completions because the necessary transportation facilities (e.g., pipelines for the various gas constituents) are not in place, he says. In other cases, he adds, low pressure in a well has made capture more difficult, or capture is less cost-effective when VOC content is low. Feldman says the 2015 implementation date will allow the industry enough time to get necessary infrastructure in place.
One company that has been using green completion equipment for more than half a dozen years is Devon Energy, headquartered in Oklahoma City. “It’s the right thing to do,” spokesman Chip Minty says. “It reduces emissions and keeps gas in the pipeline. And [the captured] commodities are just as valuable as any commodity from any well,” with no unusual impurities reducing their value.
Owners and operators that choose not to use green completions prior to January 2015 must burn off (or flare) the emissions coming from the new well. Flaring creates combustion pollutants such as carbon monoxide, nitrogen oxides, PM2.5, and CO2, and contributes to formation of often-uncharacterized secondary compounds. However, the EPA estimates that the benefits of preventing the escape of VOCs and methane far outweigh the damage caused by the pollutants produced by flaring.4 Gwen Lachelt, director of the Oil and Gas Accountability Project of the nonprofit Earthworks, says allowing flaring in transition is “certainly not ideal,” in part because it continues to waste valuable resources, but is an improvement over straight venting.Click for Larger Image.
VOC Emissions by Industry, 2008Click for Larger Image.
VOC Emissions by Sector, 2008
Finally, the new rules require reductions in emissions from equipment such as processing plants, storage tanks, pneumatic controllers, glycol dehydrators, and certain pipeline compressors, and they also add various reporting and notification requirements for the industry. “We find [the latter] to be extremely burdensome,” says Kathleen Sgamma, vice president of government and public affairs for the Western Energy Alliance, a nonprofit trade association. “It’s a lot of new record keeping with not a lot of additional environmental benefit.” Nichols of WildEarth Guardians has a different view, saying the requirements could have been more stringent. “But they’re workable for information and transparency,” he says, which is “incredibly important so we can scrutinize if industry is complying.”
The EPA estimates the green completion process and other required changes will annually cut about 95% of the VOCs emitted from 11,400 newly fracked and 1,400 refracked wells.17 For 2015 the agency estimates that full implementation of the new rules will result in reductions of 190,000 tons of VOCs, 11,000 tons of hazardous air pollutants, and methane equivalent to 18 million tons of CO2 above and beyond reductions already mandated in Wyoming, Colorado, and a few places in Texas.4,18
The agency couldn’t calculate how much hazardous air pollutants as a whole will be reduced in the context of emissions from the total oil and natural gas industry. The agency also couldn’t calculate the reductions in pollutants such as hydrogen sulfide and criteria air pollutants PM2.5 and ozone. Nor could it estimate the dollar value of health benefits attributable to the rules because of uncertainties over exactly where future extraction operations would occur and what the local and regional impacts would be.4
However, after comparing the direct cost to industry of complying with the rules against profits from the sale of captured resources, the agency says the industry should net $11–19 million per year.17 Sgamma says that works out to “a miniscule amount” of about $900–1,500 possible profit per well. Upon full implementation the agency also estimates net annual climate-related benefits of about $440 million based on effects such as avoided adverse health effects and damage to crops and coastal property.4
Flaring at a fracked natural gas well in Bradford County, Pennsylvania. Under the new EPA regulations, producers may either flare emissions from new wells until 2015 or capture the emissions using the green-completion equipment that will become mandatory for new wells starting in that year. Although cleaner than straight venting, flaring produces pollutants of its own and burns up valuable commodities.
© 2012 Les Stone/Corbis
Feldman and Sgamma (among others19) say the EPA’s economic assessment is inaccurate, due to factors such as overestimating the quantities of sellable resources recovered and underestimating costs to industry. On 4 June 2012 the American Petroleum Institute and fellow industry association America’s Natural Gas Alliance released estimates of industry methane emissions that were half as much as the EPA estimated.20 The EPA spokeswoman says the agency will review the new report.
Industry expenses vary over time with market cycles, but perhaps the biggest variable is the future price of dry natural gas (nearly pure methane that has been processed to remove water and “wet” hydrocarbon gases that may accompany it out of the ground). The price has fluctuated fourfold between 1990 and mid-2012, often making major moves up and down in just a few years.21 The EPA based its economic calculations on numbers in the middle of this overall price range.4State-Level Actions
Oil and natural gas drilling occur in 33 states.22 The number could conceivably increase; North Carolina is aggressively working to see if recent developments in fracking technology might allow its small deposits, previously considered economically marginal, to become cost-effective.23 Vermont, which also has no producing wells at the moment, is taking a different approach, banning fracking until at least 2016 in order to study potential public health and environmental impacts and develop guidance for regulating the practice.24
As awareness of air pollution from natural gas extraction, processing, and transmission has risen, high-production areas such as the city of Fort Worth and the states of Wyoming and Colorado have begun requiring processes similar to green completions. Wyoming has also been monitoring some pollution hot spots, requiring some industry reporting of emissions, and revising its regulations, says Steven Dietrich, administrator of the Wyoming Department of Environmental Quality’s Air Quality Division. By 2015 he expects the state’s rules will be nearly identical to those of the EPA.
However, that alone won’t be enough to bring Wyoming counties currently violating the ground-level ozone standard into compliance. That job might have been easier if the new EPA rules had addressed existing wells and facilities. That exclusion “makes it more difficult to reduce more emissions,” Dietrich says, because Wyoming, like the EPA, is limited in its authority to rein in existing pollution sources. In the absence of EPA regulations, he says his department will implement strategies that have helped in the past, such as incorporating requirements for diesel-powered equipment into permitting processes.
In Arkansas, the state’s Department of Environmental Quality investigates pollutant leaks in the course of routine compliance inspections or in response to citizen complaints. The state utilizes new infrared cameras as a rapid-detection tool to document leaks, says Mike Bates, chief of the department’s Air Division. The department encourages companies to address leaks voluntarily but has the capacity to pursue enforcement if the company does not act.
Low levels of VOCs have been detected around drilling sites in Arkansas, which most likely came from tanks of diesel fuel–based drilling mud (a multipurpose fluid used in drilling boreholes). A 2011 report from the Arkansas Department of Environmental Quality states, “Although mud tanks are a temporary and probably minor emissions source, their emissions have a strong hydrocarbon odor that may be a nuisance and potential health risk to people living near well sites during the drilling process. Reducing VOC emissions from mud tanks may provide an opportunity to improve the local air quality around active drilling sites.”25
Other emissions have been relatively low in Arkansas compared with other natural gas–producing areas, although some important gaps in data remain, Bates says. This, he says, is likely in part because the gas extracted in Arkansas has low VOC content, and Southwestern Energy, the company that has more than three-fourths of the Arkansas market, already uses green completions extensively. That may make the state’s overall transition to the new EPA rules relatively painless for both the industry and the state. “Since a large segment of the industry is already meeting these standards, we don’t foresee a great impact to the regulated industry in complying with the new rules,” Bates says.
Pennsylvania, which lies atop the enormous Marcellus Shale Deposit, is just beginning to obtain hard data on its industry’s air emissions and will have a final inventory for submission to the EPA by December 2012. The state hasn’t conducted any long-term air monitoring focused on natural gas drilling activities but expects to begin doing so before the end of 2012. Short-term monitoring conducted in 2010 did not identify concentrations of any compound associated with natural gas drilling that would likely trigger air-related health issues, according to Pennsylvania Department of Environmental Protection secretary Mike Krancer, quoted in a December 2011 press release.26 The state is working on an updated set of permit requirements and is analyzing the EPA’s rules, says Kevin Sunday, a spokesman with the department. Senior department officials declined multiple requests to discuss the rules.Expanding the Base
The EPA explicitly chose to not have the new rules apply to existing wells because, on a per-well basis, new wells produce far more VOC emissions and can offset costs for implementing the new rules with sales of captured products. The fact that most existing oil and natural gas wells tend to have relatively low or unknown VOC emissions lessens the potential for applying the new rules to them in a cost-effective manner, even though, combined, they remain a major source of emissions of VOCs and many other pollutants.
Older facilities also can be sources of methane emissions. Based on recent legal developments, including a 2007 Supreme Court ruling and subsequent EPA efforts to regulate greenhouse gases as air pollutants,27 the EPA should have chosen to regulate methane directly, leading to an update of both methane and VOC regulations for all existing wells and facilities, says David Doniger, policy director for the Natural Resources Defense Council’s Climate and Clean Air Program. Since the agency didn’t take that path, Doniger says his organization is deciding whether to sue to force such action.
If they do, they’ll likely be challenged by the industry. “The EPA is using a VOC rule to pursue methane reduction in an almost backhanded way,” Feldman says. “That’s a concern.” But he acknowledges the agency may have the right to regulate methane as an air pollutant, although much litigation is still in process, and the U.S. Congress also could restrict such actions.27
Like Doniger, Lachelt is chagrined that existing wells and facilities weren’t addressed, from both a greenhouse gas and a hazardous air pollutant perspective. “We’re absolutely concerned about the impacts of these facilities on the health of people living near them,” she says. “To not include them [in the new rules] is tragic.”
Neither existing nor new fracked oil wells are covered by the new rules. That’s because “the EPA does not have sufficient data on VOC emissions during completion of hydraulically fractured oil wells to set standards for these operations at this time,” the EPA spokeswoman says. That allows the hundreds of thousands of new oil wells anticipated over the next 20-plus years to operate under existing rules if nothing changes. Much of the activity is likely to occur in high-production areas in North Dakota, California, Colorado, Kansas, Montana, Nebraska, New Mexico, Texas, and Wyoming, some of which began to surge in production in 2007.28 “This is a huge issue,” Nichols says. “We pushed the EPA to rope these in [to the new regulations], but they didn’t want to go down that road.”
Furthermore, according to Nichols, the new rules will not fully protect people against hazardous air pollutants even from new facilities, and they need to be made more rigorous to further reduce emissions. In concert with that, he’d like to see more stringent requirements for monitoring and repairing defects and leaks in pipelines. Some of the pipelines of most concern, according to a Government Accountability Office report issued in March 2012, are the so-called gathering pipelines that take natural gas from wells to processing facilities.29 Only about 10% of the 200,000 miles of gathering pipelines are regulated by federal or state agencies; the remainder tend to be more than 220 yards from human-occupied buildings, so regulation usually is waived.
Unregulated lines occur in at least 29 states. State pipeline safety officials canvassed by the Government Accountability Office say these lines are at elevated risk for poor construction quality, undetected corrosion, poor maintenance, and unmarked locations that increase the odds they will be hit when an area is excavated (which may occur more frequently as natural gas fields are developed close to urbanizing areas). All these problems can contribute to increased air pollution.29 So can the fallout from pipeline cyber attacks, which are an escalating concern at high levels of government.30
Despite these and other concerns acknowledged by some health and environmental advocates, industry members, and government officials, many agree the complex set of new EPA regulations are a decent start in the right direction. Dietrich says, “I thought the rules came out as well as can be expected, balancing the needs of all the different states.” Nichols also is looking positively at the overall result: “Clearly the final rules are a step away from what they initially proposed. Still, it’s a step forward.”References and Notes
1. EPA. Oil and Natural Gas Air Pollution Standards, Regulatory Actions [website]. Washington, DC:U.S. Environmental Protection Agency (updated 20 Apr 2012). Available: http://www.epa.gov/airquality/oilandgas/actions.html [accessed 13 Jun 2012].
2. EPA. EPA Issues Updated, Achievable Air Pollution Standards for Oil and Natural Gas [press release]. Washington, DC:U.S. Environmental Protection Agency (18 Apr 2012). Available: http://yosemite.epa.gov/opa/admpress.nsf/79c090e81f0578738525781f0043619b/c742df7944b37c50852579e400594f8f!OpenDocument [accessed 13 Jun 2012].
3. API. EPA Made Constructive Changes in Hydraulic Fracturing Rules, API Says [press release]. Washington, DC:American Petroleum Institute (18 Apr 2012). Available: http://www.api.org/news-and-media/news/n ewsitems/2012/apr-2012/epa-made-construc tive-changes-in-hydraulic-fracturing-rules.aspx [accessed 13 Jun 2012].
4. EPA. Regulatory Impact Analysis: Final New Source Performance Standards and Amendments to the National Emission Standards for Hazardous Air Pollutants for the Oil and Natural Gas Industry. Research Triangle Park, NC:Office of Air Quality Planning and Standards, U.S. Environmental Protection Agency (Apr 2012). Available: http://www.epa.gov/ttn/ecas/regdata/RIAs/oil_natural_gas_final_neshap_nsps_ria.pdf [accessed 13 Jun 2012].
5. EPA. Methane [website]. Washington, DC:U.S. Environmental Protection Agency (updated 1 Apr 2011). Available: http://www.epa.gov/outreach/index.html [accessed 13 Jun 2012].
6. EPA. About Air Toxics [website]. Washington, DC:U.S. Environmental Protection Agency (updated 17 Aug 2010). Available: http://www.epa.gov/ttn/atw/allabout.html [accessed 13 Jun 2012].
7. EPA. National Ambient Air Quality Standards (NAAQS) [website]. Washington, DC:U.S. Environmental Protection Agency (updated 1 May 2012). Available: http://epa.gov/air/criteria.html [accessed 13 Jun 2012].
8. EPA. The National Emissions Inventory [website]. Research Triangle Park, NC:Office of Air Quality Planning and Standards, U.S. Environmental Protection Agency (updated 23 May 2012). Available: http://www.epa.gov/ttn/chief/net/2008inventory.html [accessed 13 Jun 2012].
9. EPA. Oil and Natural Gas Air Pollution Standards, Regulatory Actions, Section III.D [website]. Washington, DC:U.S. Environmental Protection Agency (updated 20 Apr 2012). Available: http://www.epa.gov/airquality/oilandgas/actions.html [accessed 13 Jun 2012].
10. Jaffe M. Like Wyoming, Utah Finds High Wintertime Ozone Pollution Near Oil, Gas Wells. Denver Post, Business News section, Energy subsection, online edition (26 Feb 2012). Available: http://www.denverpost.com/business/ci_20042330 [accessed 13 Jun 2012].
11. McKenzie LM, et al. Human health risk assessment of air emissions from development of unconventional natural gas resources. Sci Total Environ 424:79–87. 2012. http://dx.doi.org/10.1016/j.scitotenv.2012.02.018
12. EPA. AirData, Monitor Values Report [website]. Washington, DC:U.S. Environmental Protection Agency. Available: http://www.epa.gov/airdata/ad_rep_mon.html [accessed 13 Jun 2012].
13. City of Fort Worth. Natural Gas Air Quality Study (Final Report). Fort Worth, TX:Eastern Research Group and the City of Fort Worth (13 Jul 2011). Available: http://fortworthtexas.gov/gaswells/default.aspx?id=87074 [accessed 13 Jun 2012].
14. EPA. Final Nonattainment Areas for the 2008 Ozone Standards [website]. Washington, DC:U.S. Environmental Protection Agency (updated 1 May 2012). Available: http://www.epa.gov/ozonedesignations/2008standards/final/finalmap.htm [accessed 13 Jun 2012].
15. EPA. Oil and Natural Gas Air Pollution Standards, Regulatory Actions, Section III.B [website]. Washington, DC:U.S. Environmental Protection Agency (updated 20 Apr 2012). Available: http://www.epa.gov/airquality/oilandgas/actions.html [accessed 13 Jun 2012].
16. A few types of wells are exempted, including 1) low-pressure wells (including about 87% of those fracked in coal bed methane formations), since those can pose safety problems when handling the escaping substances due to uncertain, variable, or reverse pressure; and 2) exploratory wells used to determine if a field may be productive prior to installation of infrastructure needed to collect and transport captured substances.
17. EPA. Overview of Final Amendments to Air Regulations for the Oil And Natural Gas Industry Fact Sheet. Research Triangle Park, NC:Office of Air Quality Planning and Standards, U.S. Environmental Protection Agency (17 Apr 2012). Available: http://www.epa.gov/airquality/oilandgas/pdfs/20120417fs.pdf [accessed 13 Jun 2012].
18. The methane number reflects a decrease of 19 million tons plus an increase of 1 million tons as a result of flaring. The EPA estimates another 100,000 tons of VOCs, 8,000 tons of air toxics, and 14 million tons of CO2 equivalent are already being reduced through current voluntary efforts that will become mandatory in 2015. The term “CO2 equivalent” is used because the standard practice is to convert the greenhouse gas role of each of the many individual greenhouse gas contributors to a number relative to CO2 (the baseline reference) in order to facilitate a composite calculation for all greenhouse gas contributors.
19. EPA. Oil and Natural Gas Sector: New Source Performance Standards and National Emission Standards for Hazardous Air Pollutants Reviews. 40 CFR Parts 60 and 63. Response to Public Comments on Proposed Rule August 23, 2011 (76 FR 52738). Research Triangle Park, NC:Office of Air Quality Planning and Standards, U.S. Environmental Protection Agency (2012). Available: http://www.epa.gov/airquality/oilandgas/pdfs/20120418rtc.pdf [accessed 13 Jun 2012].
20. Shires T, Lev-On M. Characterizing Pivotal Sources of Methane Emissions from Unconventional Natural Gas Production: Summary and Analysis of API and ANGA Survey Responses. Washington, DC:American Petroleum Institute, American Natural Gas Alliance (1 Jun 2012). Available: http://www.api.org/news-and-media/news/newsitems/2012/jun-2012/api-anga-study-methane-emissions-are-half-epa-estimate.aspx [accessed 13 Jun 2012].
21. EIA. Annual Energy Outlook 2011. Washington, DC:U.S. Energy Information Administration, U.S. Department of Energy (26 Apr 2012). Available: http://18.104.22.168/forecasts/archive/aeo11/MT_naturalgas.cfm [accessed 13 Jun 2012].
22. EIA. Petroleum: Distribution and Production of Oil and Gas Wells by State. Washington, DC:U.S. Energy Information Administration, U.S. Department of Energy (7 Jan 2011). Available: http://www.eia.gov/pub/oil_gas/petrosystem/petrosysog.html [accessed 13 Jun 2012].
23. NCDENR. Shale Gas [website]. Raleigh, NC:North Carolina Department of Environment and Natural Resources. Available: http://portal.ncdenr.org/web/guest/shale-gas [accessed 13 Jun 2012].
24. State of Vermont Legislature. Bill H. 464. An act relating to hydraulic fracturing wells for natural gas and oil production. Effective 16 May 2012. Available: http://www.leg.state.vt.us/database/status/summary.cfm?Bill=H%2E0464&Session=2012 [accessed 13 Jun 2012].
25. ADEQ. Emissions Inventory & Ambient Air Monitoring of Natural Gas Production in the Fayetteville Shale Region. North Little Rock, AR:Arkansas Department of Environmental Quality. (22 Nov 2011). Available: http://www.adeq.state.ar.us/air/default.htm [accessed 13 Jun 2012].
26. PDEP. DEP to Collect Air Emissions Data about Natural Gas Operations. Operators Face March Deadline to Return Information [press release]. Harrisburg, PA:Pennsylvania Department of Environmental Protection (7 Dec 2011). Available: http://www.portal.state.pa.us/portal/server.pt/community/newsroom/14287?id=19174&typeid=1 [accessed 13 Jun 2012].
27. Meltz R. Federal Agency Actions Following the Supreme Court’s Climate Change Decision in Massachusetts v. EPA: A Chronology. Washington, DC:Congressional Research Service (1 May 2012). Available: http://www.fas.org/sgp/crs/misc/R41103.pdf [accessed 13 Jun 2012].
28. OilShaleGas.com. Oil & Shale Gas Discovery News [website] (updated daily). Available: http://oilshalegas.com [accessed 13 Jun 2012].
29. GAO. Pipeline Safety: Collecting Data and Sharing Information on Federally Unregulated Gathering Pipelines Could Help Enhance Safety. GAO-12-388. Washington, DC:U.S. Government Accountability Office (22 Mar 2012). Available: http://www.gao.gov/products/GAO-12-388 [accessed 13 Jun 2012].
30. Goode D, Martinez J. Risk of Cyberattacks Clouds Natural Gas Boom. Politico, Congress section (8 May 2012). Available: http://www.politico.com/news/stories/0512/76060.html [accessed 13 Jun 2012].
31. EIA. Petroleum & Other Liquids: U.S. Field Production of Crude Oil. Washington, DC:U.S. Energy Information Administration, U.S. Department of Energy (30 May 2012). Available: http://www.eia.gov/dnav/pet/hist/LeafHandler.ashx?n=PET&s=MCRFPUS1&f=A [accessed 13 Jun 2012].Editor's Notes
- *Bob Weinhold, MA, has covered environmental health issues for numerous outlets since 1996. He is a member of the Society of Environmental Journalists.
