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Species Recovery in the United States:Increasing the Effectiveness of the

Endangered Species ActDaniel M. Evans, Judy P. Che-Castaldo, Deborah Crouse, Frank W. Davis, Rebecca Epanchin-Niell,

Curtis H. Flather, R. Kipp Frohlich, Dale D. Goble, Ya-Wei Li, Timothy D. Male,Lawrence L. Master, Matthew P. Moskwik, Maile C. Neel, Barry R. Noon,Camille Parmesan, Mark W. Schwartz, J. Michael Scott, Byron K. Williams

Winter 2016 Report Number 20

Issues in EcologyIssues in Ecology

Species Recovery in the United States:Increasing the Effectiveness of the

Endangered Species Act

© The Ecological Society of America • [email protected] esa 1

ISSUES IN ECOLOGY NUMBER TWENTY WINTER 2016

Species Recovery in the United States: Increasing theEffectiveness of the Endangered Species Act

Daniel M. Evans, Judy P. Che-Castaldo, Deborah Crouse, Frank W. Davis, Rebecca Epanchin-Niell, Curtis H. Flather,R. Kipp Frohlich, Dale D. Goble, Ya-Wei Li, Timothy D. Male, Lawrence L. Master, Matthew P. Moskwik,

Maile C. Neel, Barry R. Noon, Camille Parmesan, Mark W. Schwartz, J. Michael Scott, and Byron K. Williams

SUMMARY

The Endangered Species Act (ESA) has succeeded in shielding hundreds of species from extinction andimproving species recovery over time. However, recovery for most species officially protected by the ESA –

i.e., listed species—has been harder to achieve than initially envisioned. Threats to species are persistent and per-vasive, funding has been insufficient, the distribution of money among listed species is highly uneven, and at least10 times more species than are actually listed probably qualify for listing. Moreover, many listed species will requireongoing management for the foreseeable future to protect them from persistent threats. Climate change will exac-erbate this problem and increase both species risk and management uncertainty, requiring more intensive and con-troversial management strategies to prevent species from going extinct.

In this Issue, we provide an overview of the ESA, summarize the causes and patterns of species endangerment inthe United States, identify key successes and shortcomings of recovery programs, and discuss the following sixbroad strategies to increase the effectiveness of ESA implementation:

1. Establish and consistently apply a system for prioritizing recovery funding to maximize strategicoutcomes for listed species.

2. Strengthen partnerships for species recovery by expanding collaboration among federal agencies,the states, and nongovernmental organizations and by developing incentives for private landowners.

3. Promote more monitoring and adaptive management for species recovery. Conduct targeted,efficient monitoring programs to assess species status and improve management strategies, and useadaptive management to deal with ecological complexity and uncertainty.

4. Refine methods to develop more objective, measurable recovery criteria based on the best availablescience.

5. Use well-established climate-smart conservation strategies such as increasing habitat connectivityand reducing nonclimate stressors; evaluate and consider using innovative climate adaptationstrategies, including protecting potential future habitats, assisted colonization, and engineeringnew habitats.

6. Evaluate ecosystem-based approaches such as surrogate species and coarse ecological filters todevelop methods that increase the efficiency of managing for recovery.

Cover photos: Clockwise starting on the left: a) Haleakala– silversword b) Desert tortoise c) Schaus' swallowtail butterfly d) Bald eagle.

Photos credits: a) Forest and Kim Starr, via Flickr b) Robb Hannawacker, National Park Service c) Mary Truglio, Florida Fish and Wildlife Conservation Commissiond) Larry Master.

© The Ecological Society of America • [email protected] esa

“For one species to mourn the death ofanother is a new thing under the sun,” wroteAldo Leopold in A Sand County Almanac.Leopold deplored the loss of the passengerpigeon, gray wolf, grizzly bear, bison, andprairie flower as a waste of America’s wildlandheritage and a failure to observe the first prin-ciple of “intelligent tinkering”—namely, “tokeep every cog and wheel.” By the turn of the20th century, market hunting and habitat loss,mainly to farmland, threatened countlessspecies across the United States. Early conser-vationists such as George Bird Grinnell helpedawaken a national awareness of—and outcryagainst—threats to America’s wildlife.

EMERGENCE OF THE ENDANGEREDSPECIES ACT

Leopold, Grinnell, and others looked to thestates for wildlife protection, in accordancewith traditions going back to medieval laws,which gave feudal lords ownership rights overgame in their domains. On royal lands, theking appointed stewards who were responsiblefor maintaining deer, elk, boar, and other gamein trust for the king. In the United States, thenotion of royal trusteeship for game evolvedinto a public trust doctrine giving states thepower to manage wildlife in the public interest.

