scientific research on endangered animals

Endangered Species

An endangered species is a type of organism that is threatened by extinction. Species become endangered for two main reasons: loss of habitat and loss of genetic variation.

Biology, Ecology, Geography, Conservation

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An endangered species is a type of organism that is threatened by extinction . Species become endangered for two main reasons: loss of habitat and loss of genetic variation . Loss of Habitat A loss of habitat can happen naturally. Nonavian dinosaurs , for instance, lost their habitat about 65 million years ago. The hot, dry climate of the Cretaceous period changed very quickly, most likely because of an asteroid striking Earth. The impact of the asteroid forced debris into the atmosphere , reducing the amount of heat and light that reached Earth’s surface. The dinosaurs were unable to adapt to this new, cooler habitat. Nonavian dinosaurs became endangered, then extinct . Human activity can also contribute to a loss of habitat. Development for housing, industry , and agriculture reduces the habitat of native organisms. This can happen in a number of different ways. Development can eliminate habitat and native species directly. In the Amazon rainforest of South America, developers have cleared hundreds of thousands of acres. To “clear” a piece of land is to remove all trees and vegetation from it. The Amazon rainforest is cleared for cattle ranches , logging , and ur ban use. Development can also endanger species indirectly. Some species, such as fig trees of the rainforest, may provide habitat for other species. As trees are destroyed, species that depend on that tree habitat may also become endangered. Tree crowns provide habitat in the canopy , or top layer, of a rainforest . Plants such as vines, fungi such as mushrooms, and insects such as butterflies live in the rainforest canopy. So do hundreds of species of tropical birds and mammals such as monkeys. As trees are cut down, this habitat is lost. Species have less room to live and reproduce . Loss of habitat may happen as development takes place in a species range . Many animals have a range of hundreds of square kilometers. The mountain lion ( Puma concolor ) of North America, for instance, has a range of up to 1,000 square kilometers (386 square miles). To successfully live and reproduce, a single mountain lion patrols this much territory. Urban areas , such as Los Angeles, California, U.S.A., and Vancouver, British Columbia, Canada, grew rapidly during the 20th century. As these areas expanded into the wilderness, the mountain lion’s habitat became smaller. That means the habitat can support fewer mountain lions. Because enormous parts of the Sierra Nevada, Rocky, and Cascade mountain ranges remain undeveloped, however, mountain lions are not endangered. Loss of habitat can also lead to increased encounters between wild species and people. As development brings people deeper into a species range, they may have more exposure to wild species. Poisonous plants and fungi may grow closer to homes and schools. Wild animals are also spotted more frequently . These animals are simply patrolling their range, but interaction with people can be deadly. Polar bears ( Ursus maritimus ), mountain lions, and alligators are all predators brought into close contact with people as they lose their habitat to homes, farms , and businesses. As people kill these wild animals, through pesticides , accidents such as collisions with cars, or hunting, native species may become endangered.

Loss of Genetic Variation Genetic variation is the diversity found within a species. It’s why human beings may have blond, red, brown, or black hair. Genetic variation allows species to adapt to changes in the environment. Usually, the greater the population of a species, the greater its genetic variation. Inbreeding is reproduction with close family members. Groups of species that have a tendency to inbreed usually have little genetic variation, because no new genetic information is introduced to the group. Disease is much more common, and much more deadly, among inbred groups. Inbred species do not have the genetic variation to develop resistance to the disease. For this reason, fewer offspring of inbred groups survive to maturity. Loss of genetic variation can occur naturally. Cheetahs ( Acinonyx jubatus ) are a threatened species native to Africa and Asia. These big cats have very little genetic variation. Biologists say that during the last Ice Age , cheetahs went through a long period of inbreeding. As a result, there are very few genetic differences between cheetahs. They cannot adapt to changes in the environment as quickly as other animals, and fewer cheetahs survive to maturity. Cheetahs are also much more difficult to breed in captivity than other big cats, such as lions ( Panthera leo ). Human activity can also lead to a loss of genetic variation. Overhunting and overfishing have reduced the populations of many animals. Reduced population means there are fewer breeding pairs . A breeding pair is made up of two mature members of the species that are not closely related and can produce healthy offspring. With fewer breeding pairs, genetic variation shrinks. Monoculture , the agricultural method of growing a single crop , can also reduce genetic variation. Modern agribusiness relies on monocultures. Almost all potatoes cultivated , sold, and consumed, for instance, are from a single species, the Russet Burbank ( Solanum tuberosum ). Potatoes, native to the Andes Mountains of South America, have dozens of natural varieties. The genetic variation of wild potatoes allows them to adapt to climate change and disease. For Russet Burbanks, however, farmers must use fertilizers and pesticides to ensure healthy crops because the plant has almost no genetic variation. Plant breeders often go back to wild varieties to collect genes that will help cultivated plants resist pests and drought, and adapt to climate change. However, climate change is also threatening wild varieties. That means domesticated plants may lose an important source of traits that help them overcome new threats. The Red List The International Union for Conservation of Nature (IUCN) keeps a “Red List of Threatened Species.” The Red List de fines the severity and specific causes of a species’ threat of extinction. The Red List has seven levels of conservation: least concern , near threatened , vulnerable, endangered, critically endangered , extinct in the wild , and extinct. Each category represents a different threat level. Species that are not threatened by extinction are placed within the first two categories—least concern and near-threatened. Those that are most threatened are placed within the next three categories, known as the threatened categories —vulnerable, endangered, and critically endangered. Those species that are extinct in some form are placed within the last two categories—extinct in the wild and extinct. Classifying a species as endangered has to do with its range and habitat, as well as its actual population. For this reason, a species can be of least concern in one area and endangered in another. The gray whale ( Eschrichtius robustus ), for instance, has a healthy population in the eastern Pacific Ocean, along the coast of North and South America. The population in the western Pacific, however, is critically endangered.

Least Concern Least concern is the lowest level of conservation . A species of least concern is one that has a widespread and abundant population. Human beings are a species of least concern, along with most domestic animals , such as dogs ( Canis familiaris ) and cats ( Felis catus ). Many wild animals, such as pigeons and houseflies ( Musca domestica ), are also classified as least concern. Near Threatened A near threatened species is one that is likely to qualify for a threatened category in the near future. Many species of violets , native to tropical jungles in South America and Africa, are near threatened, for instance. They have healthy populations, but their rainforest habitat is disappearing at a fast pace. People are cutting down huge areas of rainforest for development and timber . Many violet species are likely to become threatened. Vulnerable Species The definitions of the three threatened categories (vulnerable, endangered, and critically endangered) are based on five criteria: population reduction rate , geographic range, population size, population restrictions , and probability of extinction . Threatened categories have different thresholds for these criteria. As the population and range of the species decreases, the species becomes more threatened. 1) Population reduction rate A species is classified as vulnerable if its population has declined between 30 and 50 percent. This decline is measured over 10 years or three generations of the species, whichever is longer. A generation is the period of time between the birth of an animal and the time it is able to reproduce. Mice are able to reproduce when they are about one month old. Mouse populations are mostly tracked over 10-year periods. An elephant's generation lasts about 15 years. So, elephant populations are measured over 45-year periods. A species is vulnerable if its population has declined at least 50 percent and the cause of the decline is known. Habitat loss is the leading known cause of population decline. A species is also classified as vulnerable if its population has declined at least 30 percent and the cause of the decline is not known. A new, unknown virus , for example, could kill hundreds or even thousands of individuals before being identified. 2) Geographic range A species is vulnerable if its “ extent of occurrence ” is estimated to be less than 20,000 square kilometers (7,722 square miles). An extent of occurrence is the smallest area that could contain all sites of a species’ population. If all members of a species could survive in a single area, the size of that area is the species’ extent of occurrence. A species is also classified as vulnerable if its “ area of occupancy ” is estimated to be less than 2,000 square kilometers (772 square miles). An area of occupancy is where a specific population of that species resides. This area is often a breeding or nesting site in a species range. 3) Population size Species with fewer than 10,000 mature individuals are vulnerable. The species is also vulnerable if that population declines by at least 10 percent within 10 years or three generations, whichever is longer. 4) Population restrictions Population restriction is a combination of population and area of occupancy. A species is vulnerable if it is restricted to less than 1,000 mature individuals or an area of occupancy of less than 20 square kilometers (8 square miles). 5) Probability of extinction in the wild is at least 10 percent within 100 years. Biologists, anthropologists, meteorologists , and other scientists have developed complex ways to determine a species’ probability of extinction. These formulas calculate the chances a species can survive, without human protection, in the wild. Vulnerable Species: Ethiopian Banana Frog The Ethiopian banana frog ( Afrixalus enseticola ) is a small frog native to high- altitude areas of southern Ethiopia. It is a vulnerable species because its area of occupancy is less than 2,000 square kilometers (772 square miles). The extent and quality of its forest habitat are in decline. Threats to this habitat include forest clearance, mostly for housing and agriculture. Vulnerable Species: Snaggletooth Shark The snaggletooth shark ( Hemipristis elongatus ) is found in the tropical, coastal waters of the Indian and Pacific Oceans. Its area of occupancy is enormous, from Southeast Africa to the Philippines, and from China to Australia. However, the snaggletooth shark is a vulnerable species because of a severe population reduction rate. Its population has fallen more than 10 percent over 10 years. The number of these sharks is declining due to fisheries, especially in the Java Sea and Gulf of Thailand. The snaggletooth shark’s flesh, fins, and liver are considered high-quality foods. They are sold in commercial fish markets, as well as restaurants. Vulnerable Species: Galapagos Kelp Galapagos kelp ( Eisenia galapagensis ) is a type of seaweed only found near the Galapagos Islands in the Pacific Ocean. Galapagos kelp is classified as vulnerable because its population has declined more than 10 percent over 10 years. Climate change is the leading cause of decline among Galapagos kelp. El Niño, the natural weather pattern that brings unusually warm water to the Galapagos, is the leading agent of climate change in this area. Galapagos kelp is a cold-water species and does not adapt quickly to changes in water temperature.

Endangered Species 1) Population reduction rate A species is classified as endangered when its population has declined between 50 and 70 percent. This decline is measured over 10 years or three generations of the species, whichever is longer. A species is classified as endangered when its population has declined at least 70 percent and the cause of the decline is known. A species is also classified as endangered when its population has declined at least 50 percent and the cause of the decline is not known. 2) Geographic range An endangered species’ extent of occurrence is less than 5,000 square kilometers (1,930 square miles). An endangered species’ area of occupancy is less than 500 square kilometers (193 square miles). 3) Population size A species is classified as endangered when there are fewer than 2,500 mature individuals. When a species population declines by at least 20 percent within five years or two generations, it is also classified as endangered. 4) Population restrictions A species is classified as endangered when its population is restricted to less than 250 mature individuals. When a species’ population is this low, its area of occupancy is not considered. 5) Probability of extinction in the wild is at least 20 percent within 20 years or five generations, whichever is longer.

Endangered Species: Scimitar -horned Oryx The scimitar-horned oryx ( Oryx dammah ) is a species of antelope with long horns. Its range extends across northern Africa. Previously, the scimitar-horned oryx was listed as extinct in the wild because the last confirmed sighting of one was in 1988. However, the first group of scimitar-horned oryx was released back into the wild in Chad, in August 2016, and the population is growing. Overhunting and habitat loss, including competition with domestic livestock , are the main reasons for the decline of the oryx’s wild population. Captive herds are now kept in protected areas of Tunisia, Senegal, and Morocco. Scimitar-horned oryxes are also found in many zoos . Critically Endangered Species 1) Population reduction rate A critically endangered species’ population has declined between 80 and 90 percent. This decline is measured over 10 years or three generations of the species, whichever is longer. A species is classified as critically endangered when its population has declined at least 90 percent and the cause of the decline is known. A species is also classified as endangered when its population has declined at least 80 percent and the cause of the decline is not known. 2) Geographic range A critically endangered species’ extent of occurrence is less than 100 square kilometers (39 square miles). A critically endangered species’ area of occupancy is estimated to be less than 10 square kilometers (4 square miles). 3) Population size A species is classified as critically endangered when there are fewer than 250 mature individuals. A species is also classified as critically endangered when the number of mature individuals declines by at least 25 percent within three years or one generation, whichever is longer. 4) Population restrictions A species is classified as critically endangered when its population is restricted to less than 50 mature individuals. When a species’ population is this low, its area of occupancy is not considered. 5) Probability of extinction in the wild is at least 50 percent within 10 years or three generations, whichever is longer. Critically Endangered Species: Bolivian Chinchilla Rat The Bolivian chinchilla rat ( Abrocoma boliviensis ) is a rodent found in a small section of the Santa Cruz region of Bolivia. It is critically endangered because its extent of occurrence is less than 100 square kilometers (39 square miles). The major threat to this species is loss of its cloud forest habitat. People are clearing forests to create cattle pastures .

Critically Endangered Species: Transcaucasian Racerunner The Transcaucasian racerunner ( Eremias pleskei ) is a lizard found on the Armenian Plateau , located in Armenia, Azerbaijan, Iran, and Turkey. The Transcaucasian racerunner is a critically endangered species because of a huge population decline, estimated at more than 80 percent during the past 10 years. Threats to this species include the salination , or increased saltiness, of soil . Fertilizers used for agricultural development seep into the soil, increasing its saltiness. Racerunners live in and among the rocks and soil, and cannot adapt to the increased salt in their food and shelter. The racerunner is also losing habitat as people create trash dumps on their area of occupancy. Critically Endangered Species: White Ferula Mushroom The white ferula mushroom ( Pleurotus nebrodensis ) is a critically endangered species of fungus. The mushroom is critically endangered because its extent of occurrence is less than 100 square kilometers (39 square miles). It is only found in the northern part of the Italian island of Sicily, in the Mediterranean Sea. The leading threats to white ferula mushrooms are loss of habitat and overharvesting. White ferula mushrooms are a gourmet food item. Farmers and amateur mushroom hunters harvest the fungus for food and profit. The mushrooms can be sold for up to $100 per kilogram (2.2 pounds). Extinct in the Wild A species is extinct in the wild when it only survives in cultivation (plants), in captivity (animals), or as a population well outside its established range. A species may be listed as extinct in the wild only after years of surveys have failed to record an individual in its native or expected habitat.

Extinct in the Wild: Monut Kaala Cyanea The Mount Kaala cyanea ( Cyanea superba ) is a large, flowering tree native to the island of Oahu, in the U.S. state of Hawai‘i. The Mount Kaala cyanea has large, broad leaves and fleshy fruit. The tree is extinct in the wild largely because of invasive species. Non-native plants crowded the cyanea out of its habitat, and non-native animals such as pigs, rats, and slugs ate its fruit more quickly than it could reproduce. Mount Kaala cyanea trees survive in tropical nurseries and botanical gardens . Many botanists and conservationists look forward to establishing a new population in the wild. Extinct A species is extinct when there is no reasonable doubt that the last remaining individual of that species has died. Extinct: Cuban Macaw The Cuban macaw ( Ara tricolor ) was a tropical parrot native to Cuba and a small Cuban island, Isla de la Juventud. Hunting and collecting the birds for pets led to the bird’s extinction. The last specimen of the Cuban macaw was collected in 1864. Extinct: Ridley’s Stick Insect Ridley’s stick insect ( Pseudobactricia ridleyi ) was native to the tropical jungle of the island of Singapore. This insect, whose long, segmented body resembled a tree limb, is only known through a single specimen, collected more than 100 years ago. During the 20th century, Singapore experienced rapid development. Almost the entire jungle was cleared, depriving the insect of its habitat.

Endangered Species and People When a species is classified as endangered, governments and international organizations can work to protect it. Laws may limit hunting and destruction of the species’ habitat. Individuals and organizations that break these laws may face huge fines. Because of such actions, many species have recovered from their endangered status. The brown pelican ( Pelecanus occidentalis ) was taken off the endangered species list in 2009, for instance. This seabird is native to the coasts of North America and South America, as well as the islands of the Caribbean Sea. It is the state bird of the U.S. state of Louisiana. In 1970, the number of brown pelicans in the wild was estimated at 10,000. The bird was classified as vulnerable. During the 1970s and 1980s, governments and conservation groups worked to help the brown pelican recover. Young chicks were reared in hatching sites, then released into the wild. Human access to nesting sites was severely restricted. The pesticide DDT , which damaged the eggs of the brown pelican, was banned. During the 1980s, the number of brown pelicans soared. In 1988, the IUCN “delisted” the brown pelican. The bird, whose population is now in the hundreds of thousands, is now in the category of least concern.