- Citation: Weinhold B 2012. The Future of Fracking: New Rules Target Air Emissions for Cleaner Natural Gas Production. Environ Health Perspect 120:a272-a279. http://dx.doi.org/10.1289/ehp.120-a272
- Online: 02 July 2012
Autism, attention deficit/hyperactivity disorder (ADHD), mental retardation, dyslexia, and other biologically based disorders of brain development affect between 400,000 and 600,000 of the 4 million children born in the United States each year. Exploration of the environmental causes of autism and other NDDs has been catalyzed by growing recognition of the exquisite sensitivity of the developing human brain to toxic chemicals.
This Editorial, written by Philip J. Landrigan, Luca Lambertini, and Linda S. Birnbaum* appeared first in Environmental Health Perspectives—the peer-reviewed, open access journal of the National Institute of Environmental Health Sciences.
The article is a verbatim version of the original and is not available for edits or additions by Encyclopedia of Earth editors or authors. Companion articles on the same topic that are editable may exist within the Encyclopedia of Earth.A Research Strategy to Discover the Environmental
Causes of Autism and Neurodevelopmental Disabilities
Autism, attention deficit/hyperactivity disorder (ADHD), mental retardation, dyslexia, and other biologically based disorders of brain development affect between 400,000 and 600,000 of the 4 million children born in the United States each year. The Centers for Disease Control and Prevention (CDC) has reported that autism spectrum disorder (ASD) now affects 1.13% (1 of 88) of American children (CDC 2012) and ADHD affects 14% (CDC 2005; Pastor and Reuben 2008). Treatment of these disorders is difficult; the disabilities they cause can last lifelong, and they are devastating to families. In addition, these disorders place enormous economic burdens on society (Trasande and Liu 2011).
Although discovery research to identify the potentially preventable causes of neuro-develop-mental disorders (NDDs) has increased in recent years, more research is urgently needed. This research encompasses both genetic and environmental studies.
Genetic research has received particular investment and attention (Autism Genome Project Consortium et al. 2007; Buxbaum and Hof 2011; Fernandez et al. 2012; O’Roak et al. 2011; Sakurai et al. 2011) and has demonstrated that ASD and certain other NDDs have a strong hereditary component (Buxbaum and Hof 2011; Sakurai et al. 2011). Linkage studies have identified candidate autism susceptibility genes at multiple loci, most consistently on chromosomes 7q, 15q, and 16p (Autism Genome Project Consortium et al. 2007; Sakurai et al. 2011). Exome sequencing in sporadic cases of autism has detected new mutations (O’Roak et al. 2011), and copy number variant studies have identified several hundred copy number variants putatively linked to autism (Fernandez et al. 2012). The candidate genes most strongly implicated in NDD causation encode for proteins involved in synaptic architecture, neuro-transmitter synthesis (e.g., ©-amino-butyric acid serotonin), oxytocin receptors, and cation trafficking (Sakurai et al. 2011). No single anomaly predominates. Instead, autism appears to be a family of diseases with common phenotypes linked to a series of genetic anomalies, each of which is responsible for no more than 2–3% of cases. The total fraction of ASD attributable to genetic inheri-tance may be about 30–40%.
Exploration of the environmental causes of autism and other NDDs has been catalyzed by growing recognition of the exquisite sensitivity of the developing human brain to toxic chemicals (Grandjean and Landrigan 2006). This susceptibility is greatest during unique “windows of vulnerability” that open only in embryonic and fetal life and have no later counterpart (Miodovnik 2011). “Proof of the principle” that early exposures can cause autism comes from studies linking ASD to medications taken in the first trimester of pregnancy—thalidomide, misoprostol, and valproic acid—and to first-trimester rubella infection (Arndt et al. 2005; Daniels 2006).
This “proof-of-principle” evidence for environmental causation is supported further by findings from prospective birth cohort epidemio-logical studies, many of them supported by the National Institute of Environmental Health Sciences (NIEHS). These studies enroll women during pregnancy, measure prenatal exposures in real time as they occur, and then follow children longitudinally with periodic direct examinations to assess growth, development, and the presence of disease. Prospective studies are powerful engines for the discovery of etiologic associations between prenatal exposures and NDDs. They have linked autistic behaviors with prenatal exposures to the organophosphate insecticide chlorpyrifos (Eskenazi et al. 2007) and also with prenatal exposures to phthalates (Miodovnik et al. 2011). Additional prospective studies have linked loss of cognition (IQ), dyslexia, and ADHD to lead (Jusko et al. 2008), methyl-mercury (Oken et al. 2008), organophosphate insecticides (London et al. 2012), organo-chlorine insecticides (Eskenazi et al. 2008), polychlorinated biphenyls (Winneke 2011), arsenic (Wasserman et al. 2007), manganese (Khan et al. 2011), polycyclic aromatic hydrocarbons (Perera et al. 2009), bisphenol A (Braun et al. 2011), brominated flame retardants (Herbstman et al. 2010), and perfluorinated compounds (Stein and Savitz 2011).
Toxic chemicals likely cause injury to the developing human brain either through direct toxicity or inter-actions with the genome. An expert committee convened by the U.S. National Academy of Sciences (NAS) estimated that 3% of neuro-behavioral disorders are caused directly by toxic environmental exposures and that another 25% are caused by inter-actions between environmental factors, defined broadly, and inherited susceptibilities (National Research Council 2000). Epigenetic modification of gene expression by toxic chemicals that results in DNA methyla-tion, histone modification, or changes in activity levels of non-protein-coding RNA (ncRNAs) may be a mechanism of such gene–environment interaction (Grafodatskaya et al. 2010). Epigenetic “marks” have been shown to be able to influence gene expression and alter high-order DNA structure (Anway and Skinner 2006; Waterland and Jirtle 2004).
A major unanswered question is whether there are still undiscovered environ-mental causes of autism or other NDDs among the thousands of chemicals currently in wide use in the United States. In the past 50 years, > 80,000 new synthetic chemicals have been developed (Landrigan and Goldman 2011). The U.S. Environmental Protection Agency has identified 3,000 “high production volume” (HPV) chemicals that are in widest use and thus pose greatest potential for human exposure (Goldman 1998). These HPV chemicals are used today in millions of consumer products. Children and pregnant women are exposed extensively to them, and CDC surveys detect quantifiable levels of nearly 200 HPV chemicals in the bodies of virtually all Americans, including pregnant women (Woodruff et al. 2011).
The significance of early chemical exposures for children’s health is not yet fully understood. A great concern is that a large number of the chemicals in widest use have not undergone even minimal assessment of potential toxicity, and only about 20% have been screened for potential toxicity during early development (Landrigan and Goldman 2011). Unless studies specifically examine develop-mental consequences of early exposures to untested chemicals, sub-clinical dysfunction caused by these exposures can go unrecognized for years. One example is the “silent epidemic” of childhood lead poisoning: From the 1940s to the 1980s, millions of American children were exposed to excessive levels of lead from paint and gasoline, resulting in reduced average intelligence by 2–5 IQ points (Grosse et al. 2002). The late David Rall, former director of NIEHS, once observed that “If thalidomide had caused a 10-point loss of IQ instead of birth defects of the limbs, it would likely still be on the market” (Weiss 1982).
To begin formulation of a systematic strategy for discovery of potentially preventable environmental causes of autism and other NDDs, the Mount Sinai Children’s Environmental Health Center, with the support of the NIEHS and Autism Speaks, convened a workshop on “Exploring the Environmental Causes of Autism and Learning Disabilities.” This workshop produced a series of papers by leading researchers, some of which are published in this issue of Environmental Health Perspectives. It also generated a list of 10 chemicals and mixtures widely distributed in the environment that are already suspected of causing developmental neurotoxicity:
Lead (Jusko et al. 2008)
Methylmercury (Oken et al. 2008)
Polychlorinated biphenyls (Winneke 2011)
Organochlorine pesticides (Eskenazi et al. 2008)
Automotive exhaust (Volk et al. 2011)
Polycyclic aromatic hydrocarbons (Perera et al. 2009)
Brominated flame retardants (Herbstman et al. 2010)
Perfluorinated compounds (Stein and Savitz 2011).
This list is not exhaustive and will almost certainly expand in the years ahead as new science emerges. It is intended to focus research in environmental causation of NDDs on a short list of chemicals where concentrated study has high potential to generate actionable findings in the near future. Its ultimate purpose is to catalyze new evidence-based programs for prevention of disease in America’s children.References
- Anway MD, Skinner MK. 2006. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 147(6): supplS43–S49. Find this article online
- Arndt TL, Stodgell CJ, Rodier PM. 2005. The teratology of autism. Int J Dev Neurosci 23:189–199. Find this article online
- Autism Genome Project Consortium, Szatmari P, Paterson AD, Zwaigenbaum L, Roberts W, Brian J, et al 2007. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 39:319–328. Find this article online
- Braun JM, Kalkbrenner AE, Calafat AM, Yolton K, Ye X, Dietrich KN, et al. 2011. Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics 128(5):873–882. Find this article online
- Buxbaum JD, Hof PR. 2011. The emerging neuroscience of autism spectrum disorders. Brain Res 1380:1–2. Find this article online
- CDC (Centers for Disease Control and Prevention) 2005. Mental health in the United States. Prevalence of diagnosis and medication treatment for attention-deficit/hyperactivity disorder–United States, 2003. MMWR Morb Mortal Wkly Rep 54:842–847. Find this article online
- CDC (Centers for Disease Control and Prevention) 2012. Prevalence of autism spectrum disorders—autism and developmental disabilities monitoring network, 14 sites, United States, 2008. MMWR Surveill Summ 61(3):1–19. Find this article online
- Daniels JL. 2006. Autism and the environment. Environ Health Perspect 114:A396.. Find this article online
- Eskenazi B, Marks AR, Bradman A, Harley K, Barr DB, Johnson C, et al. 2007. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ Health Perspect 115:792–798. Find this article online
- Eskenazi B, Rosas LG, Marks AR, Bradman A, Harley K, Holland N, et al. 2008. Pesticide toxicity and the developing brain. Basic Clin Pharmacol Toxicol 102(2):228–236. Find this article online
- Fernandez TV, Sanders SJ, Yurkiewicz IR, Ercan-Sencicek AG, Kim YS, Fishman DO, et al. 2012. Rare copy number variants in tourette syndrome disrupt genes in histaminergic pathways and overlap with autism. Biol Psychiatry 71(5):392–402. Find this article online
- Goldman LR. 1998. Chemicals and children’s environment: what we don’t know about risks. Environ Health Perspect 106: suppl 3875–880. Find this article online
- Grafodatskaya D, Chung B, Szatmari P, Weksberg R.. 2010. Autism spectrum disorders and epigenetics. J Am Acad Child Adolesc Psychiatry 49(8):794–809. Find this article online
- Grandjean P, Landrigan PJ. 2006. Developmental neurotoxicity of industrial chemicals: a silent pandemic. Lancet 368(9553):2167–2178. Find this article online
- Grosse SD, Matte TD, Schwartz J, Jackson RJ. 2002. Economic gains resulting from the reduction in children’s exposure to lead in the United States. Environ Health Perspect 110:563–569. Find this article online
- Herbstman JB, Sjödin A, Kurzon M, Lederman SA, Jones RS, Rauh V, et al. 2010. Prenatal exposure to PBDEs and neurodevelopment. Environ Health Perspect 118:712–719. Find this article online
- Jusko TA, Henderson CR Jr, Lanphear BP, Cory-Slechta DA, Parsons PJ, Canfield RL. 2008. Blood lead concentrations < 10 µg/dL and child intelligence at 6 years of age. Environ Health Perspect 116:243–248. Find this article online
- Khan K, Factor-Litvak P, Wasserman GA, Liu X, Ahmed E, Parvez F, et al. 2011. Manganese exposure from drinking water and children’s classroom behavior in Bangladesh. Environ Health Perspect 119:1501–1506. Find this article online
- Landrigan PJ, Goldman LR. 2011. Children’s vulnerability to toxic chemicals: a challenge and opportunity to strengthen health and environmental policy. Health Aff 30(5):842–850. Find this article online
- London L, Beseler C, Bouchard MF, Bellinger DC, Colosio C, Grandjean P, et al. 2012. Neurotoxicology. Neurobehavioral and neurodevelopmental effects of pesticide exposures. http://dx.doi.org/10.1016/j.neuro.2012.01.004 [Online 17 January 2012].
- Miodovnik A.. 2011. Environmental neurotoxicants and developing brain. Mt Sinai J Med 78(1):58–77. Find this article online
- Miodovnik A, Engel SM, Zhu C, Ye X, Soorya LV, Silva MJ, et al. 2011. Endocrine disruptors and childhood social impairment. Neurotoxicology 32(2):261–267. Find this article online
- National Research Council 2000. Scientific Frontiers in Developmental Toxicology and Risk Assessment. Washington, DC:National Academy Press:
- Oken E, Radesky JS, Wright RO, Bellinger DC, Amarasiriwardena CJ, Kleinman KP, et al. 2008. Maternal fish intake during pregnancy, blood mercury levels, and child cognition at age 3 years in a US cohort. Am J Epidemiol 167(10):1171–1181. Find this article online
- O’Roak BJ, Deriziotis P, Lee C, Vives L, Schwartz JJ, Girirajan S, et al. 2011. Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat Genet 43:585–589. Find this article online
- Pastor PN, Reuben CA. 2008. Diagnosed attention deficit hyperactivity disorder and learning disability: United States, 2004–2006. Vital Health Stat 10 (237):1–14. Find this article online
- Perera FP, Li Z, Whyatt R, Hoepner L, Wang S, Camann D, et al. 2009. Prenatal airborne polycyclic aromatic hydrocarbon exposure and child IQ at age 5 years. Pediatrics. 124(2):pp. e195–e202. [Online 20 July 2009)
- Sakurai T, Cai G, Grice DE, Buxbaum JD 2011. Genomic architecture of autism spectrum disorders. In: Textbook of Autism Spectrum Disorders (Hollander E, Kolevzon A, Coyle JT. eds). Washington, DC:American Psychiatric Publishing: pp. 281–298.
- Stein CR, Savitz DA. 2011. Serum perfluorinated compound concentration and attention deficit/hyperactivity disorder in children 5–18 years of age. Environ Health Perspect 119:1466–1471. Find this article online
- Trasande L, Liu Y.. 2011. Reducing the staggering costs of environmental disease in children, estimated at $76.6 billion in 2008. Health Aff 30(5):863–870. Find this article online
- Volk HE, Hertz-Picciotto I, Delwiche L, Lurmann F, McConnell R. 2011. Residential proximity to freeways and autism in the CHARGE Study. Environ Health Perspect 119:873–877. Find this article online
- Wasserman GA, Liu X, Parvez F, Ahsan H, Factor-Litvak P, Kline J, et al. 2007. Water arsenic exposure and intellectual function in 6-year-old children in Araihazar, Bangladesh. Environ Health Perspect 115:285–289. Find this article online
- Waterland RA, Jirtle RL. 2004. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20:63–68. Find this article online
- Weiss B.. 1982. Food additives and environmental chemicals as sources of childhood behavior disorders. J Am Acad Child Psychiatry 21:144–152. Find this article online
- Winneke G.. 2011. Developmental aspects of environmental neurotoxicology: lessons from lead and polychlorinated biphenyls. J Neurol Sci 308(1-2):9–15. Find this article online
- Woodruff TJ, Zota AR, Schwartz JM. 2011. Environmental chemicals in pregnant women in the United States: NHANES 2003–2004. Environ Health Perspect 119:878–885. Find this article online
This study examined the association between autism and proximity of residence to freeways and major roadways during pregnancy and near the time of delivery, as a surrogate for air pollution exposure.
This research article, written by Heather E. Volk, Irva Hertz-Picciotto, Lora Delwiche, Fred Lurmann, and Rob McConnell* appeared first in Environmental Health Perspectives—the peer-reviewed, open access journal of the National Institute of Environmental Health Sciences.
Autism in the CHARGE Study Abstract
Background: Little is known about environmental causes and contributing factors for autism. Basic science and epidemiologic research suggest that oxidative stress and inflammation may play a role in disease development. Traffic-related air pollution, a common exposure with established effects on these pathways, contains substances found to have adverse prenatal effects.
Objectives: We examined the association between autism and proximity of residence to freeways and major roadways during pregnancy and near the time of delivery, as a surrogate for air pollution exposure.
Methods: Data were from 304 autism cases and 259 typically developing controls enrolled in the Childhood Autism Risks from Genetics and the Environment (CHARGE) study. The mother’s address recorded on the birth certificate and trimester-specific addresses derived from a residential history obtained by questionnaire were geocoded, and measures of distance to freeways and major roads were calculated using ArcGIS software. Logistic regression models compared residential proximity to freeways and major roads for autism cases and typically developing controls.
Results: Adjusting for sociodemographic factors and maternal smoking, maternal residence at the time of delivery was more likely be near a freeway (≤ 309 m) for cases than for controls [odds ratio (OR) = 1.86; 95% confidence interval (CI), 1.04–3.45]. Autism was also associated with residential proximity to a freeway during the third trimester (OR = 2.22; CI, 1.16–4.42). After adjustment for socioeconomic and sociodemographic characteristics, these associations were unchanged. Living near other major roads at birth was not associated with autism.
Conclusions: Living near a freeway was associated with autism. Examination of associations with measured air pollutants is needed.Keywords: autism, epidemiology, gene–environment interaction, roadway proximity, traffic emissions.
Autism is a developmental disorder characterized by significant deficits in social interaction and communication, accompanied by repetitive behaviors (American Psychiatric Association 2000). Data from family and twin studies have long supported the role of genetics in autism etiology (Abrahams and Geschwind 2008; Muhle et al. 2004). Results from linkage, copy number variation, and genomewide association studies further support the importance of genetic risk in this disease (Abrahams and Geschwind 2008; Ma et al. 2009; Wang et al. 2009). Over the last 10 years, the prevalence of diagnoses of autism, and all autism spectrum disorders, has increased (Centers for Disease Control and Prevention 2007a, 2007b, 2009). Although changes in diagnostic criteria and improved ascertainment have been thought to contribute to this increase, recent reports suggest that these factors may not fully explain the rising incidence of autism spectrum disorders (Hertz-Picciotto and Delwiche 2009; King and Bearman 2009). Therefore, it is likely that environmental factors may augment the strong genetic risks implicated in autism etiology.
Air pollution exposure during pregnancy has been reported to have physical and developmental effects on the fetus. High levels of air pollution, including carbon monoxide, nitrogen dioxide, and ambient particulate matter (PM), have been associated with very low and low birth weight, preterm birth, and infant mortality (Currie et al. 2009; Ritz and Yu 1999). Specific pollutants, including ozone, sulfur dioxide, PM, and carbon monoxide, have also been associated with significant differences in biparietal diameter and head circumference measured both during pregnancy and at birth (Hansen et al. 2008; Vassilev et al. 2001). Maternal exposure to polycyclic aromatic hydrocarbons (PAHs) during pregnancy has been associated with impaired cortical function and cognitive developmental delay (Bocskay et al. 2005; Perera et al. 2003, 2004, 2006, 2007).
Exposure to air pollution and its components, not only in the prenatal period but also in early postnatal life, has been linked to poor developmental outcomes as well. A recent epidemiologic study reported that use of gas appliances and increased nitrogen dioxide in the home during the first 3 months of life are associated with decreased cognitive test scores and increased inattention at 4 years of age (Morales et al. 2009). In a separate study, Suglia et al. (2008) estimated lifetime residential exposure to black carbon, a proxy for traffic-related PM, among 8- to 11-year-old children and reported decreased performance on intelligence and memory tasks with increasing black carbon levels. Additionally, autism has been associated with estimated regional concentrations of hazardous air pollutants, including arsenic and nickel, and with diesel PM exposure in early childhood (Windham et al. 2006).
Thus, an emerging literature suggests that near roadways, traffic-related air pollutants, possibly influenced by specific components such as PM or PAHs, affect neurodevelopment. However, the role of timing for this exposure during pregnancy or early life is not clear, nor has the relationship between traffic-related air pollutants and autism been tested. In this study, we examined the relationship between autism and traffic proximity (a marker of traffic-related air pollution) during the prenatal period and at the time of birth.Materials and Methods
We used data from 304 autism cases and 259 typically developing general-population controls from the Childhood Autism Risks from Genetics and the Environment (CHARGE) study, a population-based case–control study of preschool children. The study design is described in detail elsewhere (Hertz-Picciotto et al. 2006). Briefly, CHARGE subjects were between 24 and 60 months of age at the time of recruitment, which occurred during 2003–2009; lived with at least one English- or Spanish-speaking biological parent; were born in California; and resided in one of the study catchment areas at the time of enrollment. Recruitment was facilitated by the California Department of Developmental Services (DDS) and the regional centers with which they contract to coordinate services for persons with autism and other developmental disabilities. Population-based controls were recruited from the sampling frame of birth files from the State of California and were frequency matched by sex, age, and broad geographic area to the autism cases. All births were between 1997 and 2006.