The states traditionally relied on public trustdoctrine to manage game species while largelyignoring nongame species. The steady loss ofboth led conservationists to turn increasinglyto the federal government for help. Inresponse, Congress passed a series of laws toprotect wildlife, beginning with the Lacey Actof 1900, which regulated commercial animalmarkets. Other laws regulating the trade inanimals and animal products followed, such asthe Migratory Bird Treaty Act of 1918.

The Migratory Bird Conservation Act of

1929 further authorized the federal governmentto acquire habitat for conservation purposes, buthabitat protection was constrained until theenactment of the Land and Water ConservationFund Act of 1965, which provided funds toacquire habitat for fish and wildlife. TheEndangered Species Preservation Act of 1966authorized the listing of endangered species anda modest program to acquire additional habitat.In the years that followed, Congress continuedto refine the law, with more comprehensive pro-tections for endangered species and their habi-tats, culminating in the Endangered Species Act(ESA) of 1973—arguably the strongest piece ofenvironmental legislation in history.

THE NEED FOR NEWSTRATEGIES

The federal government and its conservationpartners have now implemented the ESA formore than 40 years. They have had many suc-cesses, but the ESA has only partly fulfilled itsconservation promise.

Critics point out that recovery efforts arefocused disproportionately on charismaticspecies, to the detriment of others, particularlyplants. Moreover, less than 2 percent of allspecies that have ever been listed (formally pro-tected by the ESA as endangered or threatened)have recovered to the point where they quali-fied for delisting. Private landowners and busi-nesses complain of infringements on propertyrights, which can yield perverse consequencessuch as efforts to discourage or eliminate listedspecies from private lands, sometimes describedas “shoot, shovel, and shut up.”

The ESA’s defenders point to success storiessuch as the bald eagle, which went from 417nesting pairs in 1963 to more than 11,000 in2007. Other successes include such hallmarksof America’s wildlife heritage as the gray wolf,whooping crane, peregrine falcon, grizzly bear,and gray whale. In fact, scientists estimate thatthe ESA has directly prevented the extinctionof more than 200 species, and the longer a

Species Recovery in the United States: Increasing theEffectiveness of the Endangered Species Act

Daniel M. Evans, Judy P. Che-Castaldo, Deborah Crouse, Frank W. Davis, Rebecca Epanchin-Niell, Curtis H. Flather,R. Kipp Frohlich, Dale D. Goble, Ya-Wei Li, Timothy D. Male, Lawrence L. Master, Matthew P. Moskwik,

Maile C. Neel, Barry R. Noon, Camille Parmesan, Mark W. Schwartz, J. Michael Scott, and Byron K. Williams


A NATIONAL COMMITMENTTO NATIVE SPECIES



species is protected by the act, the more likelyit is to increase in abundance and geographicdistribution. Recovery takes time, and mostspecies protected by the ESA have not beenprotected long enough to fully recover. Aftermore than 40 years, the ESA remains essentialto protecting species in the United States.

However, the ESA has not kept pace withrapid socioeconomic changes in the UnitedStates and advances in conservation science.Since 1973, the US population has grown bymore than 50%, and gross domestic producthas expanded from approximately $1.4 trillionto more than $16 trillion, resulting in multiplestressors to vulnerable species. At the sametime, conservation biology has developed fromits infancy into a sophisticated science. Today,scientists have much better data on the con-servation status of species and the threats theyface. They also have a better understanding ofthe monitoring and management needed toachieve and sustain species recovery.Although interpretation of the ESA continuesto evolve via litigation in US courts, the actitself has remained fairly static. Fortunately,the ESA has proved flexible in its implemen-tation, and there are many good options forincreasing its effectiveness. In this paper, wediscuss six key areas in which implementationcould be improved to further species recovery.

Before discussing strategies to increase theESA’s effectiveness, we will provide anoverview of the ESA and its implementation,discuss procedures and methods for determin-ing whether species are endangered or threat-ened, outline where endangered and threat-ened species occur across the United States,and describe the greatest threats causingspecies to decline.

ESA OVERVIEW

Recovery of species that are endangered orthreatened with extinction is a central goal ofthe ESA. The act instructs federal agencies topromote the recovery of listed species using“all methods and procedures which are neces-sary” to increase species abundance and con-serve their habitats until “the measures pro-vided pursuant to this Act are no longernecessary” (ESA sec. 3(3)). Recovery meansthat listed species no longer need the act’s pro-

tection (ESA secs. 4(f)(1), 4(g)(1)).The ESA describes the path to recovery as a

linear process: • The federal agencies that administer the

act—the U.S. Fish and Wildlife Service(FWS) in the U.S. Department of theInterior and the National Oceanic andAtmospheric Administration’s NationalMarine Fisheries Service (NMFS) in theU.S. Department of Commerce (togetherknown as the Services)—identify and assessthe threats to a species to determinewhether it is endangered or threatened.FWS has jurisdiction over terrestrial speciesand freshwater fishes; NMFS has jurisdic-tion over marine species and anadromousfishes.