Convention on Biological Diversity The Convention on Biological Diversity is an international treaty to sustain and protect the diversity of life on Earth. This includes conservation, sustainability, and sharing the benefits of genetic research and resources. The Convention on Biological Diversity has adopted the IUCN Red List of endangered species in order to monitor and research species' population and habitats. Three nations have not ratified the Convention on Biological Diversity: Andorra, the Holy See (Vatican), and the United States.

Lonesome George Lonesome George was the only living member of the Pinta Island tortoise ( Chelonoidis abingdoni ) known to exist. The Pinta Island tortoise was only found on Pinta, one of the Galapagos Islands. The Charles Darwin Research Station, a scientific facility in the Galapagos, offered a $10,000 reward to any zoo or individual for locating a single Pinta Island tortoise female. On June 25, 2012, Lonesome George died, leaving one more extinct species in the world.

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Article Contents

Does scientific research contribute to species conservation, dependent variable, predictor factors, protected area and other factors, regional research benefits species conservation, global research did not predict species recovery, acknowledgements.

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Regional scientific research benefits threatened-species conservation

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Yisi Hu, Zhenhua Luo, Colin A Chapman, Stuart L Pimm, Samuel T Turvey, Michael J Lawes, Carlos A Peres, Tien Ming Lee, Pengfei Fan, Regional scientific research benefits threatened-species conservation, National Science Review , Volume 6, Issue 6, November 2019, Pages 1076–1079, https://doi.org/10.1093/nsr/nwz090

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Although conventional wisdom considers knowledge of threatened species' ecology and status essential for conservation, few studies demonstrate this in a quantitative way across many species and within the same political entity. Here, we evaluated the impacts of scientific research against conservation interventions (including funding) and species-level correlates, accounting for phylogenetic relatedness, on the conservation of 162 threatened mammal species in China. We did so at three levels: global (all scientific papers published on the species), regional (a subset of the global papers that included at least one author from a local organization) and regional conservation-related (a subset of the regional papers that focused only on ecology and conservation). In addition to protected-area coverage and certain biological traits, regional conservation-related research emerged as an important predictor of species recovery. The same was not the case for global research. We should particularly encourage future regional research effort that has direct relevance to specific conservation issues.

Biodiversity loss is accelerating [ 1 ]. Moreover, extant vertebrate species have declined in abundance by ∼ 25% since 1970 [ 2 ]. In spite of a diverse range of conservation interventions, including the establishment of protected areas and wildlife-protection legislation [ 3 ], many threatened species continue to decline [ 4 ]. Halting declines is a priority.

Scientific research may play a vital role in conserving threatened species in at least two important ways. First, research provides knowledge about species' biology, ecology and life history, identifies critical limiting resources and determines the relative importance of threats to species. This, in turn, guides appropriate conservation action. Second, scientific research focuses research attention and public awareness, and generates support for conservation from stakeholders and the wider public (e.g. the chimpanzee, Pan troglodytes ) [ 5 ]. However, research may be decoupled from practical conservation intervention, leading to competition for limited resources between scientists and conservation practitioners. For example, some species (e.g. the Yangtze River dolphin, Lipotes vexillifer ) have been ‘monitored to almost certain extinction' without effective conservation intervention [ 6 ]. A critical assessment of the efficacy of scientific research to the conservation of threatened species is required.

Here, we assess the relative importance of scientific research, as indexed by the number of publications to mammal-species conservation in China. We included terrestrial mammals evaluated as Critically Endangered (CR), Endangered (EN) or Vulnerable (VU) in either China's 2004 [ 7 ] or 2015 Species Red List [ 8 ]. These Red Lists were conducted by Chinese scientists following IUCN Guidelines (version 4.0) and using IUCN Red List Categories and Criteria (version 8.1). More information of these assessments can be found in the Supplementary file. We believe that these extensive and robust national assessments represented a real status change of the Chinese mammal species, and are unlikely to be caused by more information being available. We calculated the change in status score for each species by converting species' status to a numerical index, i.e. 0 (Least Concern), 1 (Near Threatened), 2 (Vulnerable), 3 (Endangered) and 4 (Critically Endangered), following previous studies [ 9 ]. We subtract the species' 2015 status score from their 2004 score, such that a positive score indicates a species has become less threatened. The full species list and status-change score are provided in Supplementary Table 1.

(a) Distribution of publications and funding (mean and SD) for species in different mammalian orders in China. EU, Eulipotyphla; CH, Chiroptera; RO, Rodentia; LA, Lagomorpha; PE, Perissodactyla; CE, Cetartiodactyla; PH, Pholidota; PRI, Primates; CA, Carnivora; PRO, Proboscidea. Each column with a different colour represents the number of publications or funding allocated to that order. Numbers indicate the number of species in each order included in this study. (b) Geographical distribution of status-change scores in China. A value of +1 means an improvement of one class, e.g. from Endangered to Vulnerable; scores sum changes across all species that occur in a region. (c) Final ‘best-fitted' models using global, regional or regional conservation-related publications to represent scientific research effort. Lengths of bars indicate the relative importance of variables in different cases, and directions indicate either positive or negative impact on the response variable. (d) Partial regression plots showing the relationship between species recovery and regional conservation-relevant scientific research, with 95% confidence intervals.

Based on previous research, we selected 10 predictor factors including three intrinsic factors (body mass, generation length and annual reproductive output), four ecological factors (species range size, temperature, precipitation and human-footprint index of species distribution area) and three conservation interventions (protected-area coverage, number of publications and research funding on each species) (Supplementary Table 2). We extracted the life-history information of species from the several high-quality databases (see Supplementary Methods) and digitized their distribution maps from China's mammal-diversity and geographical-distribution dataset [ 10 ]. We converted the polygon map of each species into a raster map on a 1-km 2 equal-area grid scale. For each species, we first computed its range size and then obtained the mean value of annual temperature, precipitation [ 11 ] and Human Footprint Index (HFP) [ 12 ] across its distribution area.

To derive an index of the amount of scientific research allocated to each species, we determined the number of publications for each species from literature databases for the entire duration of their records. It is possible that we did not include some relevant unpublished publications in our indices, as these reports may not be indexed in the databases. For each species, the total number of publications represented the global research effort, while the number of publications including at least one author from a Chinese institute in the list of author affiliations represented regional research effort. We assumed that having a regional author would make species-conservation action more likely. A more direct way would be to track the conservation influence of each paper but such information is not readily available. We filtered the regional publications for ‘Biodiversity & Conservation' and ‘Environmental Science & Ecology' to determine the number of regional conservation-related publications (see Supplementary Methods for details). We determined the amount of research funding assigned to each species from the National Natural Science Foundation of China ( http://www.nsfc.gov.cn/ ) (see Supplementary Methods for details).

Protected-area coverage for each species was obtained from the World Database of Protected Areas, supplemented with data from Wu et al. [ 13 ] and the Chinese Ministry of Environmental Protection. We expressed the conservation effort allocated to each species at the national scale by calculating the proportion of species' ranges included in national protected areas.

In the modelling process, we constructed the phylogenetic tree of all species of interest according to Tree of Life [ 14 ] (Supplementary Fig. 1) and used phylogenetic generalized linear models for our analyses (Supplementary Table 3). Model selection followed an information-theoretic approach using the corrected Akaike Information Criterion AICc [ 15 ]. We calculated the relative importance ( w +) of the variables in the candidate model set using Akaike weights ( w i ) [ 16 ]. To explore the relationship between scientific research and species recovery, we performed partial regression with the species status-change score against number of scientific publications, while controlling for the influence of all other variables in the final models (see Supplementary Methods for details).

In China, the funding and number of publications varied considerably across the 162 species (Fig. 1 a). The endangerment status of 76 species improved, 59 remained the same and 27 became worse in 2015 compared to 2004. Improvements in the species-conservation status were most obvious in south-west China, where regional mammal diversity is highest [ 10 ]. In contrast, the species-conservation status in north-east China worsened or did not change (Fig.  1 b).

The best-fit phylogenetic generalized linear models (PGLM) models testing the effect of regional publications included six or seven predictor variables (Supplementary Table 3 and Fig. 1 c). Excluding the giant panda, which was a major outlier, did not affect our main results (not shown). Consistently with previous studies, our study found that conservation interventions, including the establishment of protected areas [ 3 ] and funding allocation [ 17 ], were associated with reversing population declines of threatened species, though the effects may differ for different publication indices (Supplementary Table 4 and Fig. 1 c). Protected areas maintain relatively intact habitats, reduce human disturbance and suppress hunting [ 18 ]. In addition, species occupying larger geographic ranges and warmer environments had a greater likelihood of recovery. Large-bodied mammals with slow life histories became more threatened over time (Supplementary Table 4 and Fig. 1 c).

Our analyses suggest that regional scientific research including local authors, especially regional conservation-related research, was an important predictor of improved species status (Supplementary Table 4 and Fig. 1 c and d). Although this relationship is correlational, we believe that increased research effort may have caused improvements to the status of some species. It is unlikely that species recovery caused more research, since conservation scientists usually target species that are experiencing population decline and not those in recovery. Species with deteriorating status should cause more, not less, research, which would result in a negative correlation, and that is opposite to what we found.

Conservation research of threatened mammals in China has seen considerable growth in the last two decades [ 19 ], although the number of publications is still small (average of 4.2 regional conservation-related papers per species). When few data are available for threatened species, even a small number of conservation-related research projects can contribute to conservation in at least three ways. First, research can provide crucial knowledge of species biology, ecology, behaviour and threats, thus informing and promoting species conservation. Second, research can attract public attention. When we described and published a new species of gibbon (the skywalker hoolock gibbon, [ 20 ]), it attracted >400 media reports in Chinese and English. Google hits increased rapidly after the paper was published (Supplementary Fig. 2). Third, regional research can affect policy making. Chinese scientists were involved in the conservation planning of the Giant Panda National Park since the pre-planning stage. Scientific research of tigers and leopards in north-east China directly led to the Central Government of China establishing the 14 600-km 2 Northeast Tiger Leopard National Park in 2017 ( tiger.gov.cn ). Our results reject concerns that scientific research is irrelevant to, or potentially disconnected from, practical conservation. The exact mechanisms of how research contributes to conservation will require further investigation.

The number of global publications and species status change in China were not correlated (Fig. 1 c, global panel). While global studies may provide useful knowledge to support regional conservation activities for threatened species, our analyses suggest that regional research is more predictive and more useful in promoting population recovery. This is because species in different regions often face different and contextualized ecological and anthropogenic threats. In addition, regional scientists are more likely to become involved in local conservation activities. Our findings point to the important role local and regional conservation organizations have in threatened-species research and conservation actions.

In conclusion, our study provides correlational evidence that scientific research, especially directed regional conservation-related research, plays an important role in successful species conservation, although the exact mechanisms remain to be examined. In the future, promoting regional research that has direct relevance to specific conservation issues and species should be encouraged and funded.

We are grateful to Prof. Paul A. Garber for his valuable discussion and Mr Xiaojian Tang for his help with data analysis.

This work was supported by the National Natural Science Foundation of China (31770421, 31822049, 31870396), the Top Young Talent of the Ten Thousand Talents Programme (to F.P.F.) and Sun Yat-Sen University. C.C. would like to thank the Humboldt Foundation for providing the time to develop some of these ideas, the IDRC grant ‘Climate change and increasing human-wildlife conflict' and Kyoto University.

AUTHOR CONTRIBUTIONS

F.P.F. designed the research. H.Y.S., L.Z.H., L.T.M. and F.P.F. conducted the research. All authors contributed to writing the manuscript.

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Research Article

Too few, too late: U.S. Endangered Species Act undermined by inaction and inadequate funding

Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliation Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, New York, United States of America

Roles Conceptualization, Supervision, Writing – original draft, Writing – review & editing

Affiliations Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America, Princeton School of Public and International Affairs, Princeton University, Princeton, New Jersey, United States of America

Affiliations Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America, Santa Fe Institute, Santa Fe, New Mexico, United States of America

• Erich K. Eberhard, 
• David S. Wilcove, 
• Andrew P. Dobson

• Published: October 12, 2022
• https://doi.org/10.1371/journal.pone.0275322
• Reader Comments

This year, the Conference of Parties to the Convention on Biological Diversity will meet to finalize a post 2020-framework for biodiversity conservation, necessitating critical analysis of current barriers to conservation success. Here, we tackle one of the enduring puzzles about the U.S. Endangered Species Act, often considered a model for endangered species protection globally: Why have so few species been successfully recovered? For the period of 1992–2020, we analyzed trends in the population sizes of species of concern, trends in the time between when species are first petitioned for listing and when they actually receive protection, and trends in funding for the listing and recovery of imperiled species. We find that small population sizes at time of listing, coupled with delayed protection and insufficient funding, continue to undermine one of the world’s strongest laws for protecting biodiversity.

Citation: Eberhard EK, Wilcove DS, Dobson AP (2022) Too few, too late: U.S. Endangered Species Act undermined by inaction and inadequate funding. PLoS ONE 17(10): e0275322. https://doi.org/10.1371/journal.pone.0275322

Editor: Laurentiu Rozylowicz, University of Bucharest, ROMANIA

Received: June 10, 2022; Accepted: September 14, 2022; Published: October 12, 2022

Copyright: © 2022 Eberhard et al. 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.

Data Availability: All data are within the paper and Supporting Information files. The species data and appropriations data underlying the results presented in this study were collected from notices published by the U.S. Fish & Wildlife Service and annual budget legislation, all of which are publicly available through the Federal Registrar ( www.federalregistrar.gov ). The author's accessed FWS Notices through the Service's Environmental Conservation Online System (ECOS), which organizes documents by species name. This data base is also publicly accessible ( https://ecos.fws.gov/ecp/ ).

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Accelerating rates of species extinction are a matter of global concern [ 1 ] as exemplified in the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) report that predicted the loss of over 1 million species in the foreseeable future, which will also have significant impacts on the delivery of ecosystem services [ 2 ]. The prevention of species extinction is a primary goal of the Convention on Biological Diversity and the UN Sustainable Development Goals. In the United States, the strongest law to prevent species extinctions is the Endangered Species Act (ESA) [ 3 ], which has served as a model for other nations since its passage by the Nixon Administration in 1973. A longstanding concern of both supporters and opponents of the law has been the relatively low number of listed species that have successfully recovered to the point where they no longer need protection. In the 48 years since enactment of the ESA, only 54 US species have been declared fully recovered and delisted [ 4 ].

Multiple explanations have been given for this low rate of recovery including: (a) a pattern of not protecting species until their populations have reached very low levels, which increases both the time to recovery and the likelihood that species will vanish entirely due to environmental, genetic, and demographic stochasticity [ 5 ]; (b) a lack of incentives to landowners to participate actively in efforts to increase populations of endangered species [ 6 ]; and (c) inadequate funding for recovery actions [ 7 ]. Here, we have used data from the Federal Register to examine trends in the population sizes of species at time of listing and the levels of funding available to list and recover them.

Evidence that species are not being protected under the ESA until their populations have reached dangerously low levels was initially provided in a 1993 paper by Wilcove et al. [ 8 ]. The authors found that the median population size at time of listing during the second decade of ‘legal protection’ by the ESA (1985–1991) was just 1075 for vertebrates and 999 individuals for invertebrates. The median population size at listing for plant species was less than 120 individuals. We repeated their methodology to determine whether the US Fish & Wildlife Service (FWS) has become more proactive as we approach the 50 th anniversary of the ESA and roughly 30 years since attention was first drawn to this problem.

We also examined trends in the length of time between when a species is identified as potentially deserving of protection and when it actually receives that protection under the ESA (hereafter, “wait times”). It should be noted that, in recent years, most of the species added to the ESA have been the result of petitions from non-governmental entities to FWS requesting protection of a given species. Frequently, listing follows litigation brought by environmental organizations when petition decisions are overdue or petitions are denied [ 9 ].

Finally, we examined trends in funding for the listing and recovery of imperiled species (we use “imperiled” to include both Endangered and Threatened species protected under the ESA, and, unless indicated otherwise, we use the word “species” to refer to any entity protected under the ESA, including subspecies and vertebrate populations). We give particular attention to trends in funding per species , in order to account for changes in the number of species listed each year.

Materials and methods

The list of plants and animals granted protection under the ESA was collated from annual listing records available through the U.S. Fish & Wildlife Service’s Environmental Conservation Online System (ECOS). Population data were obtained from Final and Proposed Listing Notices issued by the U.S. Fish & Wildlife Service. Our analysis was restricted to wild populations of plants and animals known to occur in the United States and its territories and did not include captive populations.