Each participating family was evaluated in person. Children with a DDS diagnosis of autism were evaluated using the Autism Diagnostic Observation Schedules (ADOS), and parents were administered the Autism Diagnostic Interview–Revised (ADI-R) (Le Couteur et al. 2003; Lord et al. 2003). Children with a diagnosed developmental delay and general population controls were given the Social Communication Questionnaire (SCQ) to screen for the presence of autistic features (Rutter et al. 2003). If the SCQ score was ≥ 15, the ADOS was then administered to the child and the ADI-R to the parent. In our study, autism cases were children with a diagnosis of autism from both the ADOS and the ADI-R. All children were also assessed using the Mullen Scales of Early Learning and the Vineland Adaptive Behavior Scales to collect information on motor skills, language, socialization, and daily living skills (Mullen 1995; Sparrow et al. 1984). Controls were children sampled from the general population with typical development, defined as having received a score ≤ 15 on the SCQ and who scored in the normal range on the Mullen Scales of Early Learning and Vineland Adaptive Behavior Scales, thereby showing no evidence of other types of delay (cognitive or adaptive).
Parents were also interviewed extensively to evaluate household exposures and demographic and medical information and to assess reproductive, occupational, and residential histories. The residential history captured addresses and corresponding dates the mother and child lived at each location beginning 3 months before conception and extending to the most recent place of residence. Further details about the collection of clinical and exposure data have been previously reported (Hertz-Picciotto et al. 2006).
We examined associations of autism with traffic-related pollutant exposure using two broad proxies: distance to the nearest freeway and distance to the nearest major road. In accord with our previous research, a freeway was defined as a state highway or interstate highway (Gauderman et al. 2007). A major road was defined as a state highway, interstate highway, or major arterial (McConnell et al. 2006). Mother’s residential address at birth, as recorded on the birth certificate, was geocoded, and distances to the nearest interstate highway, state highway, and major arterial road were estimated based on the shortest distance from the residence to the middle of the nearest side of each of the three road types using ArcGIS software (version 9.2; Environmental Systems Research Institute Inc., Redlands, CA). For each subject, freeway distance was then assigned as the shorter of the distances from the birth residence to a state or interstate highway. Similarly, major road distance was assigned as the shortest of the three distances: from a state highway, interstate highway, or major arterial. Under these definitions, it was possible for freeway and major road distances to be the same should the same road type (e.g., state highway) provide the shortest distance measure for a given address. For freeway and major road distances, we examined the distribution of values among the 563 subjects in our study and determined exposure cut points based on the top 10%, next 15%, and subsequent 25% of distance values for freeways and for major roads. The remaining 50% served as a reference category in each analysis.
Information from the residential history was used to estimate exposure to residential traffic during the first, second, and third trimesters of gestation for a subset of subjects with complete data (n = 485; 257 cases and 228 controls). We determined the conception date for each child using gestational age from ultrasound measurements or the date of last menstrual period, as determined from prenatal records. Then we calculated dates corresponding to each trimester and selected the appropriate address from the residential history. If more than one address fell into a trimester, we chose the address where the subjects had spent the most time. Addresses were geocoded and distances estimated as described above.
We used logistic regression to estimate the association between distance to the nearest freeway or major road and autism. Pertinent covariates were included in the model to adjust for potential confounding due to sociodemographic or lifestyle characteristics. Specifically, we included child’s sex and ethnicity, maximum education level of the parents, maternal age, gestational age at birth, and maternal smoking during pregnancy. We obtained 95% confidence intervals (CIs) as measures of precision and determined statistical significance using an alpha level of 0.05.Results
Description of sample. The study population was 84% male, and most participants were Caucasian (51%) or Hispanic (29%). We found no significant differences between cases and controls for any demographic or socioeconomic variables examined (Table 1). For most participants, geocoded birth certificate addresses (mother’s residence at delivery) indicated that residences at birth were concentrated in the areas around Sacramento, Los Angeles, and the San Francisco East and North Bay.
Table 1. Click for Larger Image.
Demographic characteristics of CHARGE cases with autism and controls with typical development (n = 563).
Distance to freeway. We examined the distribution of distance from the nearest freeway among subjects in our study and determined exposure cut-points to define the closest 10% (< 309 m), the next 15% (309–647 m), and the next 25% (647–1,419 m) as exposure groups. The remaining 50% (> 1,419 m) served as the reference group in our analysis. Living within 309 m of a freeway at birth was associated with autism [odds ratio (OR) = 1.86; 95% CI, 1.04–3.45]. This association was not altered by adjustment for child sex or ethnicity, maximum education in the home, maternal age, or maternal smoking during pregnancy (Table 2). When we categorized our distance measure into deciles, only the top 10%, corresponding to the < 309-m category, showed evidence of an increased autism risk compared with those living farthest from the freeway (lowest decile, > 5,150 m; unadjusted OR = 2.48; 95% CI, 1.17–5.39).
Exposure ORs (95% CIs) for autism, by category of distance from residence to the nearest freeway at time of birth (n = 563).
Among the subset of subjects with available residential history data, measures for distance to the freeway were highly correlated across trimesters, reflecting the limited number of subjects who changed residence during pregnancy (n = 17 between first and second, 13 between second and third, 30 between first and third). In each trimester, living closest to the freeway (< 309 vs. > 1,419 m) was associated with autism, but the OR reached statistical significance only during the third trimester (adjusted OR = 1.96; 95% CI, 1.01–3.93). Effect estimates for the first and second trimesters were slightly lower in magnitude (first trimester: adjusted OR = 1.66; 95% CI, 0.91–3.10; second trimester: adjusted OR = 1.65; 95% CI, 0.85–3.28). After restricting the sample with birth certificate addresses to those with residential history data for all three trimesters (n = 485; 257 cases and 228 controls), the OR for autism was more than doubled among those living within 309 m of a freeway versus > 1,419 m (adjusted OR = 2.22; 95% CI, 1.16–4.42), consistent with a late-pregnancy or early-life effect.
Distance to major road. The distribution of distance from a major road among subjects in our study was reflected in exposure cut-points corresponding to ≤ 42 m (the closest 10%), 42–96 m (subsequent 15%), and 96–209 m (next 25%) as exposure groups. The remaining 50% (> 209 m) served as the reference group in our analysis. We found no consistent pattern of association of autism with proximity to a major road, and results were changed only slightly after adjusting for distance to the freeway (Table 3). Inclusion of child sex or ethnicity, maximum education in home, maternal age, or prenatal smoking in the model did not alter these associations. Results were similar for the three trimesters.
Table 3. Click for Larger Image.
Exposure ORs (95% CIs) for autism, by category of distance from residence to the nearest major road at time of birth (n = 563).
We observed an increased risk of autism among the 10% of children living within 309 m of a freeway around the time of birth. Our findings appeared to be limited to only this group because analysis of further distances did not demonstrate associations. Analysis of trimester-specific residential information yielded associations of roughly similar magnitude, although only the effects for the third trimester and at birth reached statistical significance. The high correlations across trimesters, and lack of analysis of postnatal residences, imply that we cannot precisely define a potentially critical window.
The association of autism with proximity to freeway, and not to major road, may be related to the larger volume of traffic and concentrations of pollutants observed near freeways. In Los Angeles, for example, some freeways have more than 300,000 vehicles daily and high concentrations of traffic-related pollutants with steep gradients extending several hundred meters from the traffic corridor (Caltrans 2008; Zhu et al. 2002, 2006). Specifically, studies measuring concentration and size distribution of ultrafine PM near a major California freeway demonstrate that the PM is high nearest the freeway and becomes closer to background levels at distances ≥ 300 m (Zhu et al. 2002). Thus, our findings are consistent with the relationship between freeway proximity and PM exposures in California. Our study did not find evidence of associations with residential proximity beyond the 300-m range, and we currently lack adequate sample size to estimate the effect of living in even closer proximity to the freeway (< 100 m) where high concentrations of PM have been detected. To examine the effects of proximity at closer distances to major roadways, we estimated autism risk among subjects living within 96 m (the top quartile of exposure vs. > 96 m) and among those living within 300 m (corresponding to the region of highest exposure vs. > 300 m) and found slightly elevated non-statistically significant risks (within 96 m: OR = 1.17; 95% CI, 0.80–1.72; within 300 m: OR = 1.19; 95% CI, 0.84–1.68).
The traffic volumes on the classes of other major roadways used in this analysis are likely to be highly variable across California, so exposure to traffic-related pollutants on the spatial scale of interest may be less well classified by residential proximity to other major roadways than by proximity to freeways. For example, we found that the average distance to a freeway among subjects living in the second major road exposure group (42–96 m), with slightly increased risk of autism, was much shorter (mean ± SD = 1,481 ± 1,761 m) than in other major road categories (major road < 42 m, 2,643 ± 2,245 m to freeway; major road 96–209 m, 1,917 ± 3,946 m). Residential traffic proximity has been associated with childhood asthma and lung function growth in previous studies we have conducted in Southern California, and some of these associations have been restricted to freeway proximity or traffic modeled from freeway traffic volume (Gauderman et al. 2005, 2007; McConnell et al. 2006, 2010).
We found little evidence of confounding by the socioeconomic and sociodemographic characteristics included in this analysis. We hypothesized these confounders a priori based on literature reporting increased autism rates in higher socioeconomic areas, whereas lower socioeconomic areas are more likely to have higher levels of air pollutants (Sexton et al. 1993). In our study, we observed no difference in level of education in the home among autism cases and controls, and adjusting for these factors had little effect on the traffic and autism association, suggesting that our results were not biased by such factors. In California, clusters of autism tend to have higher levels of parental education, and in countries with highly variable access to health care, diagnosed cases of autism tend to be in families with higher socioeconomic status than the general population; at the same time, controls that participate in studies are almost always of higher socioeconomic status than nonparticipants (Van Meter et al. 2010).
To date, little research has examined the association of air pollutants and autism. Using the U.S. Environmental Protection Agency Hazardous Air Pollutants monitoring network, Windham et al. (2006) identified an increased autism risk with modeled estimates of regional census tract ambient exposure to diesel exhaust particles, as well as metals (mercury, cadmium, and nickel) and chlorinated solvents, in the San Francisco Bay Area of northern California. Additional research using models from the Hazardous Air Pollutants program found associations between autism and air toxics at the birth residence of children from North Carolina and West Virginia (Kalkbrenner et al. 2010). Our analysis builds on this work by examining associations with individual-level indicators of exposure based on traffic proximity, prenatally and at birth.
Toxicologic studies suggest a biologically plausible role of air pollution in disrupting brain development and function during critical time points in gestation and early life. Diesel exhaust particles present in traffic-related pollution have been shown to have endocrine-disrupting activity and to transplacentally affect sexual differentiation and alter cognitive function in mice (Hougaard et al. 2008; Watanabe and Kurita 2001). Prenatal exposure to ozone in rats has been seen to alter monoamine content in the cerebellum, which may then alter neural circuitry formation (Gonzalez-Pina et al. 2008). Recent work examining the effects of benzo[a]pyrene, a common PAH, indicates that prenatal oral exposure in mice results in decreased neuronal plasticity and behavioral deficits (Brown et al. 2007). Specifically, prenatal exposure was associated with reduced glutamate receptor development when synapses are formed. Additionally, exposure to benzo[a]pyrene via breast-feeding in mice during the early postnatal period, corresponding to the rapid human brain development taking place during the third trimester, affected neuromaturation as measured by classic developmental behavior tests and to reduce expression of the serotonin receptor 5HT1A (Bouayed et al. 2009; Pan et al. 2009).
Traffic-related air pollutants have been observed to induce inflammation and oxidative stress after both short-term and long-term exposures in toxicologic and human studies, and these pathways are thought to mediate effects of air pollution on respiratory and cardiovascular disease, and perhaps on neurologic outcomes (Block and Calderon-Garciduenas 2009; Calderon-Garciduenas et al. 2009; Castro-Giner et al. 2009; Gilliland et al. 2004; Künzli et al. 2010). The emerging evidence that oxidative stress and inflammation are also involved in the pathogenesis of autism may suggest a biologically plausible rationale for the observed associations in our study (Boso et al. 2006; Enstrom et al. 2009a, 2009b; James et al. 2004, 2006, 2009). In particular, research examining serum biomarkers reported increased levels of the proinflammatory cytokines tumor necrosis factor-α, interleukin (IL)-6, IL-8, and colony-stimulating factor II, as well as two markers of T-helper 1 immune response (interferon-γ and IL-8), in postmortem brain tissue of autism cases compared with controls (Li et al. 2009). Additional research from the CHARGE study has shown increased plasma levels of immunoglobulin (Ig) G-4 and reduced concentrations of tumor growth factor-β, related to immune response and inflammatory processes, in plasma of children with autism compared with typically developing controls and children with developmental delay (Ashwood et al. 2008; Enstrom et al. 2009a, 2009b). Other recent work indicates that exposure to air pollution exposure during pregnancy is associated with changes in IgE and in lymphocytes measured from cord blood, supporting the idea that maternal exposure to air pollution is associated with altered immune profiles in the fetus (Herr et al. 2010a, 2010b). Moreover, published evidence links maternal antibodies to fetal brain tissue with a subset of autism cases (Braunschweig et al. 2008).
Genetic variation in oxidative stress and inflammatory pathways has also been associated with autism. Oxidative stress endophenotypes and corresponding genotypes related to metabolism of methionine transmethylation and transsulfuration were significantly decreased in children with autism compared with controls, indicating increased susceptibility to oxidative stress (Boso et al. 2006; James et al. 2004, 2006). Markers of lipid peroxidation have also been associated with autism, as have increased levels of nitric oxide and mitochondrial dysfunction, which may be related to the formation of reactive oxygen species (Chauhan and Chauhan 2006; Filipek et al. 2004; Ming et al. 2005; Sogut et al. 2003; Yao et al. 2006). Polymorphisms in glutathione S-transferase mu 1 (GSTM1), glutathione S-transferase pi 1 (GSTP1), and glutathione peroxidase 1 (GPX1), which modulate the response to oxidative stress, have been associated with increased autism risk (Buyske et al. 2006; Ming et al. 2009; Williams et al. 2007). These genetic variants have also been shown to modify the association between exposure to air oxidant pollutant associations and respiratory outcomes (Islam et al. 2009; Salam et al. 2007). Examination of the interaction between these oxidant-associated genes and environmental exposures may help to clarify susceptibilities to environmental pollutants among children with autism.
We recognize that the moderate relative risks associated with freeway proximity in our study may have been attributable to chance or bias. The study is currently limited by sample size and potential exposure misclassification. Analysis of larger data sets would provide additional valuable insight into these findings and the potential for replication. Although we used a residential history questionnaire (available for a subset of the study participants) to choose the appropriate address for trimester, there still may be misclassification of exposure in these data due to inaccurate date reporting on the part of the mother, or in our choice among multiple addresses in each trimester. We could not distinguish the potential effect of noise from that due to pollutant exposures, both resulting from residential location near a freeway or other road in this study. Addresses on the birth certificate could also be in error, but this would probably be less likely. We were not able to examine specific pollutant concentrations in this study, and the traffic proximity metrics were subject to misclassification of exposure because they did not account for traffic volume or prevailing wind speed and direction. However, this exposure misclassification was unlikely to have been systematically related to disease, and our results may therefore have underestimated the magnitude of a true causal association.
Despite these limitations, this study has several strengths. We assessed autism through well-validated instruments that are recognized as the gold standard in the field. We examined exposure prenatally and at birth, two pivotal times in gestational development, whereas prior work on air pollution has been limited to the birth address or a cumulative lifetime exposure measure. To our knowledge, these results are the first to show an association of autism with residential traffic proximity.Conclusions
Little is known about potential environmental contributions to autism. The observed associations with traffic proximity merit further research to determine whether these results are reproducible in populations with improved estimates of exposure to specific ambient air pollutants. Examination of gene–pollution interactions may also help us learn about causal pathways involved in autism and identify potentially susceptible populations and may lead to prevention strategies. Our analysis is the first step in examining a hypothesized relationship between air pollutants and autism. It has been estimated that 11% of the U.S. population lives within 100 m of a four-lane highway, so a causal link to autism or other neurodevelopmental disorders would have broad public health implications (Brugge et al. 2007).References
- Abrahams BS, Geschwind DH. 2008. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 9(5):341–355. Find this article online
- American Psychiatric Association 2000. Diagnostic and Statistical Manual of Mental Disorders. 4th ed, Text RevisionWashington, DC: American Psychiatric Association.
- Ashwood P, Enstrom A, Krakowiak P, Hertz-Picciotto I, Hansen RL, Croen LA, et al. 2008. Decreased transforming growth factor beta1 in autism: a potential link between immune dysregulation and impairment in clinical behavioral outcomes. J Neuroimmunol 204(1–2):149–153. Find this article online
- Block ML, Calderon-Garciduenas L. 2009. Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci 32(9):506–516. Find this article online
- Bocskay KA, Tang D, Orjuela MA, Liu X, Warburton DP, Perera FP. 2005. Chromosomal aberrations in cord blood are associated with prenatal exposure to carcinogenic polycyclic aromatic hydrocarbons. Cancer Epidemiol Biomarkers Prev 14(2):506–511. Find this article online
- Boso M, Emanuele E, Minoretti P, Arra M, Politi P, Ucelli di Nemi S, et al. 2006. Alterations of circulating endogenous secretory RAGE and S100A9 levels indicating dysfunction of the AGE-RAGE axis in autism. Neurosci Lett 410(3):169–173. Find this article online
- Bouayed J, Desor F, Rammal H, Kiemer AK, Tybl E, Schroeder H, et al. 2009. Effects of lactational exposure to benzo[alpha]pyrene (B[alpha]P) on postnatal neurodevelopment, neuronal receptor gene expression and behaviour in mice. Toxicology 259(3):97–106. Find this article online
- Braunschweig D, Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Croen LA, et al. 2008. Autism: maternally derived antibodies specific for fetal brains. Neurotoxicology 29(2):226–231. Find this article online
- Brown LA, Khousbouei H, Goodwin JS, Irvin-Wilson CV, Ramesh A, Sheng L, et al. 2007. Down-regulation of early ionotrophic glutamate receptor subunit developmental expression as a mechanism for observed plasticity deficits following gestational exposure to benzo(a)pyrene. Neurotoxicology 28(5):965–978. Find this article online
- Brugge D, Durant JL, Rioux C. 2007. Near-highway pollutants in motor vehicle exhaust: a review of epidemiologic evidence of cardiac and pulmonary health risks. Environ Health 6:23.doi:10.1186/1476-069X-6-23 Find this article online
- Buyske S, Williams TA, Mars AE, Stenroos ES, Ming SX, Wang R, et al. 2006. Analysis of case-parent trios at a locus with a deletion allele: association of GSTM1 with autism. BMC Genet 7:8.; doi: 10.1186/1471-2156-7-8 Find this article online
- Calderon-Garciduenas L, Macias-Parra M, Hoffmann HJ, Valencia-Salazar G, Henriquez-Roldan C, Osnaya N, et al. 2009. Immunotoxicity and environment: immunodysregulation and systemic inflammation in children. Toxicol Pathol 37(2):161–169. Find this article online
- Caltrans 2008. Traffic and Vehicle Data Systems Unit: All Traffic Volumes on the California State Highway System. Available: http://www.dot.ca.gov/hq/traffops/saferesr/trafdata/2008all.htm [accessed 27 July 2010]
- Castro-Giner F, Künzli N, Jacquemin B, Forsberg B, de Cid R, Sunyer J, et al. 2009. Traffic-related air pollution, oxidative stress genes, and asthma (ECHRS). Environ Health Perspect 117:1919–1924. Find this article online
- Centers for Disease Control and Prevention 2007. . Prevalence of autism spectrum disorders—autism and developmental disabilities monitoring network, 14 sites, United States, 2002. MMWR Surveill Summ 56(1):12–28. Find this article online
- Centers for Disease Control and Prevention 2007. . Prevalence of autism spectrum disorders—autism and developmental disabilities monitoring network, six sites, United States, 2000. MMWR Surveill Summ 56(1):1–11. Find this article online
- Centers for Disease Control and Prevention 2009. Prevalence of autism spectrum disorders—autism and developmental disabilities monitoring network, United States, 2006. MMWR Surveill Summ 58(10):1–20. Find this article online
- Chauhan A, Chauhan V.. 2006. Oxidative stress in autism. Pathophysiology 13(3):171–181. Find this article online
- Currie J, Neidell M, Schmieder JF. 2009. Air pollution and infant health: lessons from New Jersey. J Health Econ 28(3):688–703. Find this article online
- Enstrom A, Krakowiak P, Onore C, Pessah IN, Hertz-Picciotto I, Hansen RL, et al. 2009. . Increased IgG4 levels in children with autism disorder. Brain Behav Immun 23(3):389–395. Find this article online
- Enstrom AM, Lit L, Onore CE, Gregg JP, Hansen RL, Pessah IN, et al. 2009. . Altered gene expression and function of peripheral blood natural killer cells in children with autism. Brain Behav Immun 23(1):124–133. Find this article online
- Filipek PA, Juranek J, Nguyen MT, Cummings C, Gargus JJ. 2004. Relative carnitine deficiency in autism. J Autism Dev Disord 34(6):615–623. Find this article online
- Gauderman WJ, Avol E, Lurmann F, Kuenzli N, Gilliland F, Peters J, et al. 2005. Childhood asthma and exposure to traffic and nitrogen dioxide. Epidemiology 16(6):737–743. Find this article online
- Gauderman WJ, Vora H, McConnell R, Berhane K, Gilliland F, Thomas D, et al. 2007. Effect of exposure to traffic on lung development from 10 to 18 years of age: a cohort study. Lancet 369(9561):571–577. Find this article online
- Gilliland FD, Li YF, Saxon A, Diaz-Sanchez D. 2004. Effect of glutathione-S-transferase M1 and P1 genotypes on xenobiotic enhancement of allergic responses: randomised, placebo-controlled crossover study. Lancet 363(9403):119–125. Find this article online
- Gonzalez-Pina R, Escalante-Membrillo C, Alfaro-Rodriguez A, Gonzalez-Maciel A.. 2008. Prenatal exposure to ozone disrupts cerebellar monoamine contents in newborn rats. Neurochem Res 33(5):912–918. Find this article online
- Hansen CA, Barnett AG, Pritchard G. 2008. The effect of ambient air pollution during early pregnancy on fetal ultrasonic measurements during mid-pregnancy. Environ Health Perspect 116:362–369. Find this article online
- Herr CEW, Dostal M, Ghosh R, Ashwood P, Lipsett M, Pinkerton KE, et al. 2010. . Air pollution exposure during critical time periods in gestation and alterations in cord blood lymphocyte distribution: a cohort of livebirths. Environ Health 9:46.; doi: 10.1186/1476-069X-9-46 Find this article online
- Herr CEW, Ghosh R, Dostal M, Skokanova V, Ashwood P, Lipsett M, et al. 2010. . Exposure to air pollution in critical prenatal time windows and IgE levels in newborns. Pediatr Allergy Immunol. doi:10.1111/j.1399-3038.2010.01074.x Find this article online
- Hertz-Picciotto I, Croen LA, Hansen R, Jones CR, van de Water J, Pessah IN. 2006. The CHARGE study: an epidemiologic investigation of genetic and environmental factors contributing to autism. Environ Health Perspect 114:1119–1125. Find this article online
- Hertz-Picciotto I, Delwiche L.. 2009. The rise in autism and the role of age at diagnosis. Epidemiology 20(1):84–90. Find this article online
- Hougaard KS, Jensen KA, Nordly P, Taxvig C, Vogel U, Saber AT, et al. 2008. Effects of prenatal exposure to diesel exhaust particles on postnatal development, behavior, genotoxicity and inflammation in mice. Part Fibre Toxicol 5:3.; doi: 10.1186/1743-8977-5-3 Find this article online
- Islam T, Berhane K, McConnell R, Gauderman WJ, Avol E, Peters JM, et al. 2009. Glutathione-S-transferase (GST) P1, GSTM1, exercise, ozone and asthma incidence in school children. Thorax 64(3):197–202. Find this article online
- James SJ, Cutler P, Melnyk S, Jernigan S, Janak L, Gaylor DW, et al. 2004. Metabolic biomarkers of increased oxidative stress and impaired methylation capacity in children with autism. Am J Clin Nutr 80(6):1611–1617. Find this article online
- James SJ, Melnyk S, Jernigan S, Cleves MA, Halsted CH, Wong DH, et al. 2006. Metabolic endophenotype and related genotypes are associated with oxidative stress in children with autism. Am J Med Genet B Neuropsychiatr Genet 141B(8):947–956. Find this article online
- James SJ, Rose S, Melnyk S, Jernigan S, Blossom S, Pavliv O, et al. 2009. Cellular and mitochondrial glutathione redox imbalance in lymphoblastoid cells derived from children with autism. FASEB J 23(8):2374–2383. Find this article online
- Kalkbrenner AE, Daniels JL, Chen JC, Poole C, Emch M, Morrissey J. 2010. Perinatal exposure to hazardous air pollutants and autism spectrum disorders at age 8. Epidemiology 21(5):631–641. Find this article online
- King M, Bearman P.. 2009. Diagnostic change and the increased prevalence of autism. Int J Epidemiol 38(5):1224–1234. Find this article online
- Künzli N, Jerrett M, Garcia-Esteban R, Basagana X, Beckermann B, Gilliland F, et al. 2010. Ambient air pollution and the progression of atherosclerosis in adults. PLoS One 5(2):e9096.. Find this article online
- Le Couteur A, Lord C, Rutter M 2003. Autism Diagnostic Interview–Revised (ADI-R). Los Angeles: Western Psychological Services.