• If the species is endangered or threatened,FWS or NMFS adds the species to an offi-cial list of endangered and threatenedspecies (Figure 1).

• Listing triggers two overlapping types ofconservation measures: extinction preven-tion and recovery actions.

• A tailored mix of conservation measures miti-gates the threats that the species faces and,where necessary and appropriate, restores andenhances habitat and populations.

• The Services delist a species and consider itrecovered when its abundance and geo-graphic distribution is sufficient to sustainsecure populations for the long term in thewild and the threats have sufficientlyabated. After delisting, the species thriveson its own or under other regulatory protec-

Figure 1. Endangered andthreatened species listings byyear for all U.S. states andterritories. Listings include allspecies, subspecies, anddistinct population segments ofa species, minus delistings dueto extinction, recovery, or newinformation not available at thetime of listing. Listed at the endof 2013 were 93 birds, 152fishes, 89 mammals, 29amphibians, 37 reptiles, 240invertebrates, and 871 plantsand lichens.

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SPECIES STATUS ANDTHREATS


tions. For example, after the bald eagle wasdelisted, it was still protected by the Baldand Golden Eagle Protection Act.

Listing Species

When evaluating a species for listing, theServices consider a host of factors but givespecial emphasis to (a) the actual or threat-ened destruction, modification, or curtailmentof its habitat or range; (b) overutilization ofthe species for commercial, recreational, sci-entific, or educational purposes; (c) disease orpredation; (d) the adequacy of existing regula-tory protections; and (e) any other “natural ormanmade factors that threaten its continuedexistence,” such as small population sizes orthreats due to climate change (ESA sec.4(a)(1)).

According to the ESA, a species should belisted as “endangered” if it is “in danger ofextinction throughout all or a significant por-tion of its range” (ESA sec. 3(6)) and as“threatened” if it is “likely to become anendangered species within the foreseeablefuture throughout all or a significant portionof its range” (ESA sec. 3(20)). These terms arevague and clearly open to interpretation, butthe crucial distinction is time (see Box 1). Anendangered species is in danger of extinctionnow, a threatened species in the foreseeablefuture.

The ESA requires the Services to base list-ing decisions “solely on the best scientific andcommercial data available” (ESA sec.4(b)(1)(A)). However, any decision to list aspecies also requires a policy judgment regard-ing how much risk to that species is accept-

able. Science can inform the decision bydetermining the degree of risk a species faces,but science alone cannot determine whetherthe risk is acceptable. Similarly, judgmentsabout how much risk a species faces in theforeseeable future, while necessarily supportedby science, can be influenced by social andpolitical considerations. Stakeholders withdivergent views about acceptable levels ofextinction risk frequently mount legal chal-lenges over whether species need to be listed,whether they are endangered or threatened,how much habitat represents a “significantportion” of a species’ range, and other key ele-ments of ESA implementation. Accordingly,interpretation of the ESA continues to evolve,one court case at a time.

Implementing ConservationMeasures

Listing a species triggers ESA provisionsintended to mitigate threats, stop the slidetoward extinction, and improve the species’conservation status. The corresponding con-servation measures are of two overlappingtypes: extinction prevention and recoveryactions.

Extinction Prevention

The ESA is often likened to an emergencyroom, with requirements intended to preventor slow a species’ continued decline. Onerequirement is consultation. Any federalagency that proposes an action (includingfunding or permitting activities on privatelands) that might affect a listed species must


Box 1. The Polar Bear Memo: Distinguishing between “Endangered” and “Threatened”

In 2010, FWS published a memo clarifying its decision to list thepolar bear as threatened rather than endangered. The agencynoted that climate change is diminishing the sea ice that the polarbear depends on, threatening it with extinction throughout all or asignificant portion of its range in the foreseeable future. However,FWS judged that the bear was not yet on the brink of extinction.

FWS defined “foreseeable future” as “[t]he timeframe overwhich the best available scientific data allows us to reliablyassess the effect of threats on the species.” In determining thattimeframe, the agency focused on projections of sea ice loss andthe timespan covered by several generations of polar bears (“theoptimal timeframe” for assessing the species’ “response to pop-ulation level threats”). Both timespans fell within 40 to 50 years,for an average “foreseeable future” of 45 years. The agency listedthe polar bear as threatened because it was likely to become indanger of extinction within 45 years and no regulatory mecha-nisms were in place to effectively address the threat.

Polar bear and cubs.Photo credit: Larry Master.



consult with FWS or NMFS to “insure” thatthe proposed action “is not likely to jeopar-dize the continued existence” of the speciesor “result in the destruction or adverse modi-fication” of its critical habitat (ESA sec.7(a)(2)).