When presented with a range of values, or an upper limit, for the total number of individuals or populations at time of listing, we favored interpretations that maximized population size. For example, if a population was said to be “between 500 and 1000” individuals, we recorded the population as being 1000 individuals at time of listing. Similarly, a population said to be “<1000” was recorded as being 999 individuals at time of listing. This was done in order to obtain the largest possible estimate of each plant and animal population at time of listing, making our subsequent analyses an optimistic “best case scenario”. Six species were listed with no known individuals or populations surviving in the wild. In these instances, the total number of individuals or total number of populations was recorded as being zero. Population data for plants and animals listed between 1985–1991 were obtained from Wilcove et al. in order to facilitate comparison with their results. We performed a non-parametric Wilcoxon Rank-sum Test to compare the medians of continuous variable x , the number of individuals at time of listing for species listed between 1985–1992, and continuous variable y , the number of individuals at time of listing for species listed between 1993–2020. The same approach was used to compare the median number of populations at time of listing for each time period. We adopted a significance threshold of p = 0.05.

Data for Resource Management Appropriations (discretionary funding that supports the management and recovery of imperiled species by FWS) and Section 4 Appropriations (funding allocated specifically to ESA listing activities) were obtained from the text of annual federal budget legislation and corrected for inflation to 2019 USD. These documents are publicly accessible through the Federal Registrar . Funding per species was defined as the average funding available for the management of each species in a given year. We calculated this value by dividing annual Resource Management Appropriations by the total number of species protected under the ESA as of the first day of that calendar year.

From 1992–2020, the FWS listed a total of 970 species for protection under the ESA; 68% of these listings were plants, 18% were invertebrates, and 14% were vertebrates. Full species accounted for the majority of listings during this period (80%). Of the species listed, 602 had data on their total population size (total number of individuals) at time of listing, and 843 had data on the number of populations at time of listing. For each taxonomic group analyzed, the total population size at time of listing ( Fig 1A ) did not differ significantly between the 1985–1991 and 1992–2020 time periods (Wilcox Test values of p = 0.08, p = 0.41, and p = 0.66, for plants, vertebrates and invertebrates respectively). For plants and invertebrates, the total number of populations at time of listing ( Fig 1B ) also did not differ significantly between the 1985–1991 and 1992–2020 time periods (p = 0.91 and p = 0.06, respectively). However, the median number of vertebrate populations at time of listing was slightly greater in the 1992–2020 time period, increasing from 2 to 4 populations (p = 0.04).

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(A) Comparison of population size at time of listing for plants and animals. There are no significant differences between the two periods (Wilcox Test values of p = 0.08, p = 0.41, and p = 0.66, for plants, vertebrates and invertebrates respectively). (B) Comparison of number of populations at time of listing. There are no significant differences between the two periods for plants and invertebrates. Values of zero indicate species for which there were either no known individuals or no known populations at time of listing. Median values shown above each plot.

https://doi.org/10.1371/journal.pone.0275322.g001

Our analysis revealed longer wait times for species petitioned for listing during the 2000–2009 period (median = 9.1 years), compared to those petitioned for listing during the 1992–1999 period (median = 5.9 years), followed by shorter wait times for species petitioned for listing during the 2010–2020 period (median 3.0 years). The number of petitions received during each period also varied greatly ( n = 49, 203 and 26 for 1992–1999, 2000–2009 and 2010–2020, respectively). While wait times seem to decrease when fewer species are listed, there are insufficient data to test whether this effect is significant.

Resource Management Appropriations climbed modestly from 1996–2010 before beginning a decade-long decline that was halted only in 2020 ( Fig 2A ). The same trend is observed in Section 4 Appropriations, which peaked in 2010 at $25.9 million USD before dropping to $20.1 million USD by 2020. Concurrently, the number of species listed for protection under the ESA increased by over 300% between 1985–2020. As such, Resource Management Appropriations, when measured on a per species basis, have dropped by nearly 50% since 1985.

(A) Change in cumulative number of ESA listings compared to change in Resource Management Appropriations. The lower timeline illustrates political control of the Presidency and, by a majority, each house of Congress. (B) Number of species delisted for various reasons.

https://doi.org/10.1371/journal.pone.0275322.g002

Our analysis of trends in the protection of imperiled species under the US Endangered Species Act warrants a limited amount of optimism and a larger amount of pessimism: Most species are not receiving protection until they have reached dangerously low population sizes. First reported in 1993, this pattern has persisted throughout the intervening quarter century. We suspect that most of the species listed since 1993 had fallen to low population levels well before the time span of our study, a reflection of past anthropogenic activities. Their protection under the ESA implies a painfully slow process of clearing a backlog of rare but unprotected species as opposed to a failure to respond to recent, rapid population declines in formerly more common species.

The wait-times between when a species is first petitioned for protection under the ESA and when it finally receives that protection have waxed and waned since 1992. The period with the longest median wait time (2000–2009, with a median wait-time of 9.1 years), was also the period when the greatest number of petitions were received by FWS ( n = 203). The period with the shortest median wait time (2010–2020 with a median wait-time of 3.0 years) was the period when the fewest number of petitions were received ( n = 26). This suggests that wait times may be exacerbated when limited resources for listing are strained by a large influx of petitions. Consistently, very few species have received protection in the two-year period that is prescribed in the ESA. For species with very small or rapidly declining populations, a multi-year delay in receiving protection increases the risk of extinction.

Our data suggest that inadequate funding has persisted for decades, with no clear relationship as to which political party is in power ( Fig 2A ). The unfortunate conclusion is that FWS is being asked to do more with less resources. The combination of delays in listing rare species, the typically mall population sizes of species at time of listing, and inadequate funding for recovery actions, are the key factors that can explain the relatively small number of listed species that have fully recovered ( Fig 2B ). Resource allocation frameworks and other decision-support tools can help FWS make the most efficient use of the funds it receives [ 10 ], but increased funding is essential for sustained, substantial progress in protecting imperiled species [ 11 , 12 ]. Studies have shown that government expenditures for imperiled species management do contribute to an improvement in recovery status and averted extinctions [ 13 ].

Although the US is one of only a handful of nations that have failed to ratify the Convention on Biological Diversity, its commitment to preventing the loss of its own “non-voting” species dates back nearly half a century to the passage of the ESA in 1973. In December 2022, when international leaders gather in Montréal, Canada for the 15 th meeting of the Conference of Parties to the Convention on Biological Diversity, the failure of the US to have solved the funding gaps that hamper the ESA will stand as a stark reminder of the difference between a visionary promise and its functional implementation.

Supporting information

https://doi.org/10.1371/journal.pone.0275322.s001

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• 2. Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, (IPBES). Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. IPBES Secretariat. 2019. Available from: https://ipbes.net/global-assessment
• 3. United States. The Endangered Species Act, Public Law 93–205, Section 3. Washington D.C. 1973.

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Extinction and the U.S. Endangered Species Act

Noah greenwald.

1 Center for Biological Diversity, Portland, OR, USA

Kieran F. Suckling

2 Center for Biological Diversity, Tucson, AZ, USA

Brett Hartl

3 Center for Biological Diversity, Washington, DC, USA

Loyal A. Mehrhoff

4 Center for Biological Diversity, Honolulu, HI, USA

Associated Data

The following information was supplied regarding data availability:

The raw data are available in a Supplementary File and include a complete list of the species we identified as extinct or possibly extinct along with all supporting information.

The U.S. Endangered Species Act is one of the strongest laws of any nation for preventing species extinction, but quantifying the Act’s effectiveness has proven difficult. To provide one measure of effectiveness, we identified listed species that have gone extinct and used previously developed methods to update an estimate of the number of species extinctions prevented by the Act. To date, only four species have been confirmed extinct with another 22 possibly extinct following protection. Another 71 listed species are extinct or possibly extinct, but were last seen before protections were enacted, meaning the Act’s protections never had the opportunity to save these species. In contrast, a total of 39 species have been fully recovered, including 23 in the last 10 years. We estimate the Endangered Species Act has prevented the extinction of roughly 291 species since passage in 1973, and has to date saved more than 99% of species under its protection.

Introduction

Passed in 1973, the U.S. Endangered Species Act (ESA) includes strong protections for listed threatened and endangered species and has helped stabilize and recover hundreds of listed species, such as the bald eagle and gray whale ( Taylor, Suckling & Rachlinski, 2005 ; Schwartz, 2008 ; Suckling et al., 2016 ). In part because of its strong protections, the ESA has engendered substantial opposition from industry lobby groups, who perceive the law as threatening their profits and have been effective in generating opposition to species protections among members of the U.S. Congress. One common refrain from opponents of the ESA in Congress and elsewhere is that the law is a failure because only 2% of listed species have been fully recovered and delisted ( Bishop, 2013 ).

The number of delistings, however, is a poor measure of the success of the ESA because most species have not been protected for sufficient time such that they would be expected to have recovered. Suckling et al. (2016) , for example, found that on average listed birds had been protected just 36 years, but their federal recovery plans estimated an average of 63 years for recovery. Short of recovery, a number of studies have found the ESA is effectively stabilizing or improving the status of species, using both biennial status assessments produced by the U.S. Fish and Wildlife Service for Congress and abundance trends ( Male & Bean, 2005 ; Taylor, Suckling & Rachlinski, 2005 ; Gibbs & Currie, 2012 ; Suckling et al., 2016 ).

In addition to recovering species, one of the primary purposes of the ESA is to prevent species extinction. Previous studies indicate the ESA has been successful in this regard ( McMillan & Wilcove, 1994 ; Scott et al., 2006 ). As of 2008, the ESA was estimated to have prevented the extinction of at least 227 species and the number of species delisted due to recovery outnumbered the number of species delisted for extinction by 14–7 ( Scott et al., 2006 ). In this study, we identified all ESA listed species that are extinct or possibly extinct to quantify the number of species for which ESA protections have failed and use these figures to update the estimated number of species extinctions prevented. This is the first study in over 20 years to compile data on extinction of ESA listed species, providing an important measure of one of the world’s strongest conservation laws ( McMillan & Wilcove, 1994 ).

To identify extinct or possibly extinct ESA listed species, we examined the status of all 1,747 (species, subspecies and distinct population segments) U.S. listed or formerly listed species, excluding species delisted based on a change in taxonomy or new information showing the original listing to have been erroneous. We determined species to be extinct or possibly extinct based on not being observed for at least 10 years, the occurrence of adequate surveys of their habitat, and presence of threats, such as destruction of habitat of the last known location or presence of invasive species known to eliminate the species.

To differentiate extinct and possibly extinct species we relied on determinations by the U.S. Fish and Wildlife Service, IUCN, species experts and other sources. In most cases, these determinations were qualitative rather quantitative. Species were considered extinct if surveys since the last observation were considered sufficient to conclude the species is highly likely to no longer exist, and possibly extinct if surveys were conducted after the last observation, but were not considered sufficient to conclude that extinction is highly likely ( Butchart, Stattersfield & Brooks, 2006 ; Scott et al., 2008 ).

Source information included 5-year reviews, listing rules and critical habitat designations by the U.S. Fish and Wildlife Service (for aquatic and terrestrial species) or NOAA Fisheries (for marine species), published and gray literature, personal communication with species experts and classifications and accounts by NatureServe, IUCN and the Hawaiian Plant Extinction Prevention program. For each species, we identified year of listing, year last seen, NatureServe and IUCN ranking, taxonomic group, and U.S. Fish and Wildlife Service region. For species last seen after listing, we also searched for abundance estimates at time of listing in order to give a sense of likelihood of survival regardless of ESA protection.

Following previously developed methods, we estimated the number of species extinctions prevented by the ESA by assuming that listed threatened and endangered species have a comparable extinction risk to IUCN endangered species, which was estimated as an average of 67% over 100 years ( Mace, 1995 ; Schwartz, 1999 ; Scott et al., 2006 ). We believe this estimate of extinction risk is conservative based on similarity of IUCN criteria to factors considered in ESA listings, observed low numbers for species at time of ESA listing and observed correspondence between ESA listed species and species classified as endangered or critically endangered by the IUCN ( Wilcove, McMillan & Winston, 1993 ; Wilcove & Master, 2005 ; Harris et al., 2012 ). Presumed extinction risk was then multiplied by the number of extant listed species and the proportion of a century in which species were protected by the ESA. Previous studies used the length of time the ESA has been in existence (1973-present) for the proportion of a century species have been protected ( Schwartz, 1999 ; Scott et al., 2006 ), but because many species have not been protected the entire 45 years the law has existed, we instead used the more conservative average length species were protected (25 years). This corresponds to the following formula:

We identified a total of 97 ESA listed species that are extinct (23) or possibly extinct (74). Of these, we found 71 extinct (19) or possibly extinct (52) species were last observed before they were listed under the ESA and thus are not relevant to determining the Act’s success in preventing extinction ( Table S1 ). These species were last seen an average of 24 years before protection was granted with a range of one to more than 80 years prior.

A total of 26 species were last seen after listing, of which four are confirmed extinct and 22 are possibly extinct ( Table S2 ). On average, these species were last seen 13 years after listing with a range of 2–23 years. We were able to find an abundance estimate at the time of listing for 19 of these species, ranging from one individual to more than 2,000 with an average of 272. In several cases, these estimates were based on extrapolations from very few sightings.

The distribution of extinct and possibly extinct species was non-random with 64 of the 97 species from Hawaii and other Pacific Islands, followed by 18 from the southeast ( Fig. 1 ). This was also the case for taxonomy. A total of 40 of the 97 species were mollusks dominated by Hawaiian tree snails and southeast mussels, followed by birds (18) and plants (17) ( Fig. 2 ).

Extinct or possibly extinct listed species by taxonomic group.

Extinct or possibly extinct listed species by U.S. Fish and Wildlife Service Region.

We identified several other species that have been missing for more than 10 years, but for which there has not been any effective surveys and thus classifying them as possibly extinct did not seem appropriate, including two Hawaiian yellow-faced bees ( Hylaeus facilis and Hylaeus hilaris ) (K. Magnacca, 2018, personal communication) and Fosberg’s love grass ( Eragrostis fosbergii ) ( U.S. Fish and Wildlife Service, 2011 ). If indeed extinct, all three were lost prior to protection under the ESA.

Including updated figures for number of listed species, time of protection and species extinctions, we estimate the ESA has prevented the extinction of roughly 291 species in its 45 year history. Based on the number of confirmed extinctions following listing, we further estimate that the ESA has to date prevented the extinction of more than 99% of species under its protection. To date, a total of 39 species have been delisted for recovery compared to four species that are extinct and 22 that are potentially extinct.

The few number of listed species that have gone extinct following protection combined with an estimated 291 species for which extinction was prevented demonstrate the ESA has achieved one of its core purposes—halting the loss of species. We will not attempt to catalog them here, but numerous individual examples provide further support for this conclusion. Well known species like the California condor ( Gymnogyps californianus ), black-footed ferret ( Mustela nigripes ) and Hawaiian monk seal ( Neomonachus schauinslandi ), as well as lesser known species like the yellowfin madtom ( Noturus flavipinnis ), are but a few of the species that likely would have been lost were it not for the ESA.

The madtom is a case in point. Wrongly presumed extinct when described in 1969, individual madtom were found in the Powell River in Tennessee and Copper Creek in Virginia and the species was protected under the ESA in 1977 ( U.S. Fish and Wildlife Service, 1977 ). Following protection, federal and state officials worked with a non-governmental organization, Conservation Fisheries Inc., to discover additional populations and repatriate the species to rivers and streams in its historic range and there are now populations of the yellowfin madtom in three different watersheds ( U.S. Fish and Wildlife Service, 2012a ). The history of the ESA is replete with similar such stories.

The distribution of extinct or possibly extinct listed species largely tracks those regions with the highest rates of species endangerment, including Hawaii and the Northern Mariana Islands with 64 of the 97 extinctions or possible extinctions, and the Southeast with 18 of the extinctions or possible extinctions, mostly freshwater species. The fragility of Hawaii’s endemic fauna to introduced species and habitat destruction and high degree of species imperilment is well recognized ( Duffy & Kraus, 2006 ). Similarly, the extinction and endangerment of freshwater fauna in the southeast is well documented ( Benz & Collins, 1997 ). To avoid further extinctions, these areas should be priorities for increased funding and effort.

Protection under the ESA came too late for the 71 species last seen prior to listing. It’s possible that some of these species survived undetected following listing, but we find this unlikely for most if not all of the species. It is very difficult to document extinction, but all of the species were the subject of survey both before and after listing, which is described in the listing rules and subsequent status surveys. In addition, the 71 species were last seen an average of 24 years prior to listing, providing a long window for detection prior to listing. If some of these species did survive after listing it was likely at very low numbers, such that recovery would have been difficult at best.