- Li X, Chauhan A, Sheikh AM, Patil S, Chauhan V, Li XM, et al. 2009. Elevated immune response in the brain of autistic patients. J Neuroimmunol 207(1–2):111–116. Find this article online
- Lord C, Rutter M, DiLavore P, Risi S 2003. Autism Diagnostic Observation Schedule Manual. Los Angeles: Western Psychological Services.
- Ma D, Salyakina D, Jaworski JM, Konidari I, Whitehead PL, Andersen AN, et al. 2009. A genome-wide association study of autism reveals a common novel risk locus at 5p14.1. Ann Hum Genet 73(pt 3):263–273. Find this article online
- McConnell R, Berhane K, Yao L, Jerrett M, Lurmann F, Gilliland F, et al. 2006. Traffic, susceptibility, and childhood asthma. Environ Health Perspect 114:766–772. Find this article online
- McConnell R, Islam T, Shankardass K, Jerrett M, Lurmann F, Gilliland F, et al. 2010. Childhood incident asthma and traffic-related air pollution at home and school. Environ Health Perspect 118:1021–1026. Find this article online
- Ming X, Johnson WG, Stenroos ES, Mars A, Lambert GH, Buyske S. 2009. Genetic variant of glutathione peroxidase 1 in autism. Brain Dev 32(2):105–109. Find this article online
- Ming X, Stein TP, Brimacombe M, Johnson WG, Lambert GH, Wagner GC. 2005. Increased excretion of a lipid peroxidation biomarker in autism. Prostaglandins Leukot Essent Fatty Acids 73(5):379–384. Find this article online
- Morales E, Julvez J, Torrent M, de Cid R, Guxens M, Bustamante M, et al. 2009. Association of early-life exposure to household gas appliances and indoor nitrogen dioxide with cognition and attention behavior in preschoolers. Am J Epidemiol 169(11):1327–1336. Find this article online
- Muhle R, Trentacoste SV, Rapin I. 2004. The genetics of autism. Pediatrics 113(5):e472–e486. Find this article online
- Mullen E 1995. Mullen Scales of Early Learning. Circle Pines, MN: American Guidance Services Inc.
- Pan IJ, Daniels JL, Goldman BD, Herring AH, Siega-Riz AM, Rogan WJ. 2009. Lactational exposure to polychlorinated biphenyls, dichlorodiphenyltrichloroethane, and dichlorodiphenyldichloroethylene and infant neurodevelopment: an analysis of the pregnancy, infection, and nutrition babies study. Environ Health Perspect 117:488–494. Find this article online
- Perera FP, Rauh V, Tsai WY, Kinney P, Camann D, Barr D, et al. 2003. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect 111:201–205. Find this article online
- Perera FP, Rauh V, Whyatt RM, Tsai WY, Bernert JT, Tu YH, et al. 2004. Molecular evidence of an interaction between prenatal environmental exposures and birth outcomes in a multiethnic population. Environ Health Perspect 112:626–630. Find this article online
- Perera FP, Rauh V, Whyatt RM, Tsai WY, Tang D, Diaz D, et al. 2006. Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ Health Perspect 114:1287–1292. Find this article online
- Perera FP, Tang D, Rauh V, Tu YH, Tsai WY, Becker M, et al. 2007. Relationship between polycyclic aromatic hydrocarbon–DNA adducts, environmental tobacco smoke, and child development in the World Trade Center cohort. Environ Health Perspect 115:1497–1502. Find this article online
- Ritz B, Yu F.. 1999. The effect of ambient carbon monoxide on low birth weight among children born in Southern California between 1989 and 1993. Environ Health Perspect 107:17–25. Find this article online
- Rutter M, Bailey A, Lord C 2003. A Social Communication Questionnaire (SCQ). Los Angeles: Western Psychological Services.
- Salam MT, Lin PC, Avol EL, Gauderman WJ, Gilliland FD. 2007. Microsomal epoxide hydrolase, glutathione S-transferase P1, traffic and childhood asthma. Thorax 62(12):1050–1057. Find this article online
- Sexton K, Gong H Jr, Bailar JC III, Ford JG, Gold DR, Lambert WE, et al. 1993. Air pollution health risks: do class and race matter? Toxicol Ind Health 9(5):843–878. Find this article online
- Sogut S, Zoroglu SS, Ozyurt H, Yilmaz HR, Ozugurlu F, Sivasli E, et al. 2003. Changes in nitric oxide levels and antioxidant enzyme activities may have a role in the pathophysiological mechanisms involved in autism. Clin Chim Acta 331(1–2):111–117. Find this article online
- Sparrow S, Cicchettim D, Balla D 1984. Vineland Adaptive Behavior Scales Interview Edition Expanded Form Manual. Circle Pines, MN: American Guidance Services Inc.
- Suglia SF, Gryparis A, Wright RO, Schwartz J, Wright RJ. 2008. Association of black carbon with cognition among children in a prospective birth cohort study. Am J Epidemiol 167(3):280–286. Find this article online
- Van Meter KC, Christiansen LE, Delwiche LD, Azari R, Carpenter TE, Hertz-Picciotto I. 2010. Geographic distribution of autism in California: a retrospective birth cohort analysis. Autism Res 3(1):19–29. Find this article online
- Vassilev ZP, Robson MG, Klotz JB. 2001. Outdoor exposure to airborne polycyclic organic matter and adverse reproductive outcomes: a pilot study. Am J Ind Med 40(3):255–262. Find this article online
- Wang K, Zhang H, Ma D, Bucan M, Glessner JT, Abrahams BS, et al. 2009. Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 459(7246):528–533. Find this article online
- Watanabe N, Kurita M.. 2001. The masculinization of the fetus during pregnancy due to inhalation of diesel exhaust. Environ Health Perspect 109:111–119. Find this article online
- Williams TA, Mars AE, Buyske SG, Stenroos ES, Wang R, Factura-Santiago MF, et al. 2007. Risk of autistic disorder in affected offspring of mothers with a glutathione S-transferase P1 haplotype. Arch Pediatr Adolesc Med 161(4):356–361. Find this article online
- Windham GC, Zhang L, Gunier R, Croen LA, Grether JK. 2006. Autism spectrum disorders in relation to distribution of hazardous air pollutants in the San Francisco Bay Area. Environ Health Perspect 114:1438–1444. Find this article online
- Yao Y, Walsh WJ, McGinnis WR, Pratico D. 2006. Altered vascular phenotype in autism: correlation with oxidative stress. Arch Neurol 63(8):1161–1164. Find this article online
- Zhu Y, Hinds WC, Kim S, Sioutas C. 2002. Concentration and size distribution of ultrafine particles near a major highway. J Air Waste Manag Assoc 52(9):1032–1042. Find this article online
- Zhu Y, Kuhn T, Mayo P, Hinds WC. 2006. Comparison of daytime and nighttime concentration profiles and size distributions of ultrafine particles near a major highway. Environ Sci Technol 40(8):2531–2536. Find this article online
- Citation: Volk HE, Hertz-Picciotto I, Delwiche L, Lurmann F, McConnell R 2011. Residential Proximity to Freeways and Autism in the CHARGE Study. Environ Health Perspect 119:873-877. http://dx.doi.org/10.1289/ehp.1002835
- Received: 06 August 2010; Accepted: 13 December 2010; Online: 16 December 2010
- Address correspondence to H.E. Volk, Keck School of Medicine, University of Southern California, 1540 Alcazar St. CHP 209G, Los Angeles, CA 90033 USA. Telephone: (323) 442-5101. Fax: (323) 442-3272. E-mail: firstname.lastname@example.org
- This work was supported by National Institute of Environmental Health Sciences grants ES019002, ES009581, ES013578, ES007048, ES11269, ES015359, and RD831861; U.S. Environmental Protection Agency Science to Achieve Results (STAR) grants R-823392 and R-833292; the MIND Institute matching funds and pilot grant program; and Autism Speaks.
- F.L. is employed by Sonoma Technology Inc., which provided expert services in exposure assessment for this work. The other authors declare they have no actual or potential competing financial interests. The authors declare they have no actual or potential competing financial interests.
There are thirteen ecoregions in Angola:
- Kaokoveld desert
- Namibian savanna woodlands
- Angolan Mopane woodlands
- Zambezian Baikiaea woodlands
- Western Zambezian grasslands
- Zambezian Cryptosepalum dry forests
- Angolan Miombo woodlands
- Angolan montane forest-grassland mosaic
- Angolan scarp savanna and woodlands
- Western Congolian forest-savanna mosaic
- Southern Congolian forest savanna mosaic
- Central Zambezian Miombo woodlands
- Central African mangroves
The Kaokoveld Desert stretches along the west coast of southern Africa between about 13 and 21S latitude. Encompassing the northern Namib Desert, the ecoregion extends from the Uniab River in Namibia northwards into the coastal zone of southern Angola, including the Mossamedes Desert. For most of its length, it is about 100 kilometers (km) wide and extends from the Atlantic Coastline to the foot of the great escarpment, which delimits the interior highlands of southern Africa.
The Kaokoveld Desert represents the northern area of the vast Namib Desert. It is a harsh, arid landscape of rugged mountains, gravel plains and shifting sand dunes. Surface water is scarce, with only one perennial river flowing through the region, the Kunene River. However, the dry riverbeds transecting the area are the lifelines of the desert. They are well vegetated and are home to large mammals such as elephants, black rhinos and giraffes. The rest of the landscape is poorly vegetated and extremely dry. Coastal fogs allow a range of interesting, desert-adapted animal species to survive in this low-rainfall environment. The relict gymnosperm Welwitschia mirabilis, which represents the sole surviving member of its family, is found throughout the ecoregion. The Kaokoveld Desert is well protected in the Skeleton Coast National Park, but outside this park the habitat is under threat. In Namibia, the area is threatened by poaching, and by unruly off-road enthusiasts. On the Angolan side, threats come from the collapse of infrastructure and of governance during a thirty year civil war which ended in 2002.Namibian savanna woodlands
The Namibian Savanna Woodland ecoregion covers the Great Escarpment that delimits the interior of Southern Africa from the Kaokoveld and Namib Deserts. This broken and deeply dissected escarpment is an area of high endemism for plants, invertebrates, amphibians, reptiles, mammals and birds. The northern area of the escarpment, the Kaoko escarpment, is an endemism "hotspot" (an area of extremely high species richness and endemism). This northern area is poorly protected and is under threat from poaching, off-road driving, and to a lesser extent from farming, and resultant habitat fragmentation. The formal conservation status of the southern portion of the ecoregion is poor. Other forms of protection, such as conservancies, private nature reserves and game farms do, however, promote conservation of the area. If these areas can be effectively managed through collaboration with local communities, they may solve the conservation crisis in the area.Angolan Mopane woodlands
The Angolan Mopane Woodlands are located in northern Namibia and southern Angola, completely surrounding the Etosha Pan, of Namibia which is considered a separate ecoregion. Mopane trees (Colophospermum mopane) dominate the vegetation, and are an essential resource for both the people and wildlife of the region. Elephants (Loxodonta africana) utilize almost every part of the mopane tree, and the region supports other large herbivores, including the critically endangered black rhino (Diceros bicornis). Species richness in this ecoregion is high, especially in comparison with the arid deserts to the west. Conservation potential is high in Namibia, due to the well-established Etosha National Park, and increasing community involvement and ownership of natural resources. Conservation in Angola has been severely compromised by the lengthy civil war, and many large mammal populations are near local extinction.
The Kunene River is the only perennial river flowing through this ecoregion. Its catchment lies to the north of the ecoregion in the Angolan highlands. The Kunene flows south through the ecoregion, and then it heads southwest into the Namibian Savanna Woodland ecoregion where it forms the border between Angola and Namibia.
Two national parks occur on the Angolan side of the ecoregion. These are Bikuar National Park (7900 km2) and Mupa National Park (6600 km2). While these two parks cover a representative area of the Angolan Mopane Woodlands, they do not offer adequate protection, as a result of the 30-year civil war in the country which ended in 2002.Zambezian Baikiaea woodlands
Deep Kalahari sands occur in a wide belt along the Angolan-Namibian border across to Zimbabwe, supporting dry deciduous forest dominated by Baikiaea plurijuga. The hot, semi-arid climate and nutrient-poor soils mean that this region is not suitable for farming, and thus it has retained some of its natural vegetation. Over 160 mammal species are found here, including ungulates and large predators. However, settlements occur along rivers, and the valuable Baikiaea plurijuga is sought after for the timber trade.
This ecoregion is a mosaic of dry deciduous Baikiaea plurijuga-dominated forest, thicket, and secondary grassland. The area falls within the Zambezian center of endemism and coincides largely with White’s Zambezian dry deciduous forest and scrub forest. This ecoregion forms a belt on deep Kalahari sands along the Angola-Namibia border, extending in a straight line to southwestern Zimbabwe. A portion of this ecoregion extends northwards, along the Zambia-Angola boundary. It is defined and shaped by a number of factors. The limits of the Kalahari sand delineate the east and west extent of this belt, while the southern boundary is limited by frost, and to the north, as rainfall increases the vegetation turns into evergreen Cryptosepalum forests and miombo woodland. Around the Barotse floodplain, seasonal waterlogging or flooding suppresses tree growth, and Baikiaea woodlands give way to grasslands. While the distribution of the forest, woodland, savanna, and grassland elements is partly determined by edaphic and climatic factors, disturbance factors such as fire, logging, and agriculture play an increasing role in the spread of secondary savanna and grassland.
On the whole, this ecoregion is fairly sparsely settled with fewer than 5 people per km2 in most areas. In the least populated areas, population densities are probably less than one person per km2. As a result of the scattered human population and the arid nature of the environment, much of the habitat has not been modified or fragmented. However, especially in Zambia, Angola, and Zimbabwe, timber logging together with frequent wildfires has significantly reduced the area of mature Baikiaea woodland and forest.
There are three protected areas in Angola, Bikuar and Mupa National Parks, and Luiana Partial Reserve.Western Zambezian grasslands
This ecoregion is located in southwestern Zambia, in two main portions within White’s Zambesian Center of Endemism. It extends marginally into Angola, where the grasslands are soon replaced by the Angolan Miombo Woodland ecoregion. The northern and main portion of the ecoregion consists of edaphic grasslands surrounding the patchy Zambezian Cryptosepalum Dry Forest ecoregion.
Many ungulates are found here, including the largest herd of blue wildebeest (Connochaetes taurinus) in Zambia, which undertake a spectacular migration into Angola each year. The grasslands have been inhabited by people for centuries, but are adapted to some human disturbances such as fires, and have a long history of traditional sustainable management.Zambezian Cryptosepalum dry forests
This small but distinctive ecoregion consists almost entirely of dense evergreen forest dominated by Cryptosepalum exfoliatum pseudotaxus, known locally as "mavunda." It falls into the Zambezian regional center of endemism and is mapped as ‘Zambezian dry evergreen forest.’ The two main blocks of Cryptosepalum forest are found to the north and south of the Kabompo River. Together they constitute the largest area of tropical evergreen forest in Africa outside the equatorial zone.Angolan Miombo woodlands
Covering all of central Angola and extending into the Democratic Republic of Congo, the extensive Angolan miombo woodlands are part of an even larger miombo ecosystem that covers much of eastern and southern Africa. The miombo is characterized by several unique ecological factors, including its propensity to burn, the importance of termites, and the unusual browsing conditions found here. While only poor-quality browsing is available, this ecoregion hosts a rich assortment of large mammals, some bulk feeders like the African elephant (Loxodonta africana), some specialized feeders such as the sable antelope (Hippotragus niger), and some, such as the tsessebe (Damaliscus lunatus), that utilize the wetlands scattered throughout this ecoregion. However, large mammal populations and all conservation activities have been severely affected by the decades-long civil war in Angola since 1974.
This ecoregion comprises moist, deciduous broadleaf savannas and woodlands interspersed with areas of edaphic and secondary grassland. It forms the westernmost part of the large miombo woodland belt that is the dominant type of savanna woodland in the Zambezian center of endemism. To the north and northeast lie the Southern and Western Congolian Forest-Savanna Mosaic vegetation, while the drier Zambezian Baikiaea Woodland is found on Kalahari sands to the south. The high peaks of the western highlands and the escarpment form the western boundary of the ecoregion where the miombo gives way to the Angolan Scarp Savanna and Woodlands and, at the highest elevations, to the Angolan Montane Forest-Grassland Mosaic. To the east lie the floristically distinct Central Zambezian Miombo Woodlands and the Zambezian Cryptosepalum Dry Forests and the Western Zambezian Grasslands.
Overall species richness of the ecoregion’s flora is high, though the diversity of canopy tree species is relatively low. Miombo is notable among dry tropical woodlands for the dominance of tree species with ectomycorrhizal rather than vesicular-arbuscular mycorrhizal associations. These may enable them to exploit porous, infertile soils more efficiently than groups lacking ectomycorrhizae. Many of the fungal species involved in these associations produce mushrooms, some of which are edible. This has resulted in a culture of mushroom-gathering among indigenous people that is widespread in miombo, but largely absent in other tropical African woodlands.