That these 71 species were lost before protections were applied clearly highlights the need to move quickly to protect species. Indeed, Suckling, Slack & Nowicki (2004) identified 42 species that went extinct while under consideration for protection. Since that analysis was completed, the U.S. Fish and Wildlife Service has determined five additional species did not qualify for protection because they were extinct, including the Tacoma pocket gopher ( Thomomys mazama tacomensis ), Tatum Cave beetle ( Pseudanophthalmus parvus ), Stephan’s riffle beetle ( Heterelmis stephani), beaverpond marstonia ( Marstonia castor ) and Ozark pyrg ( Marstonia ozarkensis ), meaning there are now 47 species that have gone extinct waiting for protection ( U.S. Fish and Wildlife Service, 2012b , 2016 , 2017 , 2018a ).

The U.S. Fish and Wildlife Service currently faces a backlog of more than 500 species that have been determined to potentially warrant protection, but which await a decision ( U.S. Fish and Wildlife Service, 2018b ). Under the ESA, decisions about protection for species are supposed to take 2 years, but on average it has taken the Fish and Wildlife Service 12 years ( Puckett, Kesler & Greenwald, 2016 ). Such lengthy wait times are certain to result in loss of further species and run counter to the purpose of the statute. This problem can be addressed by streamlining the Service’s process for listing species, which has become increasingly cumbersome, and by increasing funding for the listing program. For every species listed, the Service’s process includes review by upward of 20 people, including numerous individuals who have no specific knowledge of the species and in a number of cases are political appointees. We instead recommend that the Service adopt a process similar to scientific peer review, involving review by two to three qualified individuals.

The loss of 26 species after they were protected is indicative of conservation failure. This failure, however, in most cases cannot be wholly attributed to the ESA because most of these species were reduced to very low numbers by the time they were protected, making recovery difficult to impossible. Of the 19 species we could find an abundance estimate for at the time of listing, 13 had an estimated population fewer than 100 with eight having fewer than 10 individuals. Of the six other species, two Hawaiian birds, Oahu creeper ( Paroreomyza maculate ) and ‘O’u ( Psittirostra psittacea ) had estimated populations in the hundreds, but this was based on sightings of single individuals. Given the lack of further sightings and the presence of disease carrying mosquitoes throughout their habitat, these estimates were likely optimistic. The other four species, the dusky seaside sparrow ( Ammodramus maritimus nigrescens ), Morro Bay kangaroo rat ( Dipodomys heermanni morroensis ), pamakani ( Tetramolopium capillare ) and Curtis’ pearlymussel ( Epioblasma florentina curtisii ), had populations at the time of listing ranging from 100 to 3,000 individuals, but sufficient action was not taken to save them, making them true conservation failures.

At some level, all of the 97 ESA listed species that we identified as possibly extinct or extinct are conservation failures. For 42 of these species, the law itself was too late because they were last seen before the ESA was passed in 1973. But for others, there may have been time and we did not act quickly enough or dedicate sufficient resources to saving them. There are many examples of species both in the U.S. and internationally that have been successfully recovered even after dropping to very small numbers, but this can only occur with fast, effective action, resources and in many cases luck. The Mauritius kestrel ( Falco punctatus) , for example, was brought back from just two pairs ( Cade & Jones, 1993 ) and the Hawaiian plant extinction prevention program, which focuses on saving plants with fewer than 50 individuals, has rediscovered many species believed extinct, brought 177 species into cultivation, constructed fences to protect species from non-native predators and reintroduced many species into the wild ( Wood, 2012 , http://www.pepphi.org/ ).

The failure to provide sufficient resources for conservation of listed species, however, continues to the present. As many as 27 species of Oahu tree snail ( achatinella spp. ) are extinct or possibly extinct, yet expenditures for the species that still survive are inadequate to support minimal survey and captive propagation efforts. Likewise, the Hawaiian plant extinction prevention program, which has been so effective in saving species on the brink of extinction, is facing a budget cut of roughly 70% in 2019 ( http://www.pepphi.org/ ), which very likely could mean the extinction of dozens of plants that otherwise could be saved. Overall, Greenwald et al. (2016) estimate current recovery funding is roughly 3% of estimated recovery costs from federal recovery plans. We can save species from extinction, but it must be more of a priority for federal spending. Nevertheless, despite funding shortfalls and the tragedy of these species having gone extinct, the ESA has succeeded in preventing the extinction of the vast majority of listed species and in this regard is a success.

Management implications

Of the 97 species we identified as extinct or potentially extinct, only 11 have been delisted for extinction. Another 11 have been recommended for delisting due to extinction. The San Marcos gambusia ( Gambusia georgei ) could also be delisted since there is very little hope it survives. For the other 74 possibly extinct species, we recommend retaining protections in the hope that some will be rediscovered and because there is little cost in retaining listing.

Supplemental Information

Supplemental information 1.

Extinct or possibly extinct species broken out by whether last seen before or after protection was enacted, including relevant source data and literature cited.

Funding Statement

The authors received no funding for this work.

Additional Information and Declarations

All authors are employed by the Center for Biological Diversity which works to protect endangered species and their habitats.

Noah Greenwald conceived and designed the experiments, performed the experiments, analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the paper, approved the final draft.

Kieran F. Suckling conceived and designed the experiments, performed the experiments, analyzed the data, authored or reviewed drafts of the paper, approved the final draft.

Brett Hartl conceived and designed the experiments, performed the experiments, analyzed the data, authored or reviewed drafts of the paper, approved the final draft.

Loyal A. Mehrhoff conceived and designed the experiments, performed the experiments, analyzed the data, authored or reviewed drafts of the paper, approved the final draft.

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• Published: 28 June 2018

Evaluating the Contribution of North American Zoos and Aquariums to Endangered Species Recovery

• Judy P. Che-Castaldo   ORCID: orcid.org/0000-0002-9118-9202 1 ,
• Shelly A. Grow 2 &
• Lisa J. Faust 1  

Scientific Reports volume  8 , Article number:  9789 ( 2018 ) Cite this article

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• Biodiversity
• Conservation biology

The challenge of recovering threatened species necessitates collaboration among diverse conservation partners. Zoos and aquariums have long partnered with other conservation organizations and government agencies to help recover species through a range of in situ and ex situ conservation projects. These efforts tend to be conducted by individual facilities and for individual species, and thus the scope and magnitude of these actions at the national level are not well understood. Here we evaluate the means and extent to which North American zoos and aquariums contribute to the recovery of species listed under the U.S. Endangered Species Act (ESA), by synthesizing data from federal recovery plans for listed species and from annual surveys conducted by the Association of Zoos and Aquariums. We found that in addition to managing ex situ assurance populations, zoos frequently conduct conservation research and field-based population monitoring and assessments. Cooperatively managed populations in zoos tend to focus on species that are not listed on the ESA or on foreign listings, and thus it may be beneficial for zoos to manage more native threatened species. Our results highlight the existing contributions, but also identify additional opportunities for the zoo community to help recover threatened species.

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Introduction.

Due to the magnitude and complexity of the global extinction crisis, successful species conservation will require the engagement of all potential partners: state and federal agencies, non-governmental organizations, local communities and resource users, industry stakeholders, and wildlife managers 1 . These diverse partners each bring unique perspectives, expertise, and resources, not all of which will be appropriate or necessary in every case. However, a clear understanding of the potential contributions of each partner will help to identify the most relevant entities to call upon in each case.

Zoos and aquariums (hereafter, “zoos”) are becoming more broadly recognized as important partners for conserving threatened species 2 , 3 . There is a long history of zoos engaging in species recovery, from the American bison and California condor to the black-footed ferret and Panamanian golden frog 4 . However, the role of zoos in species conservation has often focused on ex situ species management, in particular ex situ breeding 5 , 6 . For example, the Conservation Measures Partnership’s Actions Classification 7 identifies 30 distinct types of conservation actions, but specifies a role for zoos in only two of those ( ex situ conservation, outreach and communications). The conservation value of ex situ breeding has also been somewhat controversial, with views ranging from it being a last resort that diverts resources from in situ efforts 8 , to part of a continuum of management actions for threatened species 9 . Even when ex situ breeding is acknowledged as part of the conservation strategy, the ability of zoos to sustain demographically and genetically viable populations for the long-term has been questioned 10 , 11 . Undoubtedly these issues and concerns must continue to be explored, but zoos also contribute to other conservation efforts beyond ex situ breeding 12 , 13 , 14 .

Several publications have explored generally how zoos contribute to species conservation, discussing both in situ and ex situ actions. Ex situ actions can directly target the species ( e . g ., ex situ population management, rehabilitation, gene banking) 7 , or indirectly support conservation through public outreach, biological and veterinary research, and fundraising for other organizations and projects 3 , 14 , 15 . In situ actions can include engaging and educating communities in the species’ native range, protecting and restoring habitat, supplying animals and/or staff for reintroductions, and field-based monitoring 3 , 15 . Although there are many case studies of these individual actions, the extent to which zoos contribute to conservation through these actions is not well understood. One study has evaluated the impacts of a subset of in situ conservation projects branded by the World Association of Zoos and Aquariums 16 , and another summarized the number of breeding and reintroduction projects for threatened species conducted by four Canadian zoos 12 . Thus far, no study has quantified both the in situ and ex situ conservation actions conducted by zoos at a national scale.

In the U.S., all institutions accredited by the Association of Zoos and Aquariums (AZA) include species conservation as a key part of their missions, in accordance with accreditation standards. To fulfill this part of their missions, zoos carry out an array of in situ and ex situ initiatives 4 , and collaborate with other conservation organizations and government agencies. This includes the agencies [U.S. Fish and Wildlife Service (USFWS) and National Oceanic and Atmospheric Administration (NOAA) Fisheries] that implement the U.S. Endangered Species Act (ESA), which was enacted in 1973 to protect threatened species through both extinction prevention and recovery actions 17 . However, the extent and scope of these zoo conservation efforts have not been systematically evaluated beyond annual reports within the zoo community.

The goal of this study was to evaluate the contribution of zoos to the recovery of threatened species in the U.S. by quantifying and summarizing their conservation activities. Our analysis consisted of three parts: (1) Summarize the management actions for which zoos are the responsible parties, based on data from federal recovery plans for listed species; (2) Summarize the recent conservation activities reported by AZA-accredited facilities in responses to the association’s annual field conservation and research surveys; and (3) Quantify the number of listed species that currently have managed populations in AZA facilities in order to identify additional opportunities for species conservation. Using multiple datasets allowed us to compare the contributions as self-reported by AZA facilities against those as recognized by the agencies responsible for implementing the ESA. Due to the scope of our study, we did not aim to quantify the impacts of these conservation activities, although it would be a valuable assessment that could be implemented following the methods of Mace et al . 18 .

In this study we focused on the terrestrial (including invertebrate and amphibian) and avian species listed under the ESA as of February 2017. Therefore, the large number of zoo conservation projects on marine and aquatic species, and the small number on plant species, were outside the scope of this assessment. Zoo conservation projects involving species with other risk statuses ( e . g ., Candidate, Under Review, or Proposed status under the ESA; state-listed; those ranked as Threatened (VU, EN, CR) or Extinct in the Wild (EW) under the IUCN Red List but not listed under the ESA) were also not represented in this assessment. Additionally, we focused on listed species whose native range included the U.S. ( i . e ., U.S. or U.S./foreign listings under the ESA; “U.S. listings” hereafter) in the first two parts of our analysis, but explored the overlap between both U.S. and foreign listings with managed zoo programs in the last section.

Roles of Zoos and Aquariums in Recovery Plans

The ESA requires every listed species to have a recovery plan, which documents the management actions and the criteria that determine when the species can be delisted. We gathered recovery plan data from the USFWS Recovery Plan Ad Hoc Report database ( http://ecos.fws.gov/ecp0/ore-input/ad-hoc-recovery-actions-public-report-input ), by querying all recovery actions that list a zoo, aquarium, or AZA (“zoos”) as the responsible party. As of September 2016, the recovery plans for 73 listed species (15.1% of the 482 listings that have recovery plans) named zoos as responsible for at least one recovery action. Of these, we focused on the 54 terrestrial and avian animals (6 amphibians, 31 birds, 7 invertebrates, and 10 mammals) for this analysis. Forty-two of these species are currently listed as Endangered and eight as Threatened, one is not listed due to extinction but was a species of concern at the time of recovery planning ( Moho bishopi ), and three have been delisted since the plan was written due to recovery ( Urocyon littoralis subspecies littoralis , santacruzae , and santarosae ).

In total, there were 38 recovery plans (some plans included more than one species) that described 468 recovery actions for which zoos were the responsible party. These actions involved 39 individual zoos or aquariums, or else listed AZA as the responsible party (see Table  S1 for complete list of institutions). We determined 11 keywords to represent the major types of conservation activities attributed to zoos (Table  1 ), which were derived through an iterative process. We started with 52 keywords used by AZA to categorize zoo conservation and science projects (see next section), and condensed them into 9 categories ( e . g ., anti-poaching/patrolling, disaster/emergency response, human-wildlife conflict, and wildlife trade were grouped into “threat mitigation”). We assigned these broader keywords to each recovery action based on the action descriptions from the plans, and added two keywords (fundraising, management/planning) to describe recovery actions that did not fit into existing keywords. In some cases multiple keywords were assigned to an action, resulting in a total of 605 keywords assigned.

The majority of recovery actions related to managing and/or maintaining an assurance population (36.1% of keywords), research (27.4%), and population augmentation (23.5%; Fig.  1A ). Research included a broad range of topics relevant to species recovery, from investigating the impacts of contaminants, to modeling disease dynamics, to evaluating methods for habitat restoration. Besides population augmentation, other in situ recovery actions primarily consisted of population monitoring and assessments (12.4%), but there were also a small number of projects related to mitigating threats (1.7%) and to protecting and restoring habitat (0.9%). An unexpected type of zoo recovery action was management and planning (8.3%), which included projects that either involved or supported decision-making by the recovery team, such as coordinating program components, prioritizing tasks, or evaluating existing strategies. These tasks help to improve efficiency and flexibility and therefore can contribute greatly to the success of a conservation program. Other previously recognized contributions from zoos such as education and outreach 7 , 19 and husbandry knowledge and veterinary care 13 were also represented in recovery plans (7.5% and 7.1%, respectively). Finally, zoos contributed to conservation by providing project funds (4.5%), which were raised not only through visitor fees 8 but also by securing state, federal, and private grants. The keyword related to providing rescue, rehabilitation, or sanctuary facilities did not apply to any zoo-based recovery actions described in these plans. However, they may be more likely to be included in plans for ESA-listed marine species ( e . g ., sea turtles).

Conservation activities carried out by North American zoos and aquariums for species listed under the Endangered Species Act, sorted by type using 11 keywords. The number of instances of each keyword is shown at the base of the bars. ( A ) Distribution of the 468 recovery actions for which zoos and aquariums are the responsible party as described in recovery plans; a total of 606 keywords were assigned. ( B ) Distribution of the 644 field conservation and research project submissions by zoos to the 2013–2015 Annual Report on Conservation and Science (ARCS) survey; a total of 786 keywords were assigned.

Recovery actions were distributed unevenly across taxa (Fig.  2A ), with the majority of actions pertaining to birds (357 out of 468 actions). This was because the Revised Hawaiian Forest Birds Recovery Plan 20 included a very similar set of up to 19 recovery actions for each of 19 different bird species (for a total of 289 recovery actions) that involved either the San Diego Zoological Society or the Honolulu Zoo. To compare recovery action types among taxonomic groups, we further clustered the 11 project keywords into three broader categories: ex situ , in situ , and knowledge/capacity. Ex situ included the projects related to animal care and management at zoos (i.e., assurance population, husbandry/veterinary care, rescue/rehabilitation/sanctuary), whereas in situ included projects that took place at the species’ native range (i.e., population augmentation, monitoring/assessments, threat mitigation, and habitat creation/restoration/protection). The remaining project types all focused on increasing biological knowledge or the capacity for conservation (i.e. research, education/outreach, management/planning, fundraising). For birds, all three categories of projects were similarly common, with a slightly lower proportion of in situ projects (Fig.  2A ). In contrast, in situ projects were the most common category for invertebrates. Knowledge and capacity-building projects (primarily research) were the most common type of zoo recovery action for mammals and amphibians, accounting for 56% and 40% of their action keywords, respectively.

Conservation activities carried out by North American zoos and aquariums for species listed under the Endangered Species Act, by taxonomic group. Activities were aggregated into three categories based on the activity type keywords: conservation knowledge or capacity (research, education/outreach, management/planning, fundraising), ex situ (assurance population, husbandry/veterinary care, rescue/rehab/sanctuary), and in situ (population augmentation, monitoring/assessments, threat mitigation, and habitat creation/restoration/protection). The total instances of keywords for each taxonomic group are shown in parentheses. ( A ) Distribution of the 468 recovery actions for which zoos and aquariums are the responsible party from recovery plans; a total of 606 keywords were assigned. ( B ) Distribution of the 644 field conservation and research project submissions by zoos to the 2013–2015 Annual Report on Conservation and Science (ARCS) survey; a total of 786 keywords were assigned.