Faunal richness is moderate, with birds being better represented than other vertebrate taxa. The ecoregion is part of the large miombo woodland belt, the most extensive tropical seasonal woodland and dry forest formation in Africa, covering an estimated 2.7 million km2. Many of the plant and animal species found in the ecoregion are widespread throughout the savanna and woodland areas in southern Africa. While there are many species specialized and endemic to miombo vegetation, relatively few are confined to this ecoregion. Because little biological research has been carried out in Angola over the last 25 years due to the ongoing civil war, species richness estimates are likely to be an under-representation. Some of the species reported as endemic are poorly studied and collected, and their ranges may, in fact, be larger than is currently known.Angolan montane forest-grassland mosaic
This ecoregion comprises a number of small montane forest patches surrounded by grasslands and Protea savanna in the west-central highlands of Angola. The forest patches are restricted to the deep ravines or remote valleys of the highest mountains in the Huambo and Cuanza Sul provinces and an area of Afromontane forest mosaic further south, on the Serra da Chela in Huíla province. The ecoregion represents a small fragment of the Afromontane archipelago-like center of endemism, which consists of widely scattered "islands" of forest on mountain systems in southern, eastern, and western Africa. The characteristic elements of the ecoregion’s fauna and flora are more closely related to other such [Afromontane areas than to the surrounding Angolan biomes.
The ecoregion lies on the Marginal Mountain Chain of Angola, which is restricted to a narrow band running along the inland margin of the escarpment from 11° to 16° S. Residual land surfaces that possibly date back to the Gondwanan age form the highest points here, reaching 2,620 meters (m) on Mt. Môco, 2,582 m on Mt. Mepo, and 2,554 m on Mt. Lubangue.
The forests of this ecoregion are highly fragmented as a result of fires, agriculture, and woodcutting. The remaining forest patches seldom exceed 20 ha in size, and their total area is probably less than 200 ha. The most extensive forest areas, at Mt. Namba, were exploited for timber during the colonial period and are devoid of pristine patches. Relatively undisturbed patches remain at Mt. Môco between 1,800 and 2,400 m elevation. However, due to the lack of data, it is not known how extensive the forest patches once were, and at what rate their extent and quality have changed since the 1970’s. No protected areas currently exist in this ecoregion. Unless drastic conservation efforts are implemented, it is possible that little or nothing will remain of the forest patches and their fauna.Angolan scarp savanna and woodlands
This ecoregion comprises a long narrow strip of land running from about 6° to 14° S latitude between the Atlantic Ocean, the Southwest Arid biome of Angola and the top of the scarp face of the Central African Plateau. It is a complex area where several major African ecological zones meet, and where topographical features have resulted in a high diversity of vegetation types and significant levels of endemism. Biologically, the most important portion of the ecoregion is the west-facing scarp that supports rain forest at higher altitudes. This forest holds a significant number of endemic birds, and some other endemic animals and plants. The long period of civil instability in Angola means that these forests and other parts of the ecoregion have never been adequately surveyed biologically, and hence more endemics can be expected with further study.
Due to its low agricultural potential, the dry coastal belt and lower escarpment are relatively sparsely settled, and large areas remain unfragmented. For instance, large stretches of completely undisturbed habitat have been reported in Kisama National Park. Around the larger urban centers, particularly Luanda, human settlement and activities such as woodcutting and livestock grazing have had considerable, though mostly localized, impacts on the vegetation and soils.
Two areas in the ecoregion are protected, with three more areas proposed for protection but not yet established. The large Kisama National Park is bordered by the Atlantic Coast and the banks of the Cuanza and Longa Rivers and is listed by many to be among critical sites for biodiversity conservation. Marine, estuarine, floodplain, grassland and thicket habitats are represented here. Ilheu dos Passaros Integral Nature Reserve is a small offshore island with mangrove communities and mud flats which are of great botanical interest and provide key breeding habitats for water birds.
The proposed Gabela and Chingoroi Strict Nature Reserves, both representing patches of escarpment forest, are needed to protect the area’s rare endemic bird species, because their small forest habitats are declining due to agricultural activities. Without these two protected areas, the escarpment forest vegetation and its fauna are unprotected despite their vulnerability and great biological interest. The Pungo Andongo Natural Monument comprises a series of large rocky outcrops between Gabela and the coast, which should be protected for their biological and aesthetic value.Western Congolian forest-savanna mosaic
This ecoregion consists of 159,700 square miles of tropical and subtropical grasslands, savannas, and shrublands covering much of the southern part of the the Republic of Congo and the western part of the Democratic Republic of the Congo, extending north into Gabon and south into Angola.Southern Congolian forest savanna mosaic
Covering a broad area of southern Democratic Republic of Congo, the Southern Congolian Forest-Savanna Mosaic is a blend of forest, woodland, shrubland and grassland habitats. While the forests here boast only a few endemic species, they have a rich fauna, including a number of different antelope species and high numbers of African elephants. This rich blend of habitats provides key insights into the biogeography of Central Africa, which has experienced large climatic fluctuations over the last 10 million years. While there is only one protected area in this ecoregion, the human population is low. However, the civil war in the Democratic Republic of Congo has had unknown effects on this ecoregion and, until stability returns, no significant conservation work is likely to be accomplished.Central Zambezian Miombo woodlands
The Central Zambezian Miombo Woodland is one of the largest ecoregions in Africa, ranging from Angola up to the shores of Lake Victoria in Tanzania. All the typical miombo flora are represented here, but this region has a higher degree of floral richness, with far more evergreen trees than elsewhere in the miombo biome. The harsh dry season, long droughts, and poor soils are ameliorated by the numerous wetlands spread throughout the ecoregion, covering up to 30 percent of the region’s total area. As a result, a diverse mix of animals is found here, from sitatunga (swamp-dwelling antelopes), to chimpanzees, in the world-famous Gombe Stream Reserve. The bird life is also exceptionally rich, as is the fauna of some amphibian groups. The ecoregion contains areas of near-wilderness with exceptionally low human populations and extensive protected areas. Other parts of the ecoregion, typically close to lakes and mountains, have higher population densities and the miombo is much more degraded. Bushmeat hunting, dryland agriculture, deforestation especially for charcoal production near larger towns, and mining are increasing threat in this ecoregion.Central African mangroves
The Central African mangrove ecoregion is located in western Africa, and encompasses mangrove areas along the coastlines of Ghana, Nigeria, Cameroon, Equatorial Guinea, Gabon, Democratic Republic of Congo (DRC), and Angola (to 19°18' S). The structure of the mangrove areas varies considerably, from the lagoon systems found in the western part of this ecoregion to systems modified by complex patterns of sediment deposition at river mouths in the central and southern portions.
These mangroves flank the coastline of western and central Africa, in suitable low energy marine environments. The largest mangrove stand is found in the Niger Delta, which supports the most extensive area of mangrove in Africa. In Angola, large mangrove communities occur at the mouths of the Cuvo, Longa, Cuanza, Dande, and M'Bridge Rivers, though they are not as extensive as the vast mangrove swamps at the mouth of the Zaire River. The dominant trees are Rhizophora racemosa, R. mangle, R. harrisonii and, Avicennia africana, the former two species reaching heights of approximately 30 meters (m).Context
Ecoregions are areas that:
 share similar environmental conditions; and,
 interact ecologically in ways that are critical for their long-term persistence.
Scientists at the World Wildlife Fund (WWF), have established a classification system that divides the world in 867 terrestrial ecoregions, 426 freshwater ecoregions and 229 marine ecoregions that reflect the distribution of a broad range of fauna and flora across the entire planet.
WWF identifies fourteen ecoregions the exist entirely or in part in Angentina:
- Araucaria moist forests
- Humid Chaco
- Arid Chaco
- Southern Andean Yungas
- Central Andean puna
- Central Andean dry puna
- Southern Andean steppe
- Argentine Monte (Low Monte)
- Argentine Espinal
- Humid Pampas
- Paraná flooded savanna
- Valdivian temperate forests
- Patagonian steppe
- Magellanic subpolar forests
Araucaria moist forests
This ecoregion spans the mountainous areas of southern Atlantic Brazil and extends into northeastern Argentina. These forests are a relict of a once widespread ecosystem of mixed coniferous and broad-leafed trees, spread out across a mountainous landscape. Annual precipitation is high, and ranges from 1300-3000 millimeters (mm). Less than one percent of the ecoregion is covered by protected areas. More reserves are needed to save these biologically rich forest from illegal logging and urban expansion.Most of this ecoregion is on sedimentary rocks of the Paraná Plateaus.
The climate is subtropical with frequent frosts and with no dry season. Annual precipitation shows a significant variation between 1,300 mm and 3,000 mm. The main vegetation is Atlantic moist forest, with a particular 45-meter-tall emergent strata of the Brazilian Araucaria (Araucaria angustifolia). Canopy layers are rich in species of Lauraceae (Ocotea pretiosa, O. catharinense), Myrtaceae (Campomanesia xanthocarpa), and Leguminosae (Parapiptadenia rigida). These forests form complex mosaics of plant associations among the pioneer Brazilian Araucaria and tree species from different types of Atlantic forest. This moist forest ecoregion is recognized as an important Endemic Bird Area. It is also home for Atlantic endemic and threatened vertebrates such as the brown howler monkey (Alouatta fusca) and the red spectacled Amazon (Amazona petrei), which have few populations scattered in remnants of these forests.
Threatened vascular plant species also survive here, including the Brazilian Araucaria. From a evolutionary perspective, Brazilian Araucaria moist forests represent more widespread South America coniferous forests of the past and, therefore, have great importance for conservation. Illegal timber extraction and forest conversion into agricultural lands represent a large threat to the future of these forests because they possess fertile soils that are attractive to agricultural interests.Humid Chaco
This region is a mosaic of ecosystems, combining woods with savanna. In this mosaic, various species of trees, shrubs, and coarse grass develop and are associated with numerous species of fauna adapted to this diverse environment. Poaching and exploitation of plants are the main threats to the natural habitat in this ecoregion, which has been considerably altered due to cattle raising. The Chaco Humedo ecoregion is located in northeastern Argentina, the center of Paraguay, and small areas in southwestern Brazil. The region slopes gently towards the east and overlooks areas full of depressions. The soils are generally sedimentary, originating from river flows and composed of fine materials. Precipitation varies between 1,300 millimeters (mm) annually in the east and 750 mm in the west.
The vegetation consists of xenophile forests mixed with palm savannas. The grasslands of this region are quite varied depending upon the soils. The fauna is very diversified resulting due to the heterogeneity of the habitat. Among the large mammals we find: maned wolf, black howler monkey, Azara's night monkey, pecaries, giant anteater, capybara, deer, marsh deer, pampas deer, puma, and jaguar. Some of the birds include the ñandú, Crypturellus undulatus, Celeus lugubris, Heterospizias meridionalis, and others. Dinerstein et al. have classified this ecoregion as vulnerable, and of importance on a local and a national scale. Cattle raising and forest exploitation have profoundly changed the composition of the vegetative communities either by destroying the herbaceous layer, eliminating the hardiest forest species or by burning all of the forest for agriculture. Commercial hunting and poaching threaten the fauna chaqueña. Illegal shipments of leather and furs violating the established quotas and/or containing threatened, and thus prohibited, species are found at ports.Arid Chaco
The Guarani Indians initially described this region as "Gran Chaco", which implies productive hunting grounds. Today much of the northern Chaco is still abundant with large game mammals, suggesting sustainably harvested populations. However, this is no longer the case in much of the southern Chaco where rampant overgrazing and human population growth has preceded the pristine nature of the Chaco. An important migration route, many species of avifauna can be found in this ecoregion throughout the year. More protected areas are needed in order to save this habitat from overwhelming agricultural development.
The Chaco represents a region that was inadequately explored until recently, with new species of large vertebrates such as the Chacoan Peccary (Catagonus wagneri) being discovered as recently as the 1970’s. Moreover, new records of known species are increasingly documented as the international scientific community realizes more fieldwork-hours.
Argentina has several reserves in the Chaco, primarily in the northern Argentine Chaco (RN Formosa, PNs Pilcomayo, Baritú, Callilegua, El Rey, and RPs Agua Dulce, Potreros de Yala, El Bagual), with a couple in the central (RP Los Palmares and RP Copo) and southern (RP Chaco) regions.Southern Andean Yungas
This ecoregion is extremely fascinating from a biogeographic perspective, as it contains what may be the last of the isolated ‘evergreen’ forests resulting from Quaternary glaciations. This region is rich in fauna species, especially avifauna. Many tropical species meet their southern limits of geographic distribution in this region. The forests of Argentina have suffered more damage than Bolivia. A number of national parks protect the forest of this ecoregion.
This ecoregion essentially forms a mesic habitat that lies between two much drier habitats: the Chaco to the east, and the higher Puna to the west. The habitat is evergreen forest, with canopy height typically not exceeding 15 m. Between 1,200 – 2,500 m the forest is dominated by Andean Alder (Alnus acuminata) and Mountain Pine (Podocarpus parlatorei) or Queñoa (P. australis); at lower elevations these species form a mosaic with other trees, especially Lauraceae and Myrtaceae.Central Andean puna
This ecoregion is a high elevation montane grassland in the southern high Andes, extending from southern Peru, though Bolivia, into northern Argentina. Open meadows are dotted with an assortment of rock, bunchgrass, herbs, moss, and lichens. The landscape is characteristically mountainous, with snow capped peaks, mountain pastures, high lakes, plateaus, and valleys. The Central Andean Puna, despite its characteristic dryness and because it still maintains nearly unaltered blocks of habitat, represents an important area for the **conservation of endemic species of both flora and fauna. Its climate varies from temperate to cold, it is dry with an average temperature between <0 and 15ºC. Precipitation varies between 250 and 500 millimeters (mm) per year.
This ecoregion rests on formations of volcanic origin subsequent to the formation of the Andes (about 6-8 million years ago). The vegetation is characterized by being notably drier than in the rest of the puna. This ecoregion faces increasing mining activity that is leading to the destruction of its scarce plant cover as well as the contamination of some bodies of water and the soil. In addition, this region has a large number of population centers and highways that cross the Andes, leading to a decline in natural habitat and growing pressures on the existing fauna. Fortunately, a portion of these habitats is represented within some existing protected natural areas and most plant formations are included in these areas. However, there are still some information gaps, particularly in the case of birds, and there are some priority areas to be preserved.Central Andean dry puna
This ecoregion is a very dry, high elevation montane grassland and herbaceous community of the southern high Andes, extending through western Bolivia and northern Chile and Argentina. The vegetation is characteristically tropical alpine herbs with dwarf shrubs, and occurs above 3,500 meters (m) between the tree-line and the permanent snow-line. Dry puna is distinguished from other types of puna by its annual rainfall, or lack of rainfall. This ecoregion receives less than 400 millimeters (mm) of rainfall each year, and is very seasonal with an eight-month long dry season. The Central Andean Dry Puna is a unique ecoregion with flora and fauna highly adapted to the extreme temperatures and altitudes.
The Andes were formed by large introsions of igneous rock and volcanic activity. The formation was assumed its present form in the Tertiary period approximately 50 million years ago. This ecoregion encompasses many volcanic mountains and the high plateau to the east called the Altiplano. The region lies at an elevation of 3,500-5,000 meters (m) above sea level. The northern part of the ecoregion has a temperature ranging from 8 to 11°C; temperatures in the southern area are lower. The mid-southern sections of the ecoregion are drier than the north, with an annual precipitation that varies from 51 mm to 406 mm.Southern Andean steppe
The southern Andean steppe ecoregion extends along the high elevations of the Andes of central Argentina and limiting areas of Chile, a generally dry area that includes many of the highest mountains of South America. Several plant genera that are characteristic of the ecoregion have evolved many endemic species in this area. The plants generally show adaptations to extreme dry conditions, cold and wind, and frequently have spines as anti-herbivore defenses and conspicuous flowers to attract pollinators. The fauna is related to that of limiting ecoregions, especially to that of central Andean dry Puna and to the Patagonian steppe.Argentine Monte
The Argentine Monte is located in north-central Argentina, extending along the eastern foothills of the Andes until it reaches the Patagonian steppe, then extends eastwards to the Pacific Ocean. Here thorn scrub and dry grasslands are common. It is a warm scrub desert extending between the Puna, Patagonia, and Chaco ecoregions. The climate is temperate-arid with very little rainfall (between 80 and 250 millimeters per year). The northern and central regions of the Monte receive rain in summer but in the south is colder and rainfall is distributed throughout the year. The dominant vegetative formation of this ecoregion is scrublands, that at times can be very open. This ecoregion has several endemic species of flora and fauna. The insect fauna is quite well known from the northern part of the Monte where there are a high proportion of endemic genera (10%) and out of species (35%) belong to different families.
Human populations preferred to occupy oases in valleys and other locations close to rivers that make irrigation possible. This is why some sections of the ecoregion were intensively altered but others were not. The forest also underwent significant depredation as man occupied patches and used wood for vineyards, mining, furniture making, construction, and fuel. Overgrazing and deforestation has caused erosion that affected 58 million hectares of the ecoregion. The Monte, as well as in the Chaco and Patagonia lowland, is experiencing seriously damaging effects due to human activities, especially overgrazing by goats, sheep, and cattle; clear cutting for fuel; and land clearing for agriculture, mining, and oil exploration. The deforestation and selective extraction of hardwood and clear cutting of mesquite forests began at the late 19th and early 20th centuries and continues today.Argentine Espinal
This ecoregion is described as an "espinal", literally meaning a thorny deciduous shrubland forest. The occurrence of this vegetation type is extensive from the central basin of the Paraná River (west of the flooded savannas) westward to the Córdoba Mountains. This region has become developed and cultivated and is threatened by agricultural expansion. In the northern section, the climate is warm and wet with summer rains. It is a mostly flat plain with low hilly areas. In the wetlands we find a very rich and varied fauna, including species adapted to saline environments. The number of avian species recorded is 138, among which we should emphasize the large reproductive colonies of the flamenco chileno (Phoenicopterus chilensis).
This ecoregion has been heavily modified as most of it has been used for agriculture and its forests have been highly exploited and dismantled. The carob tree is a species that has been much used by man, both for the shade it provides and for its fruit that is used as forage for livestock. The Espinal is protected in the Lihué-Calel National Park, La Reforma University Reserve, Chacharramendi Provincial Reserve, and Luro Provincial Reserve. A major threat to the Mar Chiquita lake and the floodplain of the Dulce River within this ecoregion is the growing use of its water by humans in the upper basin.Humid Pampas
The Humid Pampas ecoregion occupy one of the most human populated areas in Argentina. The ecoregion consists of the plains, many rivers, and lagoons. The natural vegetation in the area is composed of grasslands and xeric woodland. There are various endemic animals that are threatened by habitat destruction and degradation. The ecoregion is considered endangered and is regarded as a high priority conservation area at the regional scale. The Humid Pampas occupy the plains in the east of Argentina, taking up most of the province of Buenos Aires. Horizontal plains and very soft undulations with low peaks that emerge like islands characterize the relief of this area. There are a few slow moving, undulating rivers and many lagoons with fresh and salt water. The pampas plains originated in packed sediment from a large sinking tectonic pit that extends to the Chaco. The climate is hot with rain throughout the year.
The pampas region lacks endemic vegetation of importance. Species in danger of extinction include the pampas deer, a very important herbivore in this area. Little is left of the natural habitat in the Humid Pampas. This is one of the most heavily populated areas of Argentina that has been extensively used for agriculture and cattle grazing. Natural vegetation grows in small patches that persist along the railroad tracks and in some abandoned fields left to rest for many years. Only certain species of animals live in this disturbed and altered habitat. The region has been classified as a maximum priority ecoregion at regional scale. There are two severe threats in the region: conversion of remaining natural habitats for agriculture and degradation through over-grazing are severe threats. Burning and draining of lands are also threatening remaining habitats that could possibly affect protected areas.Paraná flooded savanna
This flooded savanna, fed by the Paraná river, is located in Argentina. Defined by a almost subtropical temperatures usually found much farther north, this region is rich in flora and fauna that is uncharacteristic of its surrounding regions. A number of national parks protect this habitat, which contains three endemic bird areas. The main threat to this ecoregion is the building of damsand dykes, while hunting, urban expansion, and pollution constitute other threats.
This region includes the floodplains of the middle and lower Paraná river and its tributary the Paraguay river. The southern section includes the Paraná delta and the la Plata river basin. The landscape of this region is represented by low islands that flood and are delimited by the lateral branches and major flows of the great rivers and extensive coastal lowlands.
The permanent presence of large bodies of water create local climatic effects with high ambient humidity and mitigate extreme daily and seasonal temperatures, allowing for the presence of communities and species typical of the humid subtropical regions of the country’s northeast.