In addition to working with federal agencies in recovery programs, zoos also collaborate with other partners, including academic institutions, research institutions, or universities (collectively “academic institutions”) and other non-governmental organizations (NGOs). Thus we also examined the involvement of these two types of partners in the recovery actions that specified zoos as a responsible party. All four recovery actions related to habitat creation/restoration/protection listed either academic institutions (2 actions) or other NGOs (2 actions) as additional responsible parties, suggesting such field projects may require larger collaborations to implement. Academic institutions were involved in nearly half of the actions with research as a keyword (54 out of 128 actions), but did not collaborate with zoos as much on other types of recovery actions (<13% for all other types). Other NGOs partnered with zoos most frequently on actions related to assurance populations (26 out of 169 actions) and research (26 out of 128 actions), but proportionally they collaborated primarily on actions related to education and outreach (14 out of 35 actions) and threat mitigation (2 out of 8 actions).

Although recovery plans provide an official documentation of the extent to which zoos participate in recovery programs when the plans were created, they do not provide the full picture. Nearly one-third of all U.S. listed animals do not have a recovery plan (482 out of 710 listed animal species had plans as of September 2016), and finalized plans are rarely updated and therefore tend to exclude more recent or current projects. Additionally, a zoo’s involvement may not have been explicitly described as a recovery action, or only the primary holding facilities may have been identified when multiple institutions are involved.

Conservation Activities Reported by Zoos and Aquariums

We next summarized zoo conservation activities based on the AZA’s field conservation and research surveys from 2013–2015. These surveys are used to produce the association’s Annual Report on Conservation and Science (ARCS; http://www.aza.org/annual-report-on-conservation-and-science ). In the field conservation survey, AZA member institutions report only their conservation efforts that have direct impacts on animals and habitats in the wild. In the research survey, they report on any hypothesis-driven research conducted at these institutions or by their staff and the resulting publications. Response rates differed between surveys and years, with 86–92% of institutions responding for the field conservation survey and 52–64% responding for the research survey between 2013–2015. Although this dataset likely underrepresents the conservation and research projects in zoos for listed species, it still provides the most comprehensive current summary of these activities across AZA. Because of the specific focus of these surveys, the responses would also exclude education programs that do not directly target the local communities in the species’ native range. Therefore our analysis leaves out many of the conservation-oriented education projects carried out by zoos, which can also have significant impacts on achieving biodiversity conservation 21 .

We queried the database of field conservation and research survey responses for references to ESA-listed species in the project titles, descriptions, or the selected focal species. We tallied the number of conservation project submissions, representing unique combinations of institutions, projects, and species. That is, the same project may involve multiple institutions, and we count these as unique projects for each institution. This is because each institution may submit the project under a different name or description, thereby making it difficult to consistently delineate unique projects. Between 2013–2015, 142 AZA institutions reported a total of 644 active conservation projects involving 74 ESA-listed, U.S. terrestrial and avian species (23 mammals, 21 birds, 12 amphibians, 11 reptiles, and 7 invertebrates). Of these, 50 are currently listed as Endangered and 24 as Threatened. Although 54 of the 74 listings have finalized recovery plans, only 18 of those plans mentioned zoos as responsible parties for recovery actions.

Similar to the actions from recovery plans, we assigned each zoo project from the survey data to one or more of the 11 keywords representing different types of conservation activities (Table  1 ). Of the 786 keywords assigned, most were related to research (25.2%), monitoring/assessments (17.6%), population augmentation (16.0%), and managing assurance populations (12.7%; Fig.  1B ). Fundraising directed to recovery programs or conservation organizations (for purposes unspecified in the survey response) accounted for 11.3% of the keywords. Projects related to education and outreach (targeting local communities in the species’ native range) accounted for 5.2% of the keywords, and all other keywords were used fewer than 3% of the time. Compared to the conservation actions described in recovery plans, zoos reported a smaller proportion of activities related to assurance populations, but a larger proportion related to monitoring and assessments, and to habitat creation/restoration/protection. This suggests that zoos are contributing more to in situ conservation projects than is recognized in recovery plans. Zoos also reported more fundraising projects than represented in recovery plans, and additionally reported several projects related to providing rescue, rehabilitation, or sanctuary facilities. Both data sources agreed that research made up a large proportion of the conservation activities in zoos, and that there was great variation in the types of research conducted. Research projects reported by zoos ranged from understanding the genetic structure of Hawaiian petrel ( Pterodroma sandwichensis ) populations, to measuring stress levels of Guam kingfishers ( Todiramphus cinnamominus ) in human care, to developing gene banking methods for black-footed ferrets ( Mustela nigripes ).

Comparing among taxonomic groups, the majority of zoo conservation projects involved listed mammal species (318 of 644 projects), and only 25 projects involved invertebrates. Although the distribution of projects among taxa is similar to a previous assessment of in situ conservation efforts by zoos around the world 16 , none of the mammalian species in our dataset were primates due to our focus on U.S. species. Based on the keyword categories we assigned to each project, we found in situ projects were most common for listed amphibians and invertebrates (Fig.  2B ), and they primarily consisted of population augmentation projects. Knowledge and capacity projects were least common for amphibians and invertebrates, but they made up the largest proportion of projects for mammals, birds, and reptiles (consisting primarily of research projects). Ex situ projects made up less than 20% of all conservation projects reported by zoos for listed mammals, birds, and reptiles. Compared to the actions from recovery plans, a larger proportion of in situ projects were reported by zoos for all taxonomic groups, and a smaller proportion of ex situ projects were reported for all taxa except amphibians (Fig.  2 ).

We estimated the amount that AZA zoos spend on listed species by summing the project expenditures reported in the ARCS surveys. From 2013–2015, total spending on the reported field conservation and research projects specifically targeting the 74 ESA-listed species summed to $28.9 million, or on average $9.6 million per year. For context, the reported average spending per year on the same set of species in 2013–2015 was $146.4 million by all federal agencies, and $7.9 million by all state agencies 22 , 23 , 24 . Among the different types of conservation activities, the majority of funds were spent on assurance populations, followed by population monitoring and assessment and research (Fig.  3A ). Comparing across taxa, expenditures were greatest on conservation projects for bird and mammal species (Fig.  3B ).

Spending by North American zoos and aquariums on conservation projects for species listed under the Endangered Species Act, as reported in the 2013–2015 Annual Report on Conservation and Science (ARCS) survey. The proportional spending (out of the total $28.9 M spent across 3 years) is shown by ( A ) project keyword and ( B ) taxonomic group.

Listed Species with Managed Populations in Zoos and Aquariums

The recovery plans and AZA surveys provide an overview of the extent to which zoos currently contribute to recovering listed species. However, additional opportunities for conservation may exist, as a number of ESA-listed species have ex situ populations in zoos that are cooperatively managed. Since the 1980s, zoos have collaborated in managing the animals in their care through goal setting, cooperative breeding, and exchanging animals across institutions, with the aim of improving the health (e.g., demographic viability, genetic diversity) of those zoo animal populations 25 , 26 . In North America, cooperatively managed populations are those with a Species Survival Plan ® (SSP) program, which is implemented by AZA member institutions. SSPs may also coordinate the conservation, research, and educational initiatives among institutions to support in situ species recovery. These programs therefore represent opportunities for zoos to contribute further to conservation efforts, because they have an established management structure and working partnerships across institutions. Cooperative management also generates a great deal of species-specific knowledge on breeding, veterinary care, behavior, and demography, which can inform or facilitate conservation actions. For example, knowledge on how to breed animals successfully and to care for and rear offspring may be important for helping to improve reproduction of a threatened species. Further, the establishment of an SSP program demonstrates a long-term commitment to the species by multiple AZA institutions, which may be leveraged to promote engagement in and support for wild populations of the same species.

Overall, 143 of the 482 SSP programs (29.7%) were for ESA-listed species, representing 154 listings (which included separate listings for Distinct Population Segments or subspecies of the same species). The majority of these were for species listed as Endangered (83.4%) and as foreign (77.9%). Of the 387 listings for U.S. terrestrial and avian species, 36 (9.3%) currently have zoo populations managed by an SSP program. Interestingly, only 14 of the 54 species whose recovery plans specified roles for zoos had SSP populations, and 24 of the 74 species identified in the AZA surveys had SSP populations. Only 10 species overlapped across the three datasets, meaning they have recovery plans that specified a role for zoos, conservation projects reported by zoos in AZA surveys, and zoo populations managed by an SSP program. This finding suggests that an SSP program is not required for zoos to participate in recovery programs, and many zoos work with listed species outside of the SSP framework. On the other hand, there are additional SSP programs that could participate in that species’ recovery but currently do not.

Most of the SSP programs for listed species involved mammals, with existing programs for 21 of the 74 (28.4%) U.S. mammal listings (Fig.  4A ). All other listed taxa were much less represented, especially invertebrates, for which the American burying beetle was the only listing (out of 148) with an SSP program. The picture was similar when including both U.S. and foreign listings, with 84 additional SSP programs for foreign-listed mammals, and a smaller number of additional SSP programs for foreign-listed birds and reptiles (14 and 13, respectively; Fig.  4B ). In summary, the majority of SSP programs did not manage listed species, but those that did tended to focus on species that were more at risk (listed as Endangered rather than Threatened). There was also a taxonomic bias for SSP programs to focus on mammals and a geographic bias for non-U.S. species, many of which were native to African and Central American countries. Our results parallel findings from a previous study that zoo and aquarium collections favor larger vertebrate species 5 . However, the bias of SSP programs toward non-U.S. species contrasts with an earlier finding that zoos tended to focus on mammal and bird species that are native to economically developed countries 27 .

The proportion of terrestrial and avian animal species listed under the Endangered Species Act that have cooperatively managed populations in AZA-accredited zoos and aquariums, by taxonomic group and listing status (T = Threatened, E = Endangered). ( A ) The proportion of U.S. listings with managed programs for the listed species. ( B ) The proportion of U.S. and foreign listings with managed programs for the listed species. ( C ) The proportion of U.S. listings with managed programs for a congener of the listed species. ( D ) The proportion of U.S. and foreign listings with managed programs for a congener of the listed species.

Zoos have the potential to contribute even further to species recovery, as shown by the number of listed species that have a congener with a managed SSP population in zoos (Fig.  4C,D ). Management of a closely related species in the same genus produces valuable husbandry and biological information that may be useful for informing the conservation of the listed species. Institutions holding the congeners may also develop education programs or design exhibits to promote conservation actions for the closely related listed species. Additionally, since zoos already have the resources and facilities to house a closely related species, it may be possible for those institutions to house the more threatened species instead, if ex situ breeding or rehabilitation is deemed beneficial (of course, species-specific behaviors and requirements will determine the extent to which that would be feasible, while threats and recovery strategies will determine the appropriateness of an ex situ breeding program). Across all taxa, there were SSP programs for the congeners of 70 out of 387 (18.1%) U.S. listings, and 299 out of 969 (30.9%) U.S. and foreign listings of terrestrial and avian species. In particular, there were managed programs for the congeners of 36.5% and 41.4% of U.S. listings for mammals and reptiles, respectively (Fig.  4C ), and 51.5% and 53.2% of total (U.S. and foreign) listings for mammals and reptiles, respectively (Fig.  4D ). This represents a significant body of knowledge and resources that could greatly enhance species recovery efforts, but have yet to be broadly utilized.

Our evaluation showed that zoos contribute to a diverse array of in situ and ex situ conservation efforts, and serve as important partners in the recovery of threatened species in the U.S. Zoo conservation activities (Table  1 ) spanned many of the conservation actions previously described 7 . Beyond maintaining ex situ populations 5 and increasing public understanding of biodiversity 21 , zoos carry out many more in situ projects than typically recognized (though see Olive and Jansen 12 ), including a large number of monitoring projects. We also found that zoos conduct a range of field- and zoo-based conservation research projects, which were nearly as numerous as ex situ breeding efforts (Fig.  1 ). Biodiversity monitoring and research both help to support successful species recovery, but they are not commonly viewed as significant ways in which zoos contribute to conservation. Our findings support earlier studies that showed these critical conservation actions are increasingly being funded or conducted by NGOs 28 , 29 , including zoos.

However, additional opportunities exist. We found that similar to zoo holdings overall 27 , managed SSP populations currently focus on non-threatened species. Among listed species, however, managed programs do tend to prioritize species that are more at risk of extinction. There are many considerations that determine the selection of species for zoo exhibits, and management programs are increasingly including conservation status in their decision-making. However, if a species is especially difficult to house, cannot reproduce successfully, or has low survivorship in zoos, then establishing ex situ populations may not be feasible or worthwhile. Further, there are ways to contribute to conservation even if zoos are managing the less at-risk species that are closely related to a threatened species, as discussed above.

U.S. zoos may also increase their conservation efforts by managing more native threatened species, as our results showed a tendency for SSP programs to focus on foreign-listed species. Ex situ populations would ideally be established in the species’ native range 2 , but currently >90% of the U.S. listed avian and terrestrial species do not have an SSP population in North American zoos. Further research is needed to evaluate whether and the extent to which those listed species would benefit from ex situ population management. Zoos are also carrying out relatively few education and outreach programs that directly impact listed species in the wild (Fig.  1B ). By including more native threatened species, zoos could develop associated education and outreach programs to engage the community most likely to impact the species and promote direct conservation actions. Of course, zoo education programs that do not directly affect wild populations are still valuable 21 , and we reiterate that our review did not summarize the magnitude of those existing efforts.

Finally, our findings suggest a need for greater coordination across zoos and better engagement with other conservation science partners. For example, 40 institutions reported working on various field conservation and research projects for the polar bear in the AZA surveys, but it is unclear the extent to which these efforts were coordinated to maximize their effectiveness. Only 5 recovery plans (for 5 species) named two or more zoos as the responsible party for any recovery action, suggesting such coordination among zoos is infrequent or poorly represented in plans. Only a quarter of the recovery plan actions conducted by zoos involved either academic or NGO partners, although integrating efforts into larger collaborations could lead to better outcomes 29 . However, coordination with other conservation partners may be increasing, as more partnerships between zoos and academic institutions are being formed ( e . g ., Smithsonian-Mason School of Conservation, the Phoenix Zoo - Arizona State University conservation partnership, the Living Earth Collaborative). Other zoo partnerships supporting species recovery include concentrated breeding centers and consortiums such as the Conservation Centers for Species Survival (C2S2), and AZA’s SAFE: Saving Animals From Extinction, a conservation framework launched in 2015 that prioritizes collaboration 14 . There are also efforts to integrate ex situ and in situ species management through the IUCN Conservation Planning Specialist Group’s One Plan Approach 30 , 31 .

In this assessment we focused on terrestrial and avian species listed under the ESA. Thus, the role of zoos in helping to conserve marine animals, plants, and species with other risk statuses remain to be examined. Additionally, further research is needed to evaluate the impacts of the many zoo conservation projects 18 , which could inform and improve future efforts. In summary, our study highlights the wide-ranging conservation actions conducted by North American zoos, and identify opportunities for better integration with the broader conservation community. By evaluating the current role of zoos in species conservation, our study provides a better understanding of the expertise, resources, and opportunities that zoos can offer as one of the many necessary partners in recovering threatened species.

Data availability

The recovery plan data analyzed in the current study are included in the Supplementary Information (Table  S2 ). The AZA survey data, except financial information, are available on AZA’s website ( http://www.aza.org/field-conservation ; http://www.aza.org/research-and-science ). Additional data are available from the corresponding author on reasonable request.

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Acknowledgements

We thank all of the AZA-accredited zoos, aquariums, and certified facilities that submitted information about their field conservation and research to AZA’s annual surveys. We also thank AZA’s Field Conservation and Research and Technology Committees for helping to refine surveys, review data submissions, and work with AZA members on their submissions. We thank A. Ahmad and S.Y. Kim for assistance with data compilation.

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J.P.C., S.G. and L.J.F. co-developed the project. S.G. compiled and analyzed the AZA survey data, and J.P.C. compiled and analyzed the recovery plan and managed program data, and prepared the manuscript and figures. All authors reviewed the manuscript.

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Correspondence to Judy P. Che-Castaldo .

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Che-Castaldo, J.P., Grow, S.A. & Faust, L.J. Evaluating the Contribution of North American Zoos and Aquariums to Endangered Species Recovery. Sci Rep 8 , 9789 (2018). https://doi.org/10.1038/s41598-018-27806-2

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The Role of Animal Experimentation in Endangering Species

On May 19th we celebrated Endangered Species Day, dedicated to learning about and taking action to protect endangered and threatened species. 2023 also marks the 50th anniversary of the landmark Endangered Species Act—a silver lining in the face of a sixth mass extinction .

The Endangered Species Act (ESA):

• Establishes protections for wildlife (including fish) and plants that are listed as threatened or endangered,
• Implements plans for the recovery of the aforementioned,
• Establishes provisions of the Convention on International Trade in Endangered Species of Wild Flora and Fauna ( CITES ),
• Calls for interagency cooperation to avoid issuing permits for listed species.

Despite the Endangered Species Act working to protect more than 1,300 listed species, many considered endangered by the International Union for Conservation of Nature (IUCN) are not covered by the ESA. Most notably the long-tailed and southern pig-tailed macaques.

Macaques are the most common non-human primates used in biomedical research and are the majority of the 113,000 non-human primates reportedly used in research in 2021 by the United States Department of Agriculture.

Even with the populations of both the long-tailed and southern pig-tailed macaques declining between 40-50% over the past few decades, the animal research industry’s demand continues to climb.

The United States Fish and Wildlife Service (USFWS) has the ability to grant protections to vulnerable species who face a single threatening factor, and these macaques face more than five each. Beyond animal research, these threats include pollution, residential and commercial development, agricultural development including factory farming, and the pet trade. The ESA can make it illegal to import, export, take, possess, sell, or transport listed threatened or endangered species.

Macaques are largely recognized by experts as adaptable generalist primates . The sharp decline in their numbers can be attributed to a two-pronged issue: the failure of the USFWS to protect these macaques by granting them protections under the ESA and the continued reliance on ineffective animal models for biomedical research.

Macaques, along with species including mice, rats, pigs, and birds, are subjected to cruel experimentation despite scientific research that reveals subtle nuances in physiology, biochemistry, and genetic expression drive misleading drug development.

In fact, between  90—95 percent of drugs  found safe and effective in animal tests fail during human clinical trials, primarily due to toxicities not predicted by animal tests or because of lack of efficacy.

We need to accelerate a shift away from animal experimentation, not only for the benefit of human health but to mitigate humanity’s role in the sixth mass extinction . Join us in protecting humans, animals, and the environment by supporting recent developments in medical science, such as human chip models, 3D printed human tissues, and organoids that more faithfully recapitulate human physiology than animal tests and have the potential to predict human safety much more accurately.

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Understanding Permits and Authorizations for Protected Species

Permits and authorizations allow people and entities—whether they are researchers, commercial fishermen, a public display facility, or an energy corporation—to conduct their activities legally under the Endangered Species Act and Marine Mammal Protection Act. Learn more about permits and authorizations for protected species.

Table of Contents

Why does noaa fisheries issue permits and authorizations for protected species, what’s the difference between directed and incidental take, what types of permits and authorizations are available for endangered and threatened species, what types of permits and authorizations are available for marine mammals, for what activities does noaa fisheries issue permits, which protected species require a permit from noaa fisheries, do i need a permit, how can i find out about pending and issued permits and authorizations.

The  Endangered Species Act and the  Marine Mammal Protection Act are two laws that protect endangered and threatened species and marine mammals. These laws make it illegal to take, export, and import these species or their parts. Some examples of “take” actions are harassing, hunting, capturing, collecting, trapping, and killing protected animals. Learn more about take .

However, there are some exceptions that make it legal to take, export, or import protected animals, such as marine mammals or sea turtles.

Permits and authorizations allow people and entities—whether they are researchers, commercial fishermen, a public display facility, or an energy corporation—to conduct their activities legally under the ESA and MMPA.

By issuing permits and authorizations, NOAA Fisheries is able to:

• Allow important activities to occur that are compliant with the ESA and/or the MMPA.
• Ensure that mitigation measures are implemented to reduce the impact of the activities.
• Keep track of the activities and how they impact protected species.

Directed take means that the activity is a purposeful interaction with the protected animal for a specific purpose that may result in take. Examples include:

• Capturing animals and taking measurements and samples to study their health.
• Tagging animals to study their distribution and migration.
• Photographing and counting animals to get population estimates.
• Taking animals in poor health to an animal hospital.
• Filming animals for a documentary.

Incidental take means that the activity is unrelated to the protected species, but the protected species may still be affected. In these cases, the take is unintentional. Examples include:

• Commercial fishing operations.
• Oil and gas development.
• Seismic surveys.
• Military readiness activities.
• Power plant operations.
• Construction projects.

Directed Take

• For scientific purposes—these are permits for research to study species listed under the  Endangered Species Act . Examples include permits for someone studying endangered salmon in California or the health of  sea turtles  off Florida. Some researchers have permits to import samples of endangered species to study genetics.
• For enhancement purposes—these are permits to enhance or aid the recovery of endangered species. Examples include:
• Protective regulations—sometimes when species are listed as threatened under the ESA, NOAA Fisheries writes protective regulations. For example, our salmon, steelhead, and green sturgeon 4(d) rules  prohibit take, except for specific categories of activities that are described in the rule.
• Relocating endangered seal pups to a safer location.
• Disentangling large whales from life-threatening fishing gear.
• Collecting broodstock for salmon and steelhead hatchery programs.
• Establishing and maintaining experimental populations.

Incidental Take

The ESA allows for permits for activities that take protected species incidental to otherwise lawful activities. In these cases, the person or agency is not trying to take the protected species, but they may do unintentionally during their operations. Examples include:

• Catching sea turtles in a state commercial fishery.
• Operating power plants with cooling water intake structures that may capture protected sturgeon.
• Operating hydropower projects.
• Managing private timberlands.
• Maintaining municipal water supply systems.

Some marine mammals, like blue whales  and Hawaiian monk seals , are listed as endangered or threatened under the ESA. Because these species are also protected under the  Marine Mammal Protection Act , permits and authorizations for activities on these species must comply with both laws.

• For scientific purposes—these are permits for research to study marine mammals. Examples include people studying feeding behavior of bottlenose dolphins  off North Carolina, how Weddell seals raise young in Antarctica, or the physiology of harbor seals  held for captive research at a university. Some researchers have research permits to import tissue samples to study genetics or other aspects of marine mammal biology.
• For enhancement purposes—these permits are issued to enhance the survival or recovery of a species or stock in the wild by taking actions that increase an individual’s or population’s ability to recover in the wild. For example, adult male Hawaiian monk seals  that are known to attack and kill pups have been removed from sensitive islands in an effort to increase pup survival.
• For commercial/educational photography—these permits are issued to filmmakers and photographers working on documentaries, movies, and articles featuring marine mammals.
• For public display—these permits allow marine mammals to be imported or captured from the wild for public display . 
• For responding to marine mammals in need—these authorizations allow government employees and other designated responders to help marine mammals for the protection or welfare of the animal or the public (e.g., transporting sick or injured animals to an animal hospital), or to address nuisance animals.
• During commercial fisheries—owners of commercial fishing vessels or non-vessel fishing gear that are working in certain fisheries must obtain a marine mammal authorization certificate. This certificate provides legal coverage if marine mammals are accidentally caught and/or harmed during fishing operations. The certificates are issued under the  Marine Mammal Authorization Program . 
• During non-commercial fishery activities—these authorizations are issued for projects such as military sonar and training exercises, oil and gas development, construction projects, explosive structure removal, and geophysical surveys. Two types of authorizations are issued in this category: Incidental Harassment Authorizations and Letters of Authorization.

Some marine mammals, like sperm whales  and Hawaiian monk seals , are listed as endangered or threatened under the Endangered Species Act . Because these species are protected under both the Marine Mammal Protection Act  and the Endangered Species Act , permits and authorizations for activities on these species must be compliant under both laws.

NOAA Fisheries issues a variety of permits under both the Endangered Species Act and the Marine Mammal Protection Act .

Incidental Take Authorizations and Permits

Under the MMPA, incidental take authorizations are issued for activities that are not directed at marine mammals but may result in take. Most incidental take authorizations have been issued for activities that produce underwater sound. Examples include:

• Military sonar and training exercises.
• Oil and gas development, exploration, production, and abandonment projects.
• Geophysical surveys for other energy and scientific research projects.
• Pile driving associated with construction projects.
• Explosive structure removal.

Other authorizations are issued for marine mammal takes during commercial fishing operations.

Under the ESA, incidental take permits are typically issued when threatened or endangered species may be affected during the operation of:

• State commercial and recreational fisheries in state waters.
• Power plants with cooling water intake structures.

A habitat conservation plan must accompany an application for an ESA incidental take permit. The habitat conservation plan helps ensure that the effects of the authorized incidental take are minimized or mitigated to the maximum extent practicable.

Directed Take Permits

Directed take permits are issued under the ESA and/or the MMPA for activities such as:

• Scientific research on wild animals, captive animals, or parts of protected species (e.g., blood, tissue, bones, whiskers).
• Activities that enhance the propagation or survival of the species.
• Commercial/educational photography.
• Import of a marine mammal for public display.

Under the  Endangered Species Act , NOAA Fisheries has jurisdiction over endangered and threatened marine species including some marine mammals, some marine and anadromous fish, some marine invertebrates, sea turtles when in the water, and one marine plant. Protected species include both vertebrates and invertebrates and both domestic and foreign species. Examples include:

• Shortnose sturgeon
• Sacramento River winter-run Chinook salmon
• Common angelshark
• Leatherback sea turtle
• Loggerhead sea turtle
• Steller sea lion
• White abalone
• Elkhorn coral

See the full list of endangered and threatened species managed by NOAA Fisheries

Under the Marine Mammal Protection Act , NOAA Fisheries has jurisdiction over all whales, dolphins and porpoises (cetaceans), and seals and sea lions (pinnipeds). Examples include:

• Spinner dolphin
• Killer whale
• North Atlantic right whale
• Harbor porpoise
• California sea lion
• Humpback whale
• Ribbon seal
• Northern elephant seal
• Bottlenose dolphin

See the full list of marine mammals managed by NOAA Fisheries

Because some species protected under the ESA and/or the MMPA are under the jurisdiction of the U.S. Fish and Wildlife Service, permits and authorizations for activities affecting those species are issued by the U.S. FWS. Examples include sea turtles on land, walrus, manatees, polar bears, and sea otters. Visit the U.S. FWS website to learn more:

• U.S. FWS Endangered Species
• U.S. FWS Marine Mammal Laws and Regulations
• U.S. FWS Marine Mammal Permits  

You may need a permit or authorization if you will be conducting activities that directly or indirectly affect endangered or threatened species or marine mammals. Permits may be issued to federal, state, and local agencies, universities, corporations, individuals, and non-governmental organizations.

To get started, view the  Pre-Application Guide  in NOAA Fisheries’ online application system for authorizations and permits for protected species. This guide will help you determine the type of permit you need and how to apply for it.

For information about incidental take of marine mammals during commercial fishing and how to obtain a certificate, visit our  Marine Mammal Authorization Program page . 

• Search the Federal Register . Many permits and authorizations for protected species have public comment periods that are published in the Federal Register. Notices are also published in the Federal Register when certain permits or authorizations are issued.
• Use our online application system for authorizations and permits for protected species (APPS) . Most applications for directed take permits under the Endangered Species Act and Marine Mammal Protection Act can be found here, including those currently available for public comment. You can also use APPS to search issued and expired directed take permits .
• Visit our Marine Mammal Protection Act incidental take authorization page to find which applications for marine mammal incidental take have been submitted, issued, and expired, as well as related and supporting documents for each application.

April 15, 2009

How Do Zoos Help Endangered Animals?

There are more to zoos than putting animals on display

Dear EarthTalk: Do zoos have serious programs to save endangered species, besides putting a few captives on display for everyone to see? -- Kelly Traw, Seattle, WA

Most zoos are not only great places to get up close to wildlife, but many are also doing their part to bolster dwindling populations of animals still living free in the wild. To wit, dozens of zoos across North America participate in the Association of Zoos and Aquarium’s (AZA’s) Species Survival Plan (SSP) Program, which aims to manage the breeding of specific endangered species in order to help maintain healthy and self-sustaining populations that are both genetically diverse and demographically stable.

The end goal of many SSPs is the reintroduction of captive-raised endangered species into their native wild habitats. According to the AZA, SSPs and related programs have helped bring black-footed ferrets, California condors, red wolves and several other endangered species back from the brink of extinction over the last three decades. Zoos also use SSPs as research tools to better understand wildlife biology and population dynamics, and to raise awareness and funds to support field projects and habitat protection for specific species. AZA now administers some 113 different SSPs covering 181 individual species.

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To be selected as the focus of an SSP, a species must be endangered or threatened in the wild. Also, many SSP species are “flagship species,” meaning that they are well-known to people and engender strong feelings for their preservation and the protection of their habitat. The AZA approves new SSP programs if various internal advisory committees deem the species in question to be needy of the help and if sufficient numbers of researchers at various zoos or aquariums can dedicate time and resources to the cause.

AZA’s Maryland-based Conservation and Science Department administers the worldwide SSP program, generating master plans for specific species and coordinating research, transfer and reintroductions. Part of this process involves designing a “family tree” of particular managed populations in order to achieve maximum genetic diversity and demographic stability. AZA also makes breeding and other management recommendations with consideration given to the logistics and feasibility of transfers between institutions as well as maintenance of natural social groupings. In some cases, master plans may recommend not to breed specific animals, so as to avoid having captive populations outgrow available holding spaces.

While success stories abound, most wildlife biologists consider SSP programs to be works in progress. AZA zoos have been instrumental, for instance, in establishing a stable population of bongos, a threatened forest antelope native to Africa, through captive breeding programs under the SSP program. Many of these captive-bred bongos have subsequently been released into the wild and have helped bolster dwindling population numbers accordingly.

Of course, for every success story there are dozens of other examples where results have been less satisfying . SSP programs for lowland gorillas, Andean condors, giant pandas and snow leopards, among others, have not had such clear success, but remain part of the larger conservation picture for the species in question and the regions they inhabit.

CONTACTS : AZA’s Conservation & Science Program, www.aza.org/Conscience .

EarthTalk is produced by E/The Environmental Magazine. SEND YOUR ENVIRONMENTAL QUESTIONS TO: EarthTalk , P.O. Box 5098, Westport, CT 06881; [email protected] . Read past columns at: www.emagazine.com/earthtalk/archives.php . EarthTalk is now a book! Details and order information at: www.emagazine.com/earthtalkbook .

ORIGINAL RESEARCH article

Conservation genomic study of hopea hainanensis (dipterocarpaceae), an endangered tree with extremely small populations on hainan island, china.

• 1 Hainan University, Haikou, China
• 2 Haikou Marine Geological Survey Center, China Geological Survey, Haikou, Hainan Province, China
• 3 Chinese Research Academy of Environmental Sciences, Beijing, Beijing Municipality, China

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Hopea hainanensis Merrill & Chun is considered a keystone and indicator species in the tropical lowland rainforests of Hainan Island. Due to its high-quality timber, H. hainanensis has been heavily exploited, leading to its classification as a First-Class National Protected Plants in China and a Plant Species with Extremely Small Populations (PSESP). This study analyzed genome-wide single nucleotide polymorphisms (SNPs) obtained through Restriction site-associated DNA sequencing (RAD-seq) from 78 adult trees across 10 H. hainanensis populations on Hainan Island. The nucleotide diversity of the sampled populations ranged from 0.00096 to 0.00138, which is lower than that observed in several other PSESP and endangered tree species. Bayesian unsupervised clustering, principal component analysis, and NJ tree reconstruction identified 3 to 5 genetic clusters in H. hainanensis, most of which were geographically widespread and shared by multiple populations. Demographic history analysis based on pooled samples indicated that the decline of the H. hainanensis population began approximately 20,000 years ago, starting from an ancestral population size of about 10,000 individuals. The reduction of population size accelerated around 4,000 years ago and has continued to the present, resulting in a severely reduced population on Hainan Island. Intensified genetic drift in small and isolated H. hainanensis populations may contribute to moderate differentiation between some of them, as revealed by pairwise Fst. In conclusion, our conservation genomic study confirms severe population decline and extremely low level of nucleotide variation in H. hainanensis on Hainan Island. These findings provide critical insights for the sustainable management and genetic restoration of H. hainanensis on Hainan Island.

Keywords: Hopea hainanensis Merrill & Chun, conservation genomics, Plant Species with Extremely Small Populations, Population decline, Reduced-representation genome sequencing

Received: 03 Jun 2024; Accepted: 09 Aug 2024.