The vegetation in this region consists of forest and shrublands in slender coastal strips on albardones [land emerging from the water]; scrublands and pastures on the islands in open waters; hydrophilic and aquatic communities on the shores of rivers and channels; and interior island lagoons.
The forests consist primarily of Salíx humboldtiana (sauce criollo or sauce colorado), Tessaria intergrifolia (aliso), Erythrina crista-galli (ceibo), etc. Aquatic communities include camalotes, primarily of the genus Eichhornia and Reussia, onagraceae like Victoria cruziana (irupé) with large plate-shaped leaves and white flowers with many petals; we also find Cyperus giganteus (pirí), Typha latifolia and T. Domingensis (totoras) and the beautiful blue-flowered pontederiacea Pontederia lanceolata (cucharero)Valdivian temperate forests
The Valdivian temperate forests and the more hygrophilous vegetation of the Mediterranean area of central Chile, represent a true biogeographic island separated from climatically similar areas by extensive ocean barriers and deserts.Alerce trees, Lenca, Chile. (Photograph by Marco Cortez)
The Valdivian temperate forest is characterized by its extraordinary endemism (e.g., 90% at the
species level and 34% at the genus level for woody species) and the great antiquity of its biogeographic relationships.
Its taxons show close philogenetic relationships dating back to the early Tertiary, with Gondwanic taxons of Oceania forming more recent relationships with Neotropical taxons, separated from other biotas in South America by the great mountainous barrier of the Andes.Patagonian steppe
This ecoregion extents roughly from the mid-Andean Precordillera southward, ending just north of the Straights of Magellan near the Rio Gallegos. This steppe is bordered on the west by the cold temperate forest slopes of the Andes, and on the east by the Pacific Ocean. It extends north-west as shrubland steppe and to the north as thorn thicket, gradually making the transition to Argentine Monte. This area is a cold desert scrub steppe, with almost constant wind and year round frosts likely. This ecoregion has high levels of endemism in both plants and animals. This Patagonian steppe ecoregion mainly covers the Patagonia region of Argentina from the Atlantic Ocean shore to barely across the border into Chile. A characteristic of the Patagonian climate is the constant drying wind that blows with great force from the western sector, particularly in the summer months. Winter generally lasts for five months from about June to September with averages of the coldest month between 1-3°C below freezing. In general, the vegetation of this steppe ecoregion is xerophytic and highly adapted for protection against drought, wind, and herbivores.
In this ecoregion we find two endemic species of the genus Prosopis, one species of Larrea and species of the genera Lycium and Schinus. The Argentine coasts have high species diversity, including 33 species of cetaceans, 8 species of pinnipeds and more than 450 species of fish in the waters of the Argentine sea. Despite the low density of the human population, this ecoregion has been seriously affected due to the fragility of the environment. This ecoregion has many natural reserves. The major problem is desertification due to over-grazing primarily by sheep, damaging the limited plant coverage and exposing the soil to erosion. In addition, many species of fauna are now in regression due to the tempting prices paid for the skins of chulengos (baby guanacos) and choique rhea feathers. There is also pressure on foxes and pumas from hunting and/or poisoning because they are considered a potential threat to flocks.Magellanic subpolar forests
The subpolar Nothofagus forests cover the western part of the southern end of South America. The ecoregion is colder and in parts drier than the Valdivian temperate forests, and in general is floristically poorer. The fauna is related to that of the bordering ecoregions, especially to that of the Valdivian temperate forests and the Patagonian steppe. Nevertheless, its varied and majestic landscapes that include high mountain peaks, enormous icefields, and innumerable fjords are inhabited by unique and endemic animal and plant species that are sometimes abundant within this ecoregion. The northern end of the subpolar Nothofagus forests limit with the Valdivian temperate forests and the eastern part with the Patagonian steppe and the Patagonian grasslands. Towards the west the region is in contact with the cold southern Pacific Ocean, and on the high Andes vegetation floristically related to the south Andean steppe appears in parts as interrupted islands.
Permanent snow, ice caps and glaciers are present in the summits of many of the higher elevations. The climate of this area is wet and temperate-cold and very cold at high elevations. The effect of the cold northward Humboldt and Antarctica currents on the western and southern coasts makes the area colder than others at similar latitudes, with mean January (summer) temperatures lower than 10º C. The strong westerly winds blow all year round, producing high rainfall in the windward west side of the mountains and lower precipitation to the east, and no dry season. The vegetation shows principally two types of forest, mainly evergreen Nothofagus betuloides forests to the west and deciduous Nothofagus pumilio and Nothofagus antarctica forests towards the east that extend into Argentina. In the colder areas with high rainfall of the south western most parts of the ecoregion a characteristic vegetation specially termed Magellanic moorland or Magellanic tundra extends through the Chilean archipielago to 48ºS. This tundra is characterized by prostrate dwarf shrubs, cushion plants, grass-like plants and bryophytes on water-logged terrain that in different combinations form vegetation of scrub or bogs. Important levels of endemism are found among plants, with several mostly herbaceous species being confined to the ecoregion.11. Paraná flooded savanna This flooded savanna, fed by the Paraná river, is located in Argentina. Defined by a almost subtropical temperatures usually found much farther north, this region is rich in flora and fauna that is uncharacteristic of its surrounding regions. A number of national parks protect this habitat, which contains three endemic bird areas. The main threat to this ecoregion is the building of dams and dykes, while hunting, urban expansion, and pollution constitute other threats. This region includes the floodplains of the middle and lower Paraná river and its tributary the Paraguay river. The southern section includes the Paraná delta and the la Plata river basin.
Fish perhaps define the most interesting and diverse group in this region with more than 300 species with a predominance of characiforms and siluriforms. Large infrastructure projects such as dykes, dams, waterways, roads, etc. represent a great threat to the flora and fauna of Argentina. In the case of this region, we should add petroleum and mining operations, agriculture, urban expansion, pollution, habitat fragmentation, and poorly-managed tourism. Commercial hunting and poaching also threaten wildlife as illegal shipments of hides and skins, in violation of established quotas and/or involving the hunting of prohibited species, are often detained.Protected Areas
- Iguazú National Park
- Los Glaciares National Park
- Pali Aike volcanic formations (straddles border with Chile)
- Península Valdés
- Tierra del Fuego National Park
Ecoregions are areas that:
 share similar environmental conditions; and,
 interact ecologically in ways that are critical for their long-term persistence.
Chemicals that mimic or antagonize the actions of naturally occurring estrogens are defined as having estrogenic activity (EA), which is the most common form of endocrine disruptor activity.
This article, written by Chun Z. Yang, Stuart I. Yaniger, V. Craig Jordan, Daniel J. Klein, and George D. Bittner* appeared first in Environmental Health Perspectives—the peer-reviewed, open access journal of the National Institute of Environmental Health Sciences.
A Potential Health Problem That Can Be Solved Abstract
Background: Chemicals having estrogenic activity (EA) reportedly cause many adverse health effects, especially at low (picomolar to nanomolar) doses in fetal and juvenile mammals.
Objectives: We sought to determine whether commercially available plastic resins and products, including baby bottles and other products advertised as bisphenol A (BPA) free, release chemicals having EA.
Methods: We used a roboticized MCF-7 cell proliferation assay, which is very sensitive, accurate, and repeatable, to quantify the EA of chemicals leached into saline or ethanol extracts of many types of commercially available plastic materials, some exposed to common-use stresses (microwaving, ultraviolet radiation, and/or autoclaving).
Results: Almost all commercially available plastic products we sampled—independent of the type of resin, product, or retail source—leached chemicals having reliably detectable EA, including those advertised as BPA free. In some cases, BPA-free products released chemicals having more EA than did BPA-containing products.
Conclusions: Many plastic products are mischaracterized as being EA free if extracted with only one solvent and not exposed to common-use stresses. However, we can identify existing compounds, or have developed, monomers, additives, or processing agents that have no detectable EA and have similar costs. Hence, our data suggest that EA-free plastic products exposed to common-use stresses and extracted by saline and ethanol solvents could be cost-effectively made on a commercial scale and thereby eliminate a potential health risk posed by most currently available plastic products that leach chemicals having EA into food products.Keywords: bisphenol A, endocrine disruptor, endocrine-disrupting chemical, estrogen receptor binding, estrogenic activity, plastic.
Chemicals that mimic or antagonize the actions of naturally occurring estrogens are defined as having estrogenic activity (EA), which is the most common form of endocrine disruptor activity [Interagency Coordinating Committee on the Validation of Alternative Methods (ICCVAM) 2003, 2006; National Research Council 1999]. Chemicals having EA typically interact with one or more of the classical nuclear estrogen receptor (ER) subtypes: ERα, ERβ, or nonclassical membrane or ER-related subtypes (Hewitt et al. 2005; Matsushima et al. 2008; National Research Council 1999). In mammals, chemicals having EA can produce many health-related problems, such as early puberty in females, reduced sperm counts, altered functions of reproductive organs, obesity, altered sex- specific behaviors, and increased rates of some breast, ovarian, testicular, and prostate cancers (Della Seta et al. 2006; Gray 2008; Kabuto et al. 2004; National Research Council 1999; Newbold et al. 2004; Patisaul et al. 2006, 2009). Fetal, newborn, and juvenile mammals are especially sensitive to very low (sometimes picomolar to nanomolar) doses of chemicals having EA (Gray 2008; vom Saal et al. 2005). Many of these effects observed in mammals are also expected to be produced in humans, because basic endocrine mechanisms have been highly conserved across all classes of vertebrates (Kavlock et al. 1996; National Research Council 1999).
Thermoplastics, which are used for many items that contain food, are made by polymerizing a specific monomer or monomers in the presence of catalysts into a high-molecular- weight chain known as a thermoplastic polymer [see Supplemental Material, Figure 1 (doi:10.1289/ehp.1003220)]. The resulting polymer is mixed with small quantities of various additives (antioxidants, plasticizers, clarifiers, etc.) and melted, mixed, extruded, and pelletized to form a base thermoplastic resin. Base resins are either used as is [e.g., bisphenol A (BPA)-based polycarbonate (PC), non-BPA-based polypropylene (PP) copolymer (PPCO), and non-BPA-based PP homopolymer (PPHO)] or, more commonly, mixed with other resins, additives, colorants, and/or extenders to form plastic compounds (e.g., polymer blends and precolored polymers). Plastic products are then made by using one or more plastic compounds or resins to form a finished plastic part that can be subjected to finishing processes that may use inks, adhesives, and so forth, to make a finished product.Figure 1. Click for Larger Image.
Results of MCF‑7 assays shown as dilution response curves (%E2) for E2 (A), E2 and BPA (B), BHA (C), and %RME2 of extracts of plastic bags (D), a PC bottle (E), and a BPA-free bottle made from PETG (F). Abbreviations: PETG, PET glycol-modified polyethylene terephthalate; VC, vehicle control. Dotted lines represent 3 SD from the response. In B–F, the negative control (1% EtOH or saline) equals 0% E2. The E2 standard (10–9 M) is the positive control diluted as indicated in C–F. Each point plotted is the average of three or four replicates for each concentration whose SD is very small and falls within the space taken up by each data point. In (A), E2 was dissolved in EtOH (standard extract) or concentrated 10× and rediluted to show that the EtOH concentration protocol has very little effect on the EC50 of E2 (50% E2). The EC50 of E2 is approximately 1.3 × 10–13 M, and the threshold of detection (15% E2) is approximately 10–15 M. The maximum E2 response was attained at 10–11 M and remained constant at higher E2 concentrations. (B) The EC50 of both E2 (as in A) and BPA is approximately 6.6 × 10–8 M, and threshold detection is approximately 10–9 M, all suppressed by 10–8 M ICI. (C) BHA does not meet criteria needed for accurate calculation of EC50 [see Supplemental Material, pp. 5–7 (doi:10.1289/ehp.1003220)]. EA is positive; its maximum response is about 50% E2 (i.e., 50% RME2) and is suppressed by 10–8 M ICI. In D, commercially available plastic bags were extracted by 100% EtOH. Commercially available PC (E) and BPA-free (F) bottles were extracted with saline or EtOH as indicated.
As previously described (Begley et al. 1990, 2005; De Meulenaer and Huyghebaert 2004), plastic resins and manufacturing protocols [see Supplemental Material, Figure 1 (doi:10.1289/ehp.1003220)] collectively use many monomers and additives that may exhibit EA because they have physicochemical properties, often from an insufficiently hindered phenol (HP) group, that enable them to bind to ERs (see Supplemental Material, Table 1). Because polymerization of monomers is rarely complete and additives are not chemically part of the polymeric structure, chemicals having EA can leach from plastic products at very low (e.g., nanomolar to picomolar) concentrations that individually or in combination can produce adverse effects, especially in fetal to juvenile mammals. This leaching of monomers and additives from a plastic item into its contents is often accelerated if the product is exposed to common-use stresses such as ultraviolet (UV) radiation in sunlight, microwave radiation, and/or moist heat via boiling or dishwashing. The exact chemical composition of almost any commercially available plastic part is proprietary and not known. A single part may consist of 5–30 chemicals, and a plastic item containing many parts (e.g., a baby bottle) may consist of ≥ 100 chemicals, almost all of which can leach from the product, especially when stressed. Unless the selection of chemicals is carefully controlled, some of those chemicals will almost certainly have EA, and even when using all materials that initially test EA free, the stresses of manufacturing can change chemical structures or create chemical reactions to convert an EA-free chemical into one with EA.
Table 1. Click for Larger Image.
Percentage of unstressed plastic products having EA in at least one extract.
Very few studies (Soto et al. 1991; Till et al. 1982) have examined the extent to which plastics that presumably do not contain BPA nevertheless release other chemicals having detectable EA. For example, a recent comprehensive review [table on page 72 of Gray (2008)] described polyethylene (PE), PP, and PE terephthalate (PET) plastics as being “‘OK’ for use with respect to release of chemicals exhibiting EA.”
Here, we report that most of the > 500 commercially available plastic products that we sampled—even those that are presumably BPA free—release chemicals having detectable EA, especially if they are assayed by more polar and less polar solvents and exposed to common-use stresses. That is, we show that, to reliably detect such leachable chemicals having EA, unstressed or stressed plastic resins or products should be extracted with more polar (e.g., saline) and less polar [e.g., ethanol (EtOH)] solutions and exposed to common-use stresses (boiling water, microwaving, and UV radiation).Materials and Methods
We developed a sensitive and accurate roboticized version of the MCF-7 cell proliferation assay (E-SCREEN assay) that has been used for decades to reliably assess EA and anti-EA (Leusch et al. 2010; Soto et al. 1995) and is currently undergoing validation for international use by ICCVAM/NTP (National Toxicology Program) Interagency Center for the Evaluation of Alternative Toxicological Methods (NICEATM). Chemicals with EA bind to ERs (ERα, ERβ, or ER-related subtypes) and activate the transcription of estrogen-responsive genes, which leads to proliferation of MCF-7 cells.
Detailed methods for the MCF-7 assay are provided in Supplemental Material, (doi:10.1289/ehp.1003220). In brief, plastic resins or products were extracted using saline, a more polar solvent, or EtOH, a less polar solvent. Aliquots of the extracts were then diluted four to eight times to produce up to eight test concentrations. Each test chemical or extract at each concentration was added in triplicate or quadruplicate to 96-well plates containing MCF-7 cells in EA-free culture media. After 6 days of exposure, the amount of DNA per well, an indication of cell proliferation, was assayed using a microplate modification of the Burton diphenylamine assay (Burton 1956; Natarajan 1994).
The effect of a test chemical or extract on proliferation was expressed as the %E2, a percentage of the maximum DNA per well produced by the maximum response to 17β-estradiol (E2; positive control) corrected by the DNA response to the vehicle (negative) control [see Supplemental Material, Equation 1 (doi:10.1289/ehp.1003220)]. For estrogenic test chemicals, the concentration needed to obtain half-maximum stimulation of cell proliferation [half-maximal effective concentration (EC50), a measure of binding affinity] was calculated from best fits to dose–response data that meet a well-defined set of criteria by Michaelis-Menton kinetics. The estrogenicity of extracts was calculated as the relative maximum %E2 (%RME2; a measure of response amplitude), a percentage of the maximum DNA per well produced by an extract at any dilution with respect to the maximum DNA per well produced by E2 at any dilution, corrected by the DNA response to the vehicle (negative) control (see Supplemental Material, Equation 2). If a test chemical had a positive response (> 15% RME2) but an EC50 could be calculated because not all criteria were met, then the estrogenicity of the test chemical was characterized simply as EA positive or by its %RME2.
The EA of a test chemical or extract was considered detectable if it produced cell proliferation > 15% of the maximum response to E2 (> 15% RME2), which is > 3SDs from the historic control baseline response (about 10–15 M), which is a rather conservative measure of EA detectability. Stimulation of MCF-7 proliferation induced by the test chemical or extract was confirmed to be estrogenic (compared with nonspecific) in an EA confirmation study: If the stimulation of MCF-7 proliferation by a test chemical or extract was suppressed by coincubation with a strong antiestrogen [ICI 182,780 (ICI) at 10–7 to 10–8 M], the EA of the test chemical or extract was confirmed. Therefore, a test chemical or extract was classified as not having detectable EA if it did not induce MCF-7 cell proliferation or if it induced proliferation that could not be inhibited by ICI.
Figure 1 shows typical MCF-7 responses plotted as %E2. Figure 1A–C show responses to some test chemicals: E2 (positive control), BPA, and butylated hydroxyanisole (BHA; a common antioxidant). Figure 1D–F show %RME2 responses to test extracts of plastic food bags, PC bottles, and BPA-free baby bottles and their ICI-suppressed responses, confirming their EA. Some chemicals or products were also analyzed for anti-EA [for details, see Supplemental Material, pp. 7–8 (doi:10.1289/ehp.1003220)].
Purchase and analyses of plastic products in survey studies. For Tables 1 and 2, we purchased 455 plastic products used to contain foodstuffs from various commercial retailers from 2005 through 2008. The relative frequency of products having detectable EA did not change with later compared with earlier purchases. In some cases, we instructed undergraduate students or employees to purchase a mix of plastic items used to contain foodstuffs from a given large retailer (Albertsons, H-E-B, Randalls, Target, Wal-Mart, Trader Joe’s, and Whole Foods) mainly in the Austin, Texas, or Boston, Massachusetts, areas, some of which market many “organic” products. In other cases, we purchased products of a particular plastic type (e.g., PE- or PP-based containers). We recorded the retailer, resin type [high-density PE (HDPE), PET, PC, PP, polystyrene (PS), polylactic acid], and product type (flexible packaging, food wrap, rigid packaging, baby bottle component, deli containers, plastic bags). In addition, because the contents of some plastic items might have added or extracted chemicals having EA from the plastic containers before we purchased and tested the products (Sax 2010), we recorded whether the plastic items had contents or were empty when purchased. For any plastic container having contents, we thoroughly washed out the container with distilled water before testing the plastic. Except for PC-based items, none of these products were known to contain BPA. (Plastic products typically do not list their chemical composition, which is proprietary to the manufacturer.) Samples were chosen in product areas where adverse health effects might occur if the samples leached chemicals having EA. Samples from each retailer generally included most of the product types listed above. In addition to surveying commercially available products, we tested plastic resins [e.g., PC, PET, glycol-modified PET (PETG)] that were purchased from M. Holland Company (Northbrook, IL) and individual chemicals used to manufacture plastic products [e.g., BPA, BHA, butylated hydroxytoluene (BHT), dimethyl terephthalate, etc.] that were purchased in their purest form from Sigma-Aldrich (St. Louis, MO).Table 2. Click for Larger Image.
Percentage of unstressed plastic products having detectable EA (> 15% RME2) in two extracts.
Many plastic products have more than one plastic part. For example, baby bottles have 3–10 different plastic parts in various combinations [bottle, nipple, anticolic item(s), sealing ring(s), liner bag, cap, etc.], each part typically having different and rather unique combinations of 5–30 chemicals. Over the course of this entire study, we assayed > 100 component parts from > 20 different baby bottles, including many advertised as BPA free. Only some (13) of these component parts were purchased for the initial survey study (Tables 1 and 2).
Most of the samples (338 of 455) in the survey study (Tables 1 and 2) were extracted using only one extraction protocol. For the remaining samples (n = 102), both saline and EtOH extractions were used so that the efficacy of each protocol could be directly compared. We used a paired Student’s t-test to test whether differences between pairs of samples were statistically significant (p < 0.05).
Protocols for common-use stresses of some plastic items. Given that common-use stresses can alter the complex chemical composition of plastics and/or increase the rate of leaching (Begley et al. 1990, 2005; De Meulenaer and Huyghebaert 2004), for some resins or products, we examined how leaching of chemicals having EA might be affected by exposure to microwave radiation, autoclaving (moist heat), and UV light. Additional plastic items, some of which are described in Figure 2 and Table 3, were purchased in 2008–2010 and subjected to common-use stresses. In addition, we tested a variety of resins (including PE- and PP-based resins; Table 3), antioxidants [see Supplemental Material, Table 3 (doi:10.1289/ehp.1003220)], and other additives or processing agents (see Supplemental Material, Table 4) identified by our laboratory as being free of detectable EA and hence possibly suitable for use to produce final products that would be EA free even after exposure to common-use stresses.Figure 2. Click for Larger Image.