Copyright: © 2024 Tang, Long, Wang, Rao, Long, Yan and Liu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Liang Tang, Hainan University, Haikou, China Jun-qiao Long, Haikou Marine Geological Survey Center, China Geological Survey, Haikou, 571127, Hainan Province, China Hai-ying Wang, Hainan University, Haikou, China Li Yan, Haikou Marine Geological Survey Center, China Geological Survey, Haikou, 571127, Hainan Province, China Yong-bo Liu, Chinese Research Academy of Environmental Sciences, Beijing, Beijing Municipality, China

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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Endangered and Threatened Species; Take of Anadromous Fish

A Notice by the National Oceanic and Atmospheric Administration on 08/08/2024

This document has been published in the Federal Register . Use the PDF linked in the document sidebar for the official electronic format.

• Document Details Published Content - Document Details Agencies Department of Commerce National Oceanic and Atmospheric Administration Agency/Docket Number RTID 0648-XE166 Document Citation 89 FR 64880 Document Number 2024-17410 Document Type Notice Pages 64880-64886 (7 pages) Publication Date 08/08/2024 Published Content - Document Details
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Supplementary information:, species covered in this notice, applications received, permit 1386-11m, permit 1484-8r, permit 1523-5r, permit 15205-5r, permit 15230-4r, permit 16298-5r, permit 17062-7r, permit 17761-3r, permit 18852-3r, permit 18921-3r, permit 19263-3r, permit 22944-2r, permit 23629-2r, permit 23843-2r, permit 26776, permit 27091-2m, permit 27824, permit 28055, permit 28158, permit 28199, permit 28292.

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Department of Commerce

National oceanic and atmospheric administration.

• [RTID 0648-XE166]

National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), Commerce.

Notice of receipt of application; 13 permit renewals, 2 permit modifications, and 6 new permits.

Notice is hereby given that NMFS has received 21 scientific research permit application requests relating to Pacific salmon, steelhead, green sturgeon, rockfish, and eulachon. The proposed research is intended to increase knowledge of species listed under the Endangered Species Act (ESA) and to help guide management and conservation efforts.

Comments or requests for a public hearing on the applications must be received at the appropriate address or fax number (see ADDRESSES ) no later than 5 p.m. Pacific standard time on September 9, 2024.

All written comments on the applications should be sent by email to [email protected] (please include the permit number in the subject line of the email).

The applications may be viewed online at: https://apps.nmfs.noaa.gov/​preview/​preview_​open_​for_​comment.cfm .

Diana Dishman, Portland, OR (ph.: 503-736-4466), email: [email protected] ). Permit application instructions are available from the address above, or online at https://apps.nmfs.noaa.gov .

The following listed species are covered in this notice:

Chinook salmon ( Oncorhynchus tshawytscha ): Threatened Puget Sound (PS); threatened Snake River (SnkR) fall-run; threatened SnkR spring/summer-run; endangered Upper Columbia River (UCR) spring-run; threatened Upper Willamette River (UWR); threatened Lower Columbia River (LCR); endangered Sacramento River (SacR) winter-run; threatened California Coastal (CC).

Steelhead ( O. mykiss ): Threatened Middle Columbia River (MCR); threatened PS; threatened SnkR Basin; threatened UCR; threatened UWR; threatened Central California Coast (CCC); threatened California Central Valley (CCV); threatened Northern California (NC); threatened LCR.

Chum salmon ( O. keta ): Threatened Hood Canal summer-run (HCS); threatened Columbia River (CR).

Coho salmon ( O. kisutch ): threatened Southern Oregon/Northern California Coast (SONCC); endangered Central California Coast (CCC); threatened LCR.

Sockeye salmon ( O. nerka ): Endangered SnkR; Threatened Ozette Lake (OL).

Eulachon ( Thaleichthys pacificus ): Threatened southern (S).

Rockfish: Endangered Puget Sound/Georgia Basin (PS/GB) Boccacio ( Sebastes paucispinis ) Distinct Population Segment (DPS); threatened PS/GB Yelloweye ( Sebastes ruberrimus ) DPS.

Green sturgeon ( Acipenser medirostris ): Threatened southern Distinct Population Segment (SDPS).

Scientific research permits are issued in accordance with section 10(a)(1)(A) of the ESA ( 16 U.S.C. 1531 et. seq ) and regulations governing listed fish and wildlife permits ( 50 CFR 222-226 ). NMFS issues permits based on findings that such permits: (1) are applied for in good faith; (2) if granted and exercised, would not operate to the disadvantage of the listed species that are the subject of the permit; and (3) are consistent with the purposes and policy of section 2 of the ESA. The authority to take listed species is subject to conditions set forth in the permits.

Anyone requesting a hearing on an application listed in this notice should set out the specific reasons why a hearing on that application would be appropriate (see ADDRESSES ). Such hearings are held at the discretion of the Assistant Administrator for Fisheries, NMFS.

Under permit 1386-11M, the Washington Department of Ecology (WDOE) is seeking to modify a permit that would authorize them to continue taking adult and juvenile PS Chinook salmon, PS steelhead, HCS chum salmon, OL sockeye salmon, UCR spring-run Chinook salmon, UCR steelhead, MCR steelhead, SnkR spring/summer-run Chinook salmon, SnkR fall-run Chinook salmon, SnkR steelhead, LCR Chinook salmon, LCR coho salmon, LCR steelhead, and CR chum salmon. in order to characterize toxic contaminants in resident freshwater fish across Washington.

The WDOE conducts this research in order to meet Federal and State regulatory requirements. This research would benefit listed species by identifying toxic contaminants in resident and prey fish and thereby inform pollution control actions. The WDOE proposes to capture fish using various methods including backpack and boat electrofishing, beach seining, block, fyke, and gill netting, and angling. All captured salmon and steelhead would either be released immediately or held temporarily in an aerated live well to help them recover before release. The researchers do not propose to kill any fish but a small number may die as an unintended result of research activities.

Under permit 1484-8R, the Washington Department of Natural Resources (WA DNR), Pacific Cascade Region, is seeking to renew for 5 years a permit that would authorize them to continue taking juvenile MCR steelhead, LCR Chinook salmon, LCR coho salmon, LCR steelhead, and CR chum salmon in order to identify fish-bearing streams on WA DNR land in Southwest Washington. Most streams are typed as fish or non-fish bearing based on the physical characteristics of average width and gradient, and connectivity to established fish-bearing waters. This activity will occur on WA DNR land in Lewis, Pacific, Grays Harbor, Wahkiakum, Clark, Cowlitz, Skamania, and Klickitat counties in the state of Washington.

Juveniles would be collected via backpack electrofishing, and would be captured, handled (weighed, measured, and checked for marks or tags), and released. The captured fish would be identified and released back to the waters from which they came. In some cases, the researchers may not actually capture any fish but would merely note their presence, however electrofishing where listed species are observed would still be reported as take. The researchers are not proposing to kill any of the listed fish being taken, but a small number may be killed as an inadvertent result of these activities. The information gathered would be used to determine salmonid presence and distribution and thereby inform land management decisions on WA DNR holdings. This information would benefit listed species by helping WDNR identify existing man-made fish barriers, and ensuring fish-bearing streams receive adequate riparian buffers.

Under permit 1523-5R, the National Council for Air and Stream Improvements (NCASI) is seeking to renew for 5 years a permit that would authorize them to continue taking juvenile and adult UWR Chinook salmon in order to study water quality and biological conditions in rivers receiving paper and pulp mill discharges from their facilities. This work would take place in the upper Willamette and McKenzie Rivers in Oregon.

Adult and juvenile fish would be collected via backpack electrofishing or boat electrofishing. Juvenile and adult fish may be captured, handled (weighed, measured, and checked for marks or tags), and released. In some cases, the researchers may not actually capture any fish but would merely note their presence, however electrofishing where listed species are observed would still be reported as take. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The goal of the project is to identify changes in physical, chemical, and biological conditions in discharge watersheds, including biological assessments of periphyton, macroinvertebrate, and resident fish communities. Monitoring natural variability as well as changes resulting from pulp and paper mill discharges will allow researchers to identify where key sources of fish stress from impaired water quality are in the context of the larger watershed, and to rank the magnitude of those stressors. This study focuses on resident fish rather than migratory species such as ESA-listed salmon and steelhead, however, we expect that identifying areas with impaired water quality or habitat will benefit recovery planning for listed as well.

Under permit 15205-5R, Kwiáht the (Center for the Historical Ecology of the Salish Sea) is seeking to renew for 5 years a permit that would authorize them to continue taking juvenile PS Chinook salmon in order to understand long term changes in the food web that supports Salish Sea Chinook salmon populations. This work would take place on Lopez Island, Waldron Island, and Decatur Island in San Juan County, Washington.

Juveniles would be collected via beach seine. Juvenile fish identified as hatchery-origin would be captured, and may be handled (measured, weighed, and checked for marks or tags) prior to release. Captured natural-origin juveniles would be anesthetized, checked for marks and tags, lavaged for stomach contents, and tissue sampled prior to release. Scales shed during handling would also be retained. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this work is to characterize the food web supporting rearing juvenile Chinook salmon in the nearshore habitats of the San Juan Islands, and is expected to benefit ESA-listed PS Chinook salmon by identifying factors that may be limiting the growth and survival of outmigrating juveniles. A regime shift in regional weather patterns starting in 2014-2015 may have de-synchronized the relationship between outmigrating juvenile Chinook salmon and availability of prey, and this work aims to evaluate whether naturally-produced Chinook salmon can adapt to changes in key prey resources.

Under permit 15230-4R, the West Fork Environmental, Inc. is seeking to renew for 5 years a permit that would authorize them to continue taking juvenile PS Chinook salmon and PS steelhead in order to better understand the seasonal use of various reaches of the Tolt River by juvenile summer steelhead prior to their outmigration as smolts. These activities would take place in King County, Washington.

Juveniles would be collected via backpack electrofishing and hook and line angling. Juvenile Chinook salmon would be captured, handled (weighed, measured, checked for marks and tags), and released. Captured juvenile steelhead would be anesthetized, tissue sampled and PIT-tagged prior to release. A subset of steelhead will also have scale samples collected. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this study is to understand the reach-specific characteristics of juvenile summer steelhead rearing in the Tolt River across seasons, including information about timing of movement, size at age, and growth of juvenile steelhead in the upper reach. This work will also provide a better understanding of juvenile and adult summer steelhead movement across seasons, and the relative contribution of hatchery-origin fish to the summer steelhead population. This work is expected to benefit ESA-listed PS steelhead by informing managers about factors that may be limiting steelhead production within the Tolt River basin.

Under permit 16298-5R, the Shoshone-Bannock Tribes Fisheries Department is seeking to renew for 5 years a permit that would authorize them to continue taking adult SnkR spring/summer-run Chinook salmon and SnkR Basin steelhead in order to measure adult and juvenile Chinook salmon abundance and other salmon population viability parameters in Bear Valley Creek, Idaho.

Juveniles would be collected via screw trap, and the majority would be captured, handled (weighed, measured, and checked for marks and tags), and released. A subsample of captured juveniles would be anesthetized, tissue sampled, PIT-tagged, and may also have scale samples collected prior to release. Adults would be observed via a temporary fish counting station comprising a fish funneling weir, fish counting chamber, video surveillance system, and PIT tag antenna. Spawning ground surveys and creel surveys would also be conducted to enumerate spawning adults. No adult capture, handling, sampling, or tagging is proposed, but fish may be unintentionally injured or killed if impinged on or entangled in the weir. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this work is to continue maintaining a long-term dataset for Chinook salmon in Bear Valley Creek that includes information on abundance, productivity, spatial structure, run-timing, proportion of hatchery-origin contribution to the population, and genetic diversity. This work is expected to benefit ESA-listed SnkR Chinook salmon and steelhead by assisting fishery resource managers in identifying key factors that are preventing recovery in this basin.

Under permit 17062-7R, the NMFS Northwest Fisheries Science Center (NWFSC) is seeking to renew a permit that would authorize them to continue taking juvenile and adult PS Chinook salmon, PS steelhead, PS/Georgia Basin DPS bocaccio, PS/Georgia Basin DPS yelloweye rockfish, HCS chum salmon, and adult Southern DPS eulachon in order to collect demographic information and genetic samples from rockfish in Puget Sound. This work would take place across the main basins of Puget Sound, Hood Canal, and the San Juan Islands and other coastal areas in northern Puget Sound and the Strait of Juan de Fuca in the state of Washington.

Juveniles would be collected via minnow trap, moored mesh bags, hand or dip nets, and hook and line angling. Any Chinook salmon, steelhead, or chum collected would be handled (weighed, measured, checked for marks and tags) and released. Adult eulachon may also be unintentionally captured via these methods and would be released. Juvenile rockfish would be intentionally lethally sacrificed for genetic, tissue, and otolith analysis, and a small number may be from ESA-listed bocaccio or yelloweye rockfish DPSs. Adult salmon, steelhead, and rockfish would be collected via hook and line angling. Adult salmon and steelhead would be released without bringing them on board research vessels. Adult rockfish would be handled (weighed, measured, checked for marks and tags), tissue sampled, and floy-tagged prior to release at depth using a rapid descending device. The researchers are proposing to kill a small number of listed juvenile rockfish, and a small number of additional juvenile and adult fish may be killed as an inadvertent result of these activities.

The goal of this work is to collect biological, genetic, physiological and habitat information to evaluate bocaccio DPS structure and investigate how rocky reef, kelp forest, and eelgrass habitat characteristics affect the relative quality of these areas as nursery habitat for rockfishes in Puget Sound. This work is expected to benefit ESA-listed rockfish by providing more information on the structure of the endangered bocaccio DPS, and on juvenile rearing habitat quality and trophic relationships of rockfish relevant to managing yelloweye rockfish and bocaccio for recovery.

This study falls within the scope of the NWFSC research program that we previously analyzed in Biological Opinion WCRO-2023-01601. In that opinion, we concluded that the NWFSC research program would not jeopardize the continued existence of any ESA-listed species or destroy or adversely modify their critical habitats. In reaching our conclusion, we also considered activities related to permitting or authorizing individual studies under that research program for up to 10 years. Therefore, neither this study nor subsequently issuing a section 10(a)(1)(A) permit requires further consultation under the ESA.

Under permit 17761-3R, the East Bay Municipal Utility District is seeking to renew a permit that would authorize them to take adult and juvenile CCV steelhead in order to conduct monitoring and research of anadromous and resident fishes in the lower Mokelumne River. This work would take place in the San Joaquin Valley, in California.

Juveniles would be collected via backpack electrofishing, boat electrofishing, hook and line angling, beach seine, incline plane trap, screw trap, fish ladder, fyke trap, bypass trap, snorkel survey, and midwater trawl. All juvenile steelhead captured would be handled (weighed, measured, checked for marks and tags), and may be anesthetized as needed to collect accurate measurements, prior to release. A subsample of captured juveniles would be anesthetized, tissue sampled, and may be marked with photonic dye, elastomer tags, coded-wire tags, PIT-tags, acoustic tags, or floy tags prior to release. A subset of captured juvenile steelhead would also be gastric lavaged for stomach contents. A batch of hatchery-reared juvenile steelhead may also be implanted with acoustic tags prior to release.

Adults would be collected via fish weir, boat electrofishing, fish ladder, hook and line angling, incline plane trap, screw trap, fyke trap, and midwater trawl. Adults would be captured, handled (anesthetized, weighed, measured, and checked for marks or tags), and released. A subsample of captured adults would be anesthetized, tissue sampled and may be marked with photonic dye, elastomer tags, coded-wire tags, PIT-tags, acoustic tags, or floy tags prior to release. A subset of captured adult steelhead would also be gastric lavaged for stomach contents. Spawned adults or post-spawn carcasses would be enumerated via spawning surveys. Juvenile and adult fish would also be observed during snorkel surveys and video monitoring in the fish ladder. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The goals of this project are to measure the success of the Lower Mokelumne River Restoration Program and determine if the modifications of the Lower Mokelumne River Project are appropriate for conserving fish and wildlife resources in the lower Mokelumne River. This project is expected to benefit ESA-listed species by providing scientific data to the Central Valley Project Improvement Act (CVPIA) Comprehensive Assessment and Monitoring Program (CAMP) to evaluate the relative effectiveness of CVPIA actions in restoring anadromous fish production.

Under permit 18852-3R, the U.S. Fish and Wildlife Service (USFWS) Mid-Columbia Fish and Wildlife Conservation Office is seeking to renew for 5 years a permit that would authorize them to continue taking juvenile and adult UCR spring-run Chinook salmon, UCR steelhead, and MCR steelhead in order to define the distribution and status of Pacific Lamprey, Bull Trout, and other native fish species. This work would take place in the Yakima, Wenatchee, Entiat, Methow, and Okanogan watersheds in the state of Washington.

Juveniles would be collected via backpack electrofishing, hand or dip net, fish ladders and weirs, minnow traps, and fyke nets. Most juvenile Chinook salmon and steelhead would not be targeted and, if captured, would be handled and immediately released. A subsample of captured juveniles may be anesthetized to identify species, obtain weights and measurements, and scanned for PIT tags before being released. Juvenile MCR steelhead trout captured in the Yakima Basin may be PIT-tagged and tissue sampled as well. Adults would be collected at dams and other structures and in traps, and may be caught by hook and line angling. Adult Chinook salmon or steelhead would be captured, handled (anesthetized, weighed, measured, and checked for marks or tags), and released, and may be anesthetized to identify species, obtain weights and measurements, and scanned for PIT tags before being allowed to recover and released. Spawned adults or post-spawn carcasses would be enumurated via spawning surveys. Juvenile and adult fish would also be observed during snorkel surveys. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this project is to assess recovery actions including capture and transport of Bull Trout to upstream of barriers, assessing fish utilization of restored habitat, and assessing Pacific Lamprey passage at existing structures and at lamprey-passage-engineered structures. This work is expected to benefit ESA-listed fish under the jurisdiction of the USFWS, and also provide information on passage barriers and habitat use relevant to managing listed Chinook salmon and steelhead in the UCR and MCR.

Under permit 18921-3R, the Samish Indian Nation is seeking to renew a permit that would authorize them to continue taking juvenile PS Chinook salmon and PS steelhead, and adult southern DPS eulachon in order to monitor the presence of fish species within and around the Cypress Island Secret Harbor restoration site. This work would take place on Cypress Island in Skagit County, Washington.

Juvenile PS Chinook salmon and steelhead and adult eulachon would be collected via beach seine. Captured fish would be handled (weighed, measured, and checked for marks or tags), and released. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this work is to assess the effectiveness of the Cypress Island Secret Harbor restoration project over 10 years after it was completed; particularly forage fish and salmonid habitat use within the site. Effective restoration at this site is expected to increase the amount of high quality estuarine habitat available to rearing PS Chinook salmon and steelhead juveniles, and this monitoring will provide managers information about whether the intended benefit has been realized.

Under permit 19263-3R, the Idaho Department of Fish and Game (IDFG) is seeking to renew for 5 years a permit that would authorize them to continue taking juvenile SnkR spring/summer-run Chinook salmon, SnkR Basin steelhead, and SnkR sockeye salmon in order to determine the distribution and abundance of various fish species in the Salmon River basin. This work would take place throughout the Salmon River basin in Idaho.

Juveniles would be collected via boat electrofishing. Juveniles of all three ESA-listed species may be anesthetized during capture and handling, however any SnkR sockeye juveniles will be released without tagging. A subsample of captured juvenile Chinook salmon and steelhead may be anesthetized, tissue sampled and PIT-tagged prior to release. In some cases, the researchers may not actually capture any fish but would merely note their presence, however electrofishing where listed species are observed would still be reported as take. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this project is to address various IDFG priority fisheries management and research issues relevant to their mandates, and to evaluate completed habitat restoration activities and prioritize future restoration actions. Both ESA-listed and resident fish are expected to benefit from research that will help inform decisions about how and where to protect and improve habitat conditions throughout the upper Salmon River basin.

Under permit 22944-2R, the NMFS NWFSC is seeking to renew a permit that would authorize them to continue taking juvenile UCR spring-run Chinook salmon, UCR steelhead, MCR steelhead, SnkR spring/summer-run Chinook salmon, SnkR fall-run Chinook salmon, SnkR Basin steelhead, SnkR sockeye salmon, LCR Chinook salmon, LCR coho salmon, LCR steelhead, CR chum salmon, Upper Willamette River Chinook salmon, and Upper Willamette River steelhead in order to document patterns of habitat occurrence, diet, and health indicators in juvenile salmon and steelhead in the Lower Columbia River. This work would take place in nearshore areas of the Lower Columbia River in Washington and Oregon, and in the Lower Willamette River in Oregon.

Juvenile salmon and steelhead would be collected via beach seine. Juvenile fish would be captured, handled (weighed, measured, and checked for marks and tags), and may be anesthetized to obtain measurements prior to release. A subsample of captured Chinook salmon juveniles would be anesthetized and further tissue sampled and PIT-tagged prior to release, and a small number would also be intentionally lethally sacrificed to determine their lipid content, conduct otolith analysis for health and growth assessment, do stomach content diet analyses, and take tissue samples for genetic stock identification. The researchers are proposing to kill a small number of listed fish, and a small number of fish may also be killed as an inadvertent result of these activities.

The objectives of the study are to better understand how juvenile salmonids utilize tidal freshwater habitats in the Columbia, to assess the quality of representative habitats in the lower river, to provide baseline data to guide habitat restoration and remediation activities, and to monitor the success of such activities at selected sites. The study is expected to benefit ESA-listed fish species by providing relevant information on (a) how habitat degradation may be affecting listed stocks that migrate through the Lower Columbia River and (b) what steps that can be taken to improve habitat quality.

Under permit 23629-2R, the U.S. Geological Survey (USGS) is seeking to renew for 5 years a permit that would authorize them to continue taking adult UWR Chinook salmon and SONCC coho salmon in order to evaluate contaminant exposure, bioaccumulation, and effects in aquatic ecosystems and aquatic-dependent wildlife by assessing a wide range of contaminants ( e.g., mercury, lead, copper, selenium, pesticides, organochlorines, PDBEs, and other emerging contaminants) in various fish and inland aquatic invertebrate species over a range of habitats and locations. This work would take place in the Willamette and Rogue River basins in the state of Oregon.

Juvenile and adult salmon would be collected via backpack electrofishing, boat electrofishing, hook and line angling, gill net, beach seine, and minnow trap. This contaminant study targets resident fish species and does not target ESA-listed salmon and steelhead, therefore listed fish would be captured, handled (weighed, measured, and checked for marks or tags), and swiftly released. In some cases, the researchers may not actually capture any fish but would merely note their presence, however electrofishing where listed species are observed would still be reported as take. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this work is to evaluate contaminant risks in aquatic ecosystems of the Pacific Northwest and assess the factors that influence contaminant exposure and effects in aquatic wildlife. This work is expected to benefit ESA-listed salmon by providing greater understanding on where and why contaminant threats exist, what impacts they may have on ecological function, and how management efforts can be targeted to minimize potential risk and thereby help recovery planning for these species.

Under permit 23843-2R the Skagit River System Cooperative is seeking to renew a permit that would authorize them to take juvenile PS Chinook salmon and PS steelhead in order to measure changes in fish densities, smolt production, and habitat attributable to restoration activities to continue the assessment of restoration efforts within the Skagit River and its floodplain. This work will take place in multiple locations across the Skagit River Basin in the State of Washington.

Juveniles PS Chinook salmon and steelhead would be collected via weir, backpack electrofishing, boat electrofishing, or beach seining. Juvenile fish would be captured, handled (weighed, measured, and checked for marks or tags), and released. A subsample of captured juveniles would marked with a caudal fin clip or dye prior to release. In some cases, the researchers may not actually capture any fish but would merely note their presence, however electrofishing where listed species are observed would still be reported as take. Spawning adults or post-spawn carcasses would be enumurated via spawning surveys. Juvenile and adult fish would also be observed during snorkel surveys. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The goals of this project are to conduct traditional restoration effectiveness monitoring following restoration projects in the Skagit River Basin, and also contribute to development of a fish and habitat association model to inform restoration design. This work is expected to benefit ESA-listed fish by informing adaptive management of one restoration site specifically (Barnaby Slough) to increase the likelihood it will provide the expected habitat benefits for PS Chinook salmon and steelhead, and more broadly, improved fish and habitat association models that incorporate hydrodynamics will inform future restoration design.

Under permit 26776, Anchor QEA is seeking a new permit that would authorize them to take juvenile PS Chinook salmon and PS steelhead in order to conduct stream typing and evaluate culverts as potential barriers to fish passage in support of Pierce County. This work would be conducted in locations across Pierce County, Washington.

Juvenile PS Chinook salmon and steelhead would be collected via hand or dip netting and backpack electrofishing. Captured fish would be handled (weighed, measured, and checked for marks or tags) prior to release. In some cases, the researchers may not actually capture any fish but would merely note their presence, however electrofishing where listed species are observed would still be reported as take. The researchers will only deploy electrofishing if attempts to visually observe and identify fish from the bank and to sample fish by dip nets are unsuccessful. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this work is to confirm the upper extent of fish presence in potentially fish-bearing streams, and support the prioritization of fish passage structures to establish access to suitable habitat in the upstream extent of fish-bearing habitat. This work is expected to benefit ESA-listed species by informing the planning of restoration and enhancement efforts to improve salmonid habitat, and salmonid access upstream of anthropogenic barriers in Pierce County.

Under permit 27091-2M, the Port of Seattle is seeking to modify a permit that would authorize them to take additional juvenile PS Chinook salmon and PS steelhead in order to assess juvenile salmonid habitat use and the presence of key invertebrate prey resources in the Lower Duwamish Waterway T-117 restoration site. This work would be conducted solely within the Lower Duwamish River in King County, Washington.

Juveniles would be collected via fyke net. Juvenile salmon and steelhead would be anesthetized, tissue sampled and PIT-tagged prior to release. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this project is to characterize salmonid use of the restoration site during individual tidal cycles and monitor the physical and biological characteristics of the site to measure whether the restoration project is meeting its stated objectives. The restoration of the T-117 site is expected to benefit PS Chinook salmon and steelhead by increasing the area and functional value of riparian, estuarine marsh, exposed intertidal substrate, and shallow subtidal habitats used by salmonids, and this monitoring work will increase the likelihood the restoration will be managed to provide the expected habitat benefits.

Under permit 27824, the USGS is seeking a new permit that would authorize them to take juvenile SacR winter-run Chinook salmon in order to conduct egg incubation studies and mark-recapture monitoring programs to address juvenile production of winter-run Chinook salmon. This work will be conducted in Battle Creek and the Sacramento River below Shasta Dam, in the California Central Valley.

Juveniles would be collected via screw traps, and captured juveniles would be anesthetized, tissue sampled and PIT-tagged prior to release. Released juveniles may be recaptured using beach seines or backpack electrofishing, and handled (weighed, measured, checked for marks and tags) prior to release. Fertilized eggs from Livingston Stone National Fish Hatchery would be placed in egg boxes and set in designated redd locations along the Sacramento River. The egg boxes would be enclosed in mesh and visually observed from fertilization through emergence, and surviving alevins or fry will be released into the Sacramento River. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this project is to estimate tributary-level survival, somatic growth, and movement patterns of Chinook salmon, focusing on winter-run eggs and juveniles. These studies will help characterize influences of environmental conditions on salmon productivity, and are expected to benefit SacR winter-run Chinook salmon by addressing important data gaps for managers and informing habitat restoration efforts.

Under permit 28055 the Gold Ridge Resource Conservation District (GRCD) is seeking a new permit that would authorize them to take juvenile and adult CC Chinook salmon, CCC coho salmon, and CCC steelhead in order to document the status and trends of salmonid populations in watersheds of the Sonoma Coast. This work will be conducted in the Bodega Bay and Russian River basins in coastal California.

Juveniles would be collected via backpack electrofishing, hook and line angling, hand or dip net, beach seine, minnow trap, and funnel or pipe trap. Juvenile fish would be captured, handled (anesthetized, weighed, measured, and checked for marks or tags), and released. A subsample of captured juveniles would also be tissue sampled and PIT-tagged prior to release. Adults are not being targeted during this work, but some may be unintentionally collected via funnel or pipe trap or encountered during electrofishing. Captured adults would be handled (weighed, measured, and checked for marks or tags), and released. Spawned adults or post-spawn carcasses would be enumerated via spawning surveys, and tissues may be collected from carcasses encountered during spawning surveys. Adult and juvenile fish would be observed during snorkel surveys. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The goals of the restoration projects conducted by the GRCD are collectively to improve watershed health and resiliency for the benefit of salmonids, and these studies are intended to improve understanding of restoration needs by addressing information gaps about the current status of salmonid species in the targeted watersheds. This work is expected to benefit ESA-listed salmon and steelhead by providing information on the status and trends of their populations, and their contributions to broader ESUs, which can be used to better inform ESA-listed species management and restoration efforts.

Under permit 28158 the Northwest Straits Foundation is seeking a new permit that would authorize them to take juvenile PS Chinook salmon and PS steelhead and adult southern DPS eulachon in order to evaluate the impact of shoreline armoring removal, beach nourishment, vegetation enhancement and toxic cleanup restoration efforts on nearshore fish habitat use. This work would take place in Bowman Bay, Cornet Bay, and Fidalgo Bay in Skagit County and Island County in the state of Washington.

Juvenile salmon and steelhead and adult eulachon would be collected via beach seining. Fish would be captured, handled (identified, weighed, measured, and checked for marks or tags), and released. The researchers are not proposing to kill any of the listed fish being captured, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of the restoration projects managed by the Northwest Straits Foundation is to restore and enhance habitat for nearshore wildlife, including migrating salmon and their prey species. These restoration efforts are expected to benefit rearing PS Chinook and steelhead, and this pre- and post-construction monitoring work will increase the likelihood the restoration projects will be designed and managed to provide the expected habitat benefits.

Under permit 28199 the California State Polytechnic University Humboldt (Cal Poly Humboldt) is seeking a new permit that would authorize them to take adult SONCC coho salmon, NC steelhead, CC Chinook salmon, and SDPS green sturgeon in order to assess the presence, distribution, migration, habitat preferences, and movement patterns of sub-adult and adult green sturgeon. This work would take place in Humboldt Bay, Arcata Bay, Mad River Slough and Mad River Estuary in Humboldt and Del Norte Counties, in California.

Adults of all fish species would be collected via hook and line angling. This study is not targeting salmon or steelhead, so any CCC coho salmon, CC Chinook salmon, or NC steelhead captured would be immediately released. Captured adult green sturgeon would be handled (weighed, measured, and checked for marks or tags), tissue sampled and tagged with pop-up satellite archival tags prior to release. Adults would also be visually observed through vessel surveys and aerial surveys, including the use of cameras attached to aerial drones. The researchers are not proposing to kill any of the listed fish being captured, and do not anticipate any will be killed as an inadvertent result of these activities.

The purpose of this study is to assess the presence, distribution, and migration patterns of sub-adult and adult SDPS green sturgeon in Humboldt and Del Norte County, describe the habitat preferences, identify potential congregation sites, and evaluate individual movement patterns and their correlation with environmental variables. This work is expected to benefit ESA-listed SDPS green sturgeon by addressing current data gaps about distribution and habitat use, providing managers information necessary to evaluate how the species may be affected by future actions that would impact these bay and estuary habitats.

Under permit 28292, the City of Portland is seeking a permit that would authorize them to take adult LCR Chinook salmon, LCR coho salmon, LCR steelhead, UWR Chinook salmon, and UWR steelhead while conducting a study to determine the levels of contamination in resident fish tissue and to continue documenting how tissue contamination levels are changing over the long term in the Columbia Slough. This work will be conducted within the lower Willamette River in Multnomah County, Oregon.

Juveniles and adults may be collected via boat electrofishing, and would be captured, handled, and released. ESA-listed fish are not being targeted for this study, but some may be unintentionally captured while targeting resident fish. In some cases, the researchers may not actually capture any fish but would merely note their presence, however electrofishing where listed species are observed would still be reported as take. The researchers are not proposing to kill any listed fish, but a small number of fish may be killed as an inadvertent result of these activities.

The purpose of this work is to assess whether or not upland source control actions are reducing toxic loads in fish tissue over time. This study is expected to benefit ESA-listed salmon and steelhead by providing data that will guide programmatic and risk management decisions in contaminated urban waterways and thereby reduce contaminant exposure and uptake in resident and migrating fish in the lower Willamette River over time.

This notice is provided pursuant to section 10(c) of the ESA. NMFS will evaluate the applications, associated documents, and comments submitted to determine whether the applications meet the requirements of section 10(a) of the ESA and Federal regulations. The final permit decisions will not be made until after the end of the 30-day comment period. NMFS will publish notice of its final action in the Federal Register .

Dated: August 1, 2024.

Angela Somma,

Chief, Endangered Species Division, Office of Protected Resources, National Marine Fisheries Service.

[ FR Doc. 2024-17410 Filed 8-7-24; 8:45 am]

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