Total EA released by some PC and BPA-free water bottles (W) and baby bottles (B). The leaching of chemicals having EA (measured as %RME2; excluding caps, nipples, and other components) were extracted using saline or EtOH as solvents and exposed to autoclaving, microwaving, and/or UV light (see “Materials and Methods” for details). BPA-free water bottles W1, W2, W3, and W4 are PETG, and W5 is PET. BPA-free baby bottles B1 and B2 are polyethersulfone; B3 is PETG; and B4 and B5 are PP. Orange bars indicate the data set for each individual product. The %RME2 for saline extracts is represented by solid black lines and for EtOH as solid red lines. Symbols represent the %RME2 of chemicals released by each assay of a product after an autoclaving stress, microwaving stress, and UV light stress (see figure key). The dotted horizontal line at 15% RME2 is the rather conservative value below which EA was considered nondetectable (ND) for any assay. For some products shown (e.g., PC B1, BPA-free B4), if one solvent and/or stress condition showed reliably detectable EA, other solvents and stress conditions were not subsequently tested. Some values plotted as 0% RME2 actually had slightly negative %RME2 values (–1% to –7% RME2) due to cellular toxicity.Table 3. Click for Larger Image.
Representative %RME2 values for stressed resins or parts made from flexible or HC polymers.
We used the following stresses:
Samples were placed about 2 feet from a 254-nm fluorescent fixture for 24 hr, simulating repeated UV stress by sunlight (e.g., water bottles) or UV sterilizers (e.g., baby bottles and medical items)
Samples were autoclaved at 134°C for 8 min, simulating moist heat stress in an automatic dishwasher
We heated samples in a microwave 10 times for 2 min each, using a 1,000-W kitchen microwave oven set to “high,” simulating heat and microwave radiation stress to reusable food containers.
Release of chemicals having EA from unstressed plastics. Tables 1 and 2 show the percentage of samples in each category that had reliably detectable EA (> 15% RME2) in our survey of 455 commercially available plastic products. [For the %RME2 and content status of individual samples, as well as the average %RME2 for products classified by resins (HDPE, PP, PET, PS, polylactic acid, PC), product type (flexible packaging, food wrap, rigid packaging, baby bottle components, plastic bags), and retailer (large retailers 1–5 and large organic retailers 1 and 2), see Supplemental Material, Table 5 (doi:10.1289/ehp.1003220).] For example, 9 of 13 HDPE plastic products extracted by our standard EtOH protocol (69%) had detectable EA (Table 1), with a %RME2 (mean ± SD) of 66% ± 25% (see Supplemental Material, Table 5A). For PET products extracted by saline, 26 of 34 (76%) had detectable EA (Table 1) with a %RME2 of 64% ± 41% (see Supplemental Material, Table 5C). We found no consistent correlation between the percentage of items in a product type with detectable EA and their mean %RME2 (data not shown).
We found no significant difference (p > 0.05) in the percentage of items with detectable EA between those with contents and those with no contents (76%, n = 160) at the time of purchase based on the standard EtOH extraction protocol [67% vs. 70%; see Supplemental Material, Table 2A (doi:10.1289/ehp.1003220)], the standard saline protocol (62% vs. 75%; see Supplemental Material, Table 2C), or all extraction protocols combined (69% vs. 76%). Most important, items with no contents in all categories exhibited detectable EA in at least one protocol (see Supplemental Material, Tables 2 and 5), including 78% of items made from HDPE (n = 18), 57% from PP (n = 14), and 100% from PET (n = 6). Given all of these results, we present the data for all items shown in Tables 1 and 2 without regard to their content status.
Using different solvents increased the probability of detecting EA. Most (71%) unstressed plastic items released chemicals with reliably detectable EA in one or more extraction protocols, independent of resin type, product type, or retailer (Table 1). Results often differed between saline and EtOH extracts of the same unstressed plastic item, and EA was reliably detected most frequently (92% of all items listed in Table 2) when analyzed using both saline (more polar) and EtOH (less polar) extracts. For example, 15% of unstressed HDPE plastic items leached chemicals with detectable EA into both EtOH and saline extracts, 15% leached only into EtOH, and 31% leached only into saline (Table 2). That is, the leaching of a chemical with EA was significantly (p < 0.01) more likely to be detected if we used both polar and nonpolar solvents (61%) than if we used only one solvent (30% for EtOH only or 45% for saline only). We obtained similar results for all types of plastic products (data not shown).
Assays of > 100 component parts from > 20 different baby bottles, including many advertised as BPA free, indicated that extracts of at least one bottle component of each baby bottle always had EA based on at least one assay (some data shown in Table 2 and Figure 2), as did at least one other component part (data not shown).
Stresses increased the release of chemicals having EA. Leaching of chemicals with EA was increased by common stresses. For example, one unstressed sample of an HDPE resin (P5 in Table 3) that had no detectable EA (i.e., RME2 < 15%) in two saline extracts and two EtOH extracts released chemicals with EA equivalent to 47% RME2 when extracted using EtOH after the resin was stressed with UV light. Similarly, two samples of low-density PE resins (LDPE resins 1 and 2) and PETG resins (PETG baby bottle and PETG resin 1) that had no detectable EA before stressing subsequently exhibited EA when stressed, especially by UV (Table 3). Samples (n > 10) of products made from PETG resins advertised as BPA free all released detectable EA when stressed, especially by UV light. Similarly, 25% of unstressed samples of PET and 50% of unstressed PS products surveyed did not have detectable EA in assays of EtOH and/or saline extracts (Table 1). However, when stressed and assayed using both saline and EtOH extracts, all PET (n > 10) and PS (n > 10) products released chemicals having detectable EA in at least one extracting solvent (Table 3).
EA-containing and EA-free monomers. Polymerization of monomers is rarely complete, and unpolymerized monomers are almost always released from polymer resins (Begley et al. 1990, 2005; De Meulenaer and Huyghebaert 2004). PE and PP polymers are often used to manufacture flexible and/or nontransparent rigid products (Figure 3). MCF-7 assays (n = 6) consistently showed that extracts of “barefoot” (no additives) polymers (e.g., LDPE resin P1 in Table 3) were EA free, even when stressed. (PP-based polymers require antioxidants to prevent severe degradation during their use in manufacturing plastic products.) Furthermore, PE- and PP-based resins containing appropriate additives to produce fit-for-use products could be constructed that remained EA free (n > 100 assays of > 10 resins), even when exposed to common-use stresses. Representative data from several such resins (LDPE resin P1, HDPE resin P2, PP homopolymer resin P3, PP copolymer resin P4) are shown in Table 3.Figure 3. Click for Larger Image.
Properties of monomers and polymers used to make common resins.
Figure 3 also shows other monomers and polymers that can or cannot be used to make hard-and-clear (HC) plastics. For example, HC PC plastics (n > 10) all released chemicals having EA (e.g., PC baby bottle B1 and PC water bottle W1 in Figure 2), almost certainly phenolics such as BPA (Figure 1B). The dimethyl terephthalate monomer used to make PET and PETG plastics exhibited anti-EA (n = 3 assays; data not shown; for anti-EA assay protocol, see Supplemental Material (doi:10.1289/ehp.1003220)]. Furthermore, breakdown products of dimethyl terephthalate, PET, and PETG resins probably contain and release phenolic moieties that have EA that account for some of the data for PET products in Tables 1 and 2. Polyethersulfone HC products also consistently released chemicals having EA or anti-EA, especially when stressed with UV light (data not shown), possibly from unreacted phenolic monomer residues or phenolic stress-degradation products. In contrast, some HC cyclic olefin polymer/cyclic olefin copolymer polymers produced from saturated cyclic olefin monomers contained no phenolics and did not release chemicals having detectable EA, even when stressed (Table 3).
Polymers that can be made EA free have a similar cost compared with polymers made from monomers that have EA. For example, currently, clarified PP having no additives that exhibit EA (even when stressed) that is suitable for molding bottles costs approximately $1.20/lb. PP resins containing additives that have EA also cost about $1.20/lb. Commodity resins such as PET, which are made from monomers having EA and are suitable for molding bottles, are priced at approximately $1.28/lb (Plastics News 2011).
EA-containing and EA-free additives. Many additives are physically, but not chemically, bound to a polymeric structure and hence can almost always leach from the polymer, especially when stressed (Begley et al. 1990, 2005; De Meulenaer and Huyghebaert 2004). Antioxidants are the most critical class of additives because they prevent or minimize plastic degradation due to oxidation that breaks polymer chains (chain scission) and/or causes cross-links (Kattas et al. 2000). The oldest and most common antioxidants deemed suitable for food contact belong to a chemical class known as HPs (hindered phenols), such as BHT and BHA, in large part because both are inexpensive and assumed to be nontoxic. However, BHT (n = 4 assays) had reliably detectable EA, as did BHA (n = 3 assays). [The EC50 of BHT and BHA (Figure 1C) could not be accurately calculated because both also exhibited cellular toxicity at higher concentrations (10–5 M).] Other commonly used HP antioxidants (n = 4/5) and organophosphines (n = 6/7) also exhibited reliably detectable EA, especially when exposed to moist heat, which presumably causes hydrolysis (data not shown). For example, proprietary antioxidants Phos (phosphate) OX 1 and HP AOX 2 had no detectable EA, whereas HP AOX 1 and Ph (bisphenol) AOX 1 had reliably detectable EA [see Supplemental Material, Table 3 (doi:10.1289/ehp.1003220)].
Many other additives (n > 50) with a phenolic group had reliably detectable EA, such as agents found in many base resins [tris(nonylphenyl) phosphite, octylphenol, nonylphenol, butylbenzene phthalate], colorants (especially blues or greens with phthalocyanine groups), PS-based purge compounds, and mold-release agents [see Supplemental Material, Table 4 (doi:10.1289/ehp.1003220)]. In contrast, many metal- oxide–based inorganic pigments did not exhibit EA. However, these EA-free pigments are often mixed with dispersing agents and carrier resins that have EA to produce colorant masterbatch concentrates. Nevertheless, we have identified resins, dispersants, pigments, and antioxidants that are approved by the Food and Drug Administration for direct food contact (see Supplemental Material, Tables 3 and 4) to create colorant masterbatch concentrates (n > 100) that produce even colorant dispersion into plastics and that have no detectable EA, cellular toxicity, or adverse processing effects, even when stressed.
Because additives comprise a small fraction (typically 0.1–1% by weight) of plastic resins and compounds and because plastic resins and compounds using EA-free additives are processed during manufacture in a nearly identical manner as conventional resins and compounds containing chemicals with EA, the replacement of additives having EA with EA-free additives should have very little impact on the cost of the final product. Furthermore, EA-free additives have only a slightly higher or no additional cost compared with additives with EA, so that their cost impact is very small or nonexistent.
Products currently marketed as BPA free are not EA free. In response to market and regulatory pressures to eliminate BPA in HC plastics, BPA-free HC materials have recently been introduced as replacements for PC resins. PET and PETG are two such resins, but HC plastic products made from these resins leached chemicals that had detectable EA (Tables 1–3, Figures 2 and 3), often in the absence of exposure to common-use stresses. Two popular brands of water bottles made from a PETG resin now marketed as an HC BPA-free replacement also released chemicals having significant EA (W1, W2, W3, and W4; Table 3, Figures 2 and 3), as did uncompounded PETG resins (Table 3). Most PE/PP-based plastic products were presumably BPA free but nevertheless had readily detectable EA (Tables 1 and 2), almost certainly due to one or more additives having EA. Many components of BPA-free baby bottles had reliably detectable EA (22–95% RME2) when extracted in either saline or EtOH, including the bottle, nipple, anticolic device, and liner (data not shown).
In fact, all BPA-replacement resins or products tested to date (n > 25) released chemicals having reliably detectable EA (data not shown), including polyethersulfone and PETG, sometimes having more total EA measured as %RME2 than many PC products when stressed. For example, the %RME2 released by various BPA-free baby and water bottle component parts extracted by saline or EtOH solutions and exposed to one or more common-use stresses can be greater than PC products under the same conditions (Figure 2). UV stress, in particular, often leads to the release of chemicals having greater EA than BPA-containing HC plastics currently sold. For example, saline extracts of BPA-free baby bottle B3 (Figure 2) after exposure to UV showed greater EA than did any of the PC baby bottle extracts after any of the stresses. Saline extracts from BPA-free baby bottle B1 after any of the stresses (microwave, autoclave, or UV) showed greater EA than did the saline extracts from PC baby bottle B2 after any of the stresses. EtOH extracts from BPA-free baby bottle B1 after UV stress showed greater EA than extracts from PC baby bottle B1. Saline extracts from BPA-free baby bottle B2 after microwave or autoclave stresses showed greater EA than did saline extracts from PC baby bottles B1 or B2 after any of the stresses. Note also in Figure 2 that multiple extracts of the same product using the same solvent/stress combination typically gave rather similar %RME2 data, but different solvent/stress combinations gave very different results, from very high EA to nondetectable EA. For example, EtOH extracts from PC baby bottle B2 showed very high EA under all stress conditions, whereas saline extracts of the same bottle under the same stress conditions showed no detectable EA. Hence, to reliably detect EA, plastic resins or products must be extracted with both polar and nonpolar solvents and exposed to common-use stresses.Discussion
Most plastic products release chemicals having EA. Our data show that both more polar (e.g., saline) and less polar (e.g., EtOH) solvents should be used to extract chemicals from plastics because the use of only one solvent significantly reduces the probability of detecting chemicals having EA. The ability to detect more polar and less polar chemicals having EA is important because plastic containers may hold either type of liquid or a liquid that is a mixture of more polar and less polar solvents (e.g., milk). When both more polar and less polar solvents are used, most newly purchased and unstressed plastic products release chemicals having reliably detectable EA independent of the type of resin used in their manufacture, type of product, processing method, retail source, and whether the product had contents before testing. However, the lack of significant difference in average percentage having detectable EA between plastic items with and without contents does not imply that the contents do not affect the total EA or specific chemicals having EA released by individual plastic items.
Our data show that most monomers and additives that are used to make many commercially available plastic items exhibit EA. Even when a “barefoot” polymer (no additives) such as PE or polyvinyl chloride does not exhibit EA, commercial resins and products from these polymers often release chemicals (almost certainly additives) having EA.
We found that exposure to one or more common-use stresses often increases the leaching of chemicals having EA. In fact, our data suggest that almost all commercially available plastic items would leach detectable amounts of chemicals having EA once such items are exposed to boiling water, sunlight (UV), and/or microwaving. Our findings are consistent with recently published reports that PET products release chemicals having EA (Wagner and Oehlmann 2009) and that different PET products leach different amounts of EA. For example, different PET products release different amounts of EA measured as %E2 or %RME2 [see Supplemental Material, Table 5C (doi:10.1289/ehp.1003220)], almost certainly because different PET copolymer manufacturers choose different monomers, additive packages, and synthetic processes to produce PET copolymer resins.
Our data are consistent with the hypotheses that the presence of a phenolic moiety is the best predictor of whether a chemical exhibits EA and that benzene moieties often probably convert to phenolic moieties when the monomer and/or polymer is exposed to one or more manufacturing or common-use stresses. For example, although in theory most organophosphites (antioxidants commonly used with HPs to provide synergistic oxidation protection) in their unaltered state should not bind to ERs [see Supplemental Material, Table 1 (doi:10.1289/ehp.1003220)], organophosphites are hydrolytically unstable and often produce phenols when exposed to water (Kattas et al. 2000). Most organophosphite antioxidants we tested exhibited detectable EA (data not shown).
Likewise, various additives that are high-molecular-weight HPs do not have EA, but if exposed to moist heat they can undergo hydrolysis and produce lower-molecular-weight phenolics that have EA. Therefore, antioxidants and other additives should be tested for EA both in their original, unstressed form and after stressing. We can identify monomers and additives (antioxidants, clarifiers, slip agents, colorants, inks, etc.) having no detectable EA for use at all stages of manufacturing processes to make flexible nontransparent or HC plastic items that are EA free, even after exposure to common-use stresses. All of our data suggest that, when both are manufactured in comparable quantities, carefully formulated EA-free plastic products could have all the fit-for-use properties of current EA-releasing products at minimal additional cost.
BPA free is not EA free. Although most items listed in Tables 1–3 would not be expected to contain BPA, nevertheless almost all stressed plastic items tested leached chemicals having reliably detectable EA measured as %RME2 if extracted with both more polar and less polar solvents. In response to market and regulatory pressures, BPA-free PET or PETG resins and products have recently been introduced as replacements for PC resins. However, all such replacement resins and products tested to date release chemicals having EA (measured as %RME2), sometimes having more EA than BPA-containing PC resins or products, especially when stressed by UV light (Figure 2, Table 3). Monomer or polymer breakdown products that have EA account for some of this EA, but the rest of the measured EA is almost certainly due to release of additives having EA in BPA-free products, including the bottle and many component parts of baby bottles advertised as BPA free.
Avoiding a potential health problem. We recognize that we quantitatively measured EA relative to E2 (EC50 or %RME2) using sensitive assay and extraction protocols. Furthermore, it is almost impossible to gauge how much EA anyone is exposed to, given such unknowns as the number of chemicals having EA, their relative EA, their release rate under different conditions, and their metabolic degradation products or half-lives in vivo. In addition, the appropriate levels of EA in males versus females at different life stages are currently unknown. Nevertheless, a) in vitro data overwhelmingly show that exposures to chemicals having EA (often in very low doses) change the structure and function of many human cell types (Gray 2008); b) many in vitro and in vivo studies document in detail cellular/molecular/systemic mechanisms by which chemicals having EA produce changes in various cells, organs, and behaviors (Gray 2008); and c) recent epidemiological studies (Gray 2008; Koch and Calafat 2009; Meeker et al. 2009; Swan et al. 2005; Talsness et al. 2009; Thompson et al. 2009) strongly suggest that chemicals having EA produce measurable changes in the health of various human populations (e.g., on the offspring of mothers given diethylstilbestrol, or sperm counts in Danish males and other groups correlated with BPA levels in body tissues).
Many scientists believe that it is not appropriate to bet our health and that of future generations on an assumption that known cellular effects of chemicals having EA released from most plastics will have no severe adverse health effects (Gray 2008; Talsness et al. 2009; Thompson et al. 2009). Because we can identify existing, relatively inexpensive monomers and additives that do not exhibit EA, even when stressed, we believe that plastics having comparable physical properties but that do not release chemicals having detectable EA could be produced at minimal additional cost.Supplemental Material References
- Begley T, Castle L, Feigenbaum A, Franz R, Hinrichs K, Lickly T, et al. 2005. Evaluation of migration models that might be used in support of regulations for food-contact plastics. Food Addit Contam 22:73–90. Find this article online
- Begley TH, Dennison JL, Hollifield HC. 1990. Migration into food of polyethylene terephthalate (PET) cyclic oligomers from PET microwave packaging. Food Addit Contam 7:797–803. Find this article online
- Burton K.. 1956. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 62:315–323. Find this article online
- Della Seta D, Minder I, Belloni V, Aloisi AM, Dessi-Fulgheri F, Farabollini F. 2006. Pubertal exposure to estrogenic chemicals affects behavior in juvenile and adult male rats. Horm Behav 50:301–307. Find this article online
- De Meulenaer B, Huyghebaert A 2004. Packaging and other food contact material residues. In: Handbook of Food Analysis. 2nd edVol 2 (Nollet LML, ed)New York: Marcel Dekker. pp. 1297–1330.
- Gray J, ed 2008. 5th edState of the Evidence: The Connection between Breast Cancer and the Environment. Breast Cancer Fund. Available: http://www.breastcancerfund.org/assets/pdfs/publications/state-of-the-evidence-2010.pdf [accessed 4 June 2011]
- Hewitt SC, Deroo BJ, Korach KS. 2005. Signal transduction: a new mediator for an old hormone? Science 307:1572–1573. Find this article online
- ICCVAM (Interagency Coordinating Committee on the Validation of Alternative Methods) 2003. ICCVAM Evaluation of In Vitro Test Methods for Detecting Potential Endocrine Disruptors: Estrogen Receptor and Androgen Receptor Binding and Transcriptional Activation Assays. NIH Publication No. 03-4503. Available: http://iccvam.niehs.nih.gov/docs/endo_docs/edfinalrpt0503/edfinrpt.pdf [accessed 3 November 2010]
- ICCVAM (Interagency Coordinating Committee on the Validation of Alternative Methods) 2006. Addendum to ICCVAM Evaluation of In Vitro Test Methods for Detecting Potential Endocrine Disruptors: Estrogen Receptor and Androgen Receptor Binding and Transcriptional Activation Assays. NIH Publication No. 03-4503. Available: http://iccvam.niehs.nih.gov/docs/endo_docs/EDAddendFinal.pdf [accessed 3 November 2010]
- Kabuto H, Amakawa M, Shishibori T.. 2004. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci 74:2931–2940. Find this article online
- Kattas L, Gastrock F, Levin I, Cacciatore A 2000. Plastics additives. In: Modern Plastics Handbook (Harper CA, ed). 1st edNew York: McGraw-Hill. pp. 4.1–4.69.
- Kavlock RJ, Daston GP, DeRosa C, Fenner-Crisp P, Gray LE, Kaattari S, et al. 1996. Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a U.S. EPA-sponsored workshop. Environ Health Perspect ( suppl 104715–740. Find this article online
- Koch HM, Calafat AM. 2009. Human body burdens of chemicals used in plastics manufacture. Phil Trans R Soc B 364:2063–2078. Find this article online
- Leusch FDL, de Jager C, Levi Y, Lim R, Puijker L, Sacher F, et al. 2010. Comparison of five in vitro bioassays to measure estrogenic activity in environmental waters. Environ Sci Technol 44:3853–3860. Find this article online
- Matsushima A, Teramoto T, Okada H, Liu X, Tokunaga T, Kakuta Y, et al. 2008. ERRγ tethers strongly bisphenol A and 4-α-cumylphenol in an induced-fit manner. Biochem Biophys Res Commun 373(3):408–413. Find this article online
- Meeker JD, Sathyanarayana S, Swan SH. 2009. Phthalates and other additives in plastics: human exposure and associated health outcomes. Philos Trans R Soc Lond B Biol Sci 364:2097–2113. Find this article online
- Natarajan N, Shambaugh GE III, Elseth KM, Haines GK, Radosevich JA. 1994. Adaptation of the diphenylamine (DPA) assay to a 96-well plate tissue culture format and comparison with the MTT assay. BioTechniques 17:166–171. Find this article online
- National Research Council 1999. Hormonally Active Agents in the Environment. Washington, DC: National Academies Press.
- Newbold RR, Jefferson WN, Padilla-Banks E, Haseman J. 2004. Developmental exposure to diethylstilbestrol (DES) alters uterine response to estrogens in prepubescent mice: low versus high dose effects. Reprod Toxicol 18:399–406. Find this article online
- Patisaul HB, Fortino AE, Polston EK. 2006. Neonatal genistein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol Teratol 28:111–118. Find this article online
- Patisaul HB, Todd KL, Mickens JA, Adewale HB. 2009. Impact of neonatal exposure to the ERα agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology 30:350–357. Find this article online
- News Plastics. 2011. Resin Pricing Chart. 21(February):: 21–22. Find this article online
- Sax L.. 2010. Polyethylene terephthalate may yield endocrine disruptors. Environ Health Perspect 118:445–448. Find this article online
- Soto AM, Justicia H, Wray JW, Sonnenschein C. 1991. p-Nonyl-phenol: an estrogenic xenobiotic released from “modified” polystyrene. Environ Health Perspect 92:167–173. Find this article online
- Soto AM, Sonnenschein C, Chung KL, Fernandez MF, Olea N, Serrano FO. 1995. The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants. Environ Health Perspect 103: suppl 7113–122. Find this article online
- Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, et al. 2005. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 113:1056–1061. Find this article online
- Talsness CE, Andrade AJ, Kuriyama SN, Taylor JA, vom Saal FS. 2009. Components of plastic: experimental studies in animals and relevance for human health. Philos Trans R Soc Lond B Biol Sci 364:2079–2096. Find this article online
- Thompson RC, Swan SH, Moore CJ, vom Saal FS. 2009. Our plastic age. Philos Trans R Soc Lond B Biol Sci 364:1973–1976. Find this article online
- Till DE, Ehntholt DJ, Reid RC, Schwartz PS, Sidman KR, Schwope AD, et al. 1982. Migration of BHT antioxidant from high density polyethylene to foods and food simulants. Ind Eng Chem Prod Res Dev 21:106–113. Find this article online
- vom Saal FS, Nagel SC, Timms BG, Welshons WV. 2005. Implications for human health of the extensive bisphenol A literature showing adverse effects at low doses. Toxicology 212:244–252. Find this article online
- Wagner M, Oehlmann J.. 2009. Endocrine disruptors in bottled mineral water: total estrogenic burden and migration from plastic bottles. Environ Sci Pollut Res 16:278–286. Find this article online
Redwood Sorrel is in the Oxalidaceae, the wood sorrel family, a relatively small family with 3 genera and 875 species of mostly tropical and subtropical regions. Redwood sorrel can be used as a groundcover in cultivated landscapes as long as the conditions are shady and cool. Plants used for landscaping can be purchased from native plant nurseries. Seeds can also be collected from native habitats but not before proper permission and permits have been obtained from the appropriate agency or land owner. The collection of entire plants from wild populations is strongly discouraged.
Redwood sorrel is a perennial herb arising 5-20 cm (2-7.9 inches) from a scaly rhizome. Leaves are all basal and typically number fewer than 10. Petioles are 3 -20 cm (1.2-7.9 inches) long and covered with brown hairs. Leaf blades are clover like in appearance and 1 to 4.5 cm (0.4-1.8 inches) long. Single flowers arise above the height of the leaves on stalks (referred to as peduncles) that are covered with brown hairs similar to the petioles. Petals are white to pink in color and 13-20 mm (0.5-0.8 inches) long. Sepals are 5-10 mm (0.2-0.4 inches) long.
This species grows in cool, moist Douglas-fir and coastal redwood forests in the Cascade, Olympic, and Coast Mountains from southwest British Columbia to the San Francisco Bay area of California. Being adapted to shady environments, redwood sorrel is capable of photosynthesis at low light levels. Higher intensity light can damage the sensitive leaves. As a protective measure, leaves fold downward within several minutes when struck by direct light, a process known as nyctinasty.
Leaves of redwood sorrel are edible cooked or raw but are mildly toxic from the presence of oxalic acid. When consumed, they should be eaten in small quantities. Northwest tribes were known to eat redwood sorrel with dried fish. Native Americans would prepare decoctions of the entire plant to wash body parts affected by rheumatism. A poultice prepared from the plant was applied to boils and sores and used to draw out infection.For More Information
- This article was written by Russ Holmes.
Ethnobotany is the study of how people of a particular culture and region make use of indigenous (native) plants. Since their earliest origins, humans have depended on plants for their primary needs and existence. Plants provide food, medicine, shelter, dyes, fibers, oils, resins, gums, soaps, waxes, latex, tannins, and even contribute to the air we breathe. Many native peoples also used plants in ceremonial or spiritual rituals. Examining human life on earth requires understanding the role of plants in historical and current day cultures.Plants and People
Throughout time, countless peoples have tested and recorded the usefulness of plants. Those plants with beneficial uses were kept and utilized. Our cultures evolved by passing from generation to generation ever more sophisticated knowledge of plants and their usefulness. Even today, we depend upon plants and their important pollinators for our existence and survival.
- Native Plant Dyes
- Fabulous Fibers
- Native Plant Oils
- Medicinal Botany
- Plants of Mind and Spirit
- Wild Crop Progenitors
Great Lakes Anishinaabe Ethnobotany
The Great Lakes Anishinaabe Ethnobotany site website is a collaboration between the Cedar Tree Institute and the Northern Michigan University Center for Native American Studies both located in Marquette, Michigan, and the USDA Forest Service. The website features video interviews, a collection of personal stories and cultural teachings related to various plants and trees of the upper Great Lakes region.
Medicinal Plants of the Southwest (MPSW)
The Medicinal Plants of the Southwest (MPSW) program, is funded by the National Institute of Health as part of the Research Initiative for Scientific Enhancement (RISE) Program at NMSU.
Native American Ethnobotany
A database of foods, drugs, dyes, and fibers of Native American peoples, derived from plants, hosted on the University of Michigan, Dearborn website.
Wings and Seeds: The Zaagkii Project, A Native Plants and Pollinator Protection Initiative
The Zaagkii Project (Anishinaabe for “The love that comes from the Earth”) is a collaborative effort between the Cedar Tree Institute, the United States Forest Service, and the Keweenaw Bay Indian Community.
Culturally and Economically Important Nontimber Forest Products of Northern Maine
A USDA Forest Service Northern Research Station Sustaining Forests web page introducing the cultural and ecological landscape of northern Maine and its Canadian neighbors through the non-timber forest products that grow there and the people who gather and depend on them.
In strong sunlight, male Rufous hummingbirds put on quite a show with throat feathers flashing, a reddish orange iridescence brighter than a neon sign.The Rufous Hummingbird:
Small but Feisty Long-Distance Migrant
Many western and southwestern gardeners know the Rufous hummingbird (Selasphorus rufus) as a delightful often-unexpected visitor to colorful garden wildflowers or hummingbird feeders. These amazing small but feisty birds (only 3 inches or 8cm long) weigh merely three or four grams; for comparison, a United States penny weighs slightly about 2.5 grams). These birds are amazing aerialists, darting in and out, and can be relentless attackers of other birds and insects at feeders and flowers. They have long slender nearly straight bills. Their wings are relatively short and do not reach the end of the tail when the birds are perched on a feeder or nearby branches. They are also one of the few North American hummingbirds to migrate long distances. Rufous hummingbirds are a western species, rarely straying into the eastern United States.
In strong sunlight, male Rufous put on quite a show with throat feathers flashing, a reddish orange iridescence brighter than a neon sign. Adult Rufous hummingbirds are often be confused with Allen’s hummingbirds (Selasphorus sasin). Allen’s hummingbirds have elongated scarlet gorget (throat) feathers. The tops of their heads and backs are a bronze or bronze-green in metallic shades. The sides of the face and flanks are often a rufous or cinnamon color, their chest is white, and there is a small white spot behind their black eye. Sometimes the feathers on the back of Allen’s males have a greenish color. However, if you notice any completely rufous (or rusty) feathers on their backs, you are looking at a Rufous hummingbird. Males of both species are more easily identified, but juvenile and female Rufous and Allen’s hummingbirds are virtually indistinguishable on the wing, especially during their migratory periods when their ranges overlap.
Although not the largest hummingbirds, Rufous are feisty, especially the males who chase and drive other hummers and large insects from their feeding territories. Rufous are pugnacious little birds. Feeding does not only include sucrose-rich floral nectars, Rufous have a high protein diet that comes from small insects. Various flies, wasps, bees and other small insects are consumed during high-speed encounters where birds splaying their bills open gulp down a meal as revealed in high-speed cinematography of captive individuals. Rufous, along with other hummingbirds, also practice a bit of larceny by stealing insects already caught in spider webs.
Rufous hummingbirds exhibit amazing flight endurance on long-distance north and south migrations from southern Alaska to southernmost Mexico. These birds spend a large proportion of their time on the move following the bloom of their favorite plants. As champion migrants, they spend their summer breeding period, to the north in Washington, Oregon and westernmost Canada. Like some warmth-loving human tourists they spend their winter non-breeding months in southern Mexico especially in wooded areas in the state of Guerrero. Rufous make an annual circuit of the western states. Just passing through, they move into portions of California, Nevada, Utah, Colorado, Arizona, and New Mexico. Some Rufous individuals have been banded and are known to fly 2,000 miles during their migratory transits, and to live to an average ripe old age of eight years old. At 3,600 wing beats per minute, that is a huge amount of effort and energy expended for these sugar-loving animals. They routinely fly at 25 miles per hour but some species reach 50 mph in courtship displays.
In the southwestern deserts of the USA and Mexico, Rufous hummingbirds can be found feeding and defending their favorite blossoms. Some of these include: tree morning glories (Ipomoea arborescens), ocotillo (Foquieria splendens and F. macdougalii), various red mint flowers (Salvia elegans and Stachys coccinea), along with “shrimp plant” (Justicia californica and J. candicans).For Additional Information
Become a citizen scientist and learn other fascinating information about Rufous hummingbirds on these websites. Your observations are important data for monitoring programs including Project FeederWatch (Cornell), NestWatch, or the Hummingbird Monitoring Network.
- Cornell Laboratory of Ornithology, and its Project FeederWatch.
- Journey North, sponsored by the Annenberg Foundation, for information on hummingbirds, monarch butterflies and other migratory animals.
- Arizona-Sonora Desert Museum, Center for Sonoran Desert Studies, Migratory Pollinators Program, Rufous hummingbirds.
- The Hummingbird Monitoring Network, a non-profit conservation organization that supports projects to improve hummingbird’s ability to survive and reproduce.
- This article was written by Stephen Buchmann of the Pollinator Partnership
The International Human Dimensions Programme on Global Environmental Change (IHDP)* announced at the Rio+20 Summit on June 17, 2012. the launch of the Inclusive Wealth Report 2012 (IWR 2012). The report measures the wealth of nations.Inclusive Wealth Report 2012
The report presents a new economic index, which looks beyond the traditional short term economic and development yardsticks of gross domestic product (GDP) and the Human Development Index (HDI). The Inclusive Wealth Index (IWI) assesses changes in a country’s productive base, including produced, human, and natural capital over time. By taking a more holistic approach, the IWI shows governments the true state of their nation’s wealth and the sustainability of its growth.
Twenty countries were assessed in the IWR 2012 over a period of 19 years (1990-2008). Together they represent more than half of the world population and almost three quarters of world GDP and include high, middle, and low-income economies on all continents.IWI Per Capita Compared to GDP Per Capita and HDI Average annual economic performance of 20 countries when assessed with Inclusive Wealth Index (IWI) per capita, Gross Domestic Product (GDP) per capita and Human Development Index (HDI) over a period of 19 years (1990-2008). Credit: UNU-IHDP.
This is the first of a series of reports that will be published every two years to monitor the well-being and sustainability of countries.
A Summary for Decision-Makers of the IWR 2012 is also available, print copies of which can be picked up at the UNU booth as well. To obtain the digital copy or sign up to order a print copy, please refer to the Website of the Inclusive Wealth Report.
Key findings from the report are:
- While 19 out of the 20 countries experienced a decline in natural capital, six also saw a decline in their inclusive wealth, putting them on an unsustainable track, Russia, Venezuela, Saudi Arabia, Colombia, South Africa and Nigeria were the nations that failed to grow. The remaining 70 per cent of countries show IWI per-capita growth, indicating sustainability.
- High population growth with respect to IWI growth created unsustainable conditions in five of the six countries mentioned above. Russia's lack of growth was due largely to a drop in manufactured capital
- 25 per cent of countries which showed a positive trend when measured by GDP per capita and HDI were found to have a negative IWI per capita. The primary driver of the difference in performance was the decline in natural capital
- With the exception of France, Germany, Japan, Norway, the United Kingdom and the United States, all countries surveyed have a higher share of natural capital than manufactured capital, highlighting its importance
- Human capital has increased in every country and is the prime capital form that offsets the decline in natural capital in most economies
- There are clear signs of trade-off effects between the different forms of capital
- Technological innovation and/or oil capital gains (due to rising prices) outweigh decline in natural capital and damages from climate change, moving a number of countries – Russia, Nigeria, Saudi Arabia and Venezuela - from an unsustainable to a sustainable trajectory
- Estimates of inclusive wealth can be improved significantly with better data on the stocks of natural, human and social capital and their values for human well-being.
While inclusive wealth has increased for most countries, the report shows that an examination of natural capital is crucial for policy makers.
Even though a reduction in natural capital can be offset by the accumulation of manufactured and human capital, which are reproducible, many natural resources such as oil and minerals cannot be replaced. As a result, a more inclusive definition of wealth that will secure a legacy for future generations is urgently needed in the discussion of sustainable economic and social development.
The report, which will be produced every two years, makes the following specific recommendations:
- Countries witnessing diminishing returns in natural capital should invest in renewable natural capital to improve their IWI and the well-being of their citizens. Example investments include reforestation and agricultural biodiversity
- Nations should incorporate the IWI within planning and development ministries to encourage the creation of sustainable policies
- Countries should speed up the process of moving from an income-based accounting framework to a wealth accounting framework
- Macroeconomic policies should be evaluated on the basis of IWI rather than GDP per capita
- Governments and international organizations should establish research programmes to value key components of natural capital, in particular ecosystems.
For inquiries, please send an email to email@example.comEditor's Note
- *The IWR 2012 is a joint initiative of the International Human Dimensions Programme on Global Environmental Change (UNU-IHDP) hosted by the United Nations University and the United Nations Environment Programme (UNEP), in collaboration with the UN-Water Decade Programme on Capacity Development (UNW-DPC) and the Natural Capital Project.
Rapid environmental change, whether human induced such as fishing and hunting pressures, toxic chemicals, or natural climatic changes resulting in altered food availability have provided opportunities to observe rapid microevolutionary changes in contemporary time, or contemporary evolution. These are population level changes which tend to occur over a few centuries or much less time (depending on the species) and may be observed after only a relatively small number of generation cycles depending on the species. Well known examples of contemporary evolution include pesticide and antibiotic resistance. Yet we now know that animals other than pest species can evolve in response to rapid environmental change (including chemical expsoures).
However distinguishing rapid, adaptive genetic change from phenotypic plasticity (altered phenotypic expression of a single genotype in response to environmental change – or nongenetic change) can be difficult, particularly in longer-lived species with long generation times, without rigorous analysis such as detailed studies of genetic markers (specific and well characterized portions of the genome) or long-term studies of isolated populations. Phenotypic plasticity has some advantages over genetic adaptation in that plastic phenotypes have a greater potential to reverse should conditions revert – although genetic adaptation has been observed to reverse as well. Sometimes the distinction becomes less important as phenotypic plasticity may eventually contribute to adaptive genetic change by providing some of the variabiilty upon which selection may act.Selected examples of contemporary evolution Historical Studies
One of the best documented examples of genetic adaptive change in response to human activity are the peppered moths of industrial England. As industries in England increasingly burned coal, the wild-type (more prevalent) light colored moths which settled onto tree trunks became more susceptible to bird predation as trees became darkened with soot. The frequency with which dark morphs of the peppered moths appeared in local populations rapidly increased. The dark-light morphs are heritable traits – meaning that changes in frequency was the result of rapid genetic adaptation. Interestingly as industrial emissions were reduced, moth populations eventually reverted back to the light-colored morph. Darwin’s finches (Geospiza fortis and Geospiza scandens), studied by Peter and Rosemary Grant provide another classic example of rapid adaptation in response to environmental change caused by fluctuations in climate, which altered available food. Over a 30-year period the Grant’s observed two species of Galapagos finches on Daphne Island, and found that populations experienced various episodes of genetic adaptation resulting in altered beak morphology and body size in response to food availability.Evolution in response to chemical contamination
More recently studies of two different fish species exposed to industrial contaminants (polychlorinated biphenyls, dioxins or similar classes of chemicals) over multiple generations have evolved resistance in their response to these and other like-acting chemicals. Studies involving over twenty distinct killifish populations (Fundulus heteroclitus) along the eastern United States by Diane Nacci, Andrew Whitehead and others demonstrate similar functional adaptations in one of the main receptors (the aryl hydrocarbon receptor or AhR) involved in the response to these chemicals. Additionally, a population of Atlantic tomcod (Microgadus tomcod) residing in the Hudson River, NY has also been identified as evolving a type of AhR resistance. In both instances resistance is the product of genetic adaptation. In the case of the killifish – distinct populations were maintained and bred under the same laboratory conditions for generations (essentially a type of "common garden experiment" which is designed to eliminate confounding by environmental conditions) enabling researchers to distinguish between plasticity as a result of local environment – and genetic adaptation. In the tomcod, a specific change in the genes encoding the AhR has been identified, which in turn alter the amino acid structure, and consequentially the PCB binding ability of the receptor.
As mentioned above, there are numerous examples of evolution in pest species in response to pesticides, and in bacteria in response to antibiotics.The Future
There is a great deal of interest in contemporary evolution (for reviews see the reading list below). Since populations may respond rapidly to overfishing or hunting pressure - understanding such rapid evolution may be useful for population managers. In addition to PCBs and like-acting chemicals animals are known to evolve resistance to industrial metal contamination and of course, pesiticides. While rapid evolution has been observed in just a few vertebrate species to date, it is likely that more species will be identified as more attention is focused on this phenomenon.
As humans continue to change the world's environment, teasing apart which species are likely to become resistant to rapid change (including industrial chemicals, climate change, or other environmental changes) will enable better prediction of which species will most likley be affected (and, in the worst case go extinct), and which species will most likely survive such changes.Further Reading
- Grant P, R Grant. 2002. Unpredictable evolution in a 30-year study of Darwin's finches. Science 296:707-711.
- Hansen M., I Olivieri, D Waller, E Nielsen, and the GeM Working Group. 2012. Molecular Ecology, 21:1311-1329
- Hendry A, M Kinnison. 1999. The pace of modern life: measuring rates of microevolution, Evolution 53:1637-1653
- Kinnison M, N Hairston. 2007. Eco-evolutionary consevation biology: contemporary evolution and the dynamics of persistance. Functional Ecology 21:444-45
- Palkovacs E, M Kinnison, C Correa, C Dalton, A Hendry. 2011. Fates beyond traits: ecological consequences of human-induced trait change. Evolutionary Applications 5:183-191.
- Whitehead A, W Pilcher, D Champlain, D Nacci. 2012. Common mechanism underlies repeated evolution of extreme polution tolerance. Proc. Biol. Sci. 279:427-433.