Another provision prohibits any “person”(including government and business entities(ESA sec. 3(12)) from “taking” endangeredanimals. The ESA’s definition of “taking”includes harassing or harming species as wellas selling the species or their parts (ESA secs.3(19), 9(a)(1)). By regulation, FWS hasextended the prohibition against taking to allthreatened animals unless it adopts alternativetake regulations for a particular species. Theprohibition against taking does not apply toendangered plants, which are protected princi-pally from removal on federal lands or destruc-tion in knowing violation of state law.

Most federal actions that result in a take donot “jeopardize the continued existence” of alisted species. For these actions, consultationswith the Services include an “incidental takestatement,” which estimates the expected takeof the listed species; federal actions that con-form to the statement may proceed. Similarly,nonfederal entities can receive an “incidentaltake permit” if they develop and agree toimplement a habitat conservation plan (ESAsec. 10(a)). Before issuing an incidental takepermit, the Services must determine that thetaking “will not appreciably reduce the likeli-hood of the survival and recovery of thespecies in the wild” (ESA sec.10(a)(2)(B)(iv)). Although incidental takestatements and permits include some safe-guards for listed species, they often allow forcontinued population reduction and habitatdegradation.

Recovery Actions

Listing also triggers affirmative recoveryactions, such as mandatory recovery plans cre-ated by the Services “for the conservation andsurvival of [listed] species” (ESA sec. 4(f)).Recovery plans are essential documents forguiding future recovery activities. However,the ESA gives few guidelines for their prepara-tion and content and does not specify a dead-line for how soon after listing the Servicesmust complete recovery plans. Funding limitsand low priority for some species can cause sig-nificant delays. The Services are also required,with narrowly defined exceptions, to designatecritical habitat (ESA sec. 4(a)(3)). Similarly,

the ESA requires all federal agencies to imple-ment “programs for the conservation of [listed]species” (ESA sec. 7(a)(1)), although judicialinterpretation has given agencies discretion incarrying out this provision.

Other recovery actions are explicitly discre-tionary, such as deciding which actions to taketo alleviate threats, protect habitats, and aug-ment populations. The Services, for example,can translocate a species as an experimentalpopulation under the agencies’ “conservation”authority (ESA secs. 10(j), 3(3), 7(a)(2)).Similarly, the Services can issue permits foractivities that “enhance the ... survival of theaffected species” (ESA sec 10(a)(1)(A)).Finally, the Services can use “activities associ-ated with scientific resources managementsuch as research, census, law enforcement,habitat acquisition and maintenance, propaga-tion, live trapping, and transplantation” (ESAsec. 3(3)).

Delisting a Recovered Species

The Services can delist a recovered speciesafter meeting the same procedural require-ments for listing. They must evaluate thespecies’ status in relation to the threats itfaces, including habitat loss, overutiliza-tion, disease or predation, inadequate regu-latory mechanisms, and any other naturalor manmade factors affecting its continuedexistence.

The Services have considerable leeway indeciding when a species has recovered. Forexample, the ESA does not require theServices to base delisting decisions onrecovery criteria given in recovery plans,and a 2012 court case upheld that recoverycriteria are not legally binding. Althoughthe Services agree with this view, somestakeholders contend that it creates falseexpectations and inconsistencies in delist-ing decisions. In addition, because the ESArequires the Services to make delistingdecisions based on the best scientific dataavailable (ESA sec. 4(b)(1)(A)), theirmethods for evaluating recovery statushave changed as scientific methods haveevolved. The Services sometimes use popu-lation viability analysis, a quantitativeassessment of the probability of extinctionbased on several often-interacting factors,including demographic, environmental,and genetic mechanisms. More recently,the Services have begun to assess speciesaccording to the “3Rs”—the resiliency,



the Pacific Northwest, for example, severaltreaties guarantee tribes the right to fish in“usual and accustomed places,” making thetribes comanagers of many of the region’simperiled salmon.

SPECIES STATUS ASSESSMENTSAND THE POTENTIAL FOR NEWLISTINGS

Nongovernmental scientific organizations alsoassess species and rank them according totheir extinction risk. By far the most compre-hensive list for the United States is main-tained by the nonprofit organizationNatureServe and its Natural HeritageNetwork, which tracks more than 28,000species and 9,000 subspecies and other nar-rowly defined taxonomic groups in all 50states and Puerto Rico. NatureServe evaluatesspecies status in terms of three primary fac-tors—rarity (i.e., relative abundance); threats(including their scope, severity, and immedi-acy); and trends (in population numbers, areaof occupancy, and range size). NatureServeweights the three factors according to astrictly applied set of rules, making its speciesstatus rankings consistent and repeatable.NatureServe’s species rankings also correspondclosely to similar assessments made by otherorganizations, including the InternationalUnion for Conservation of Nature (IUCN)Red List rankings and American FisheriesSociety rankings for aquatic species. Andthere is good concordance with listings underthe ESA: approximately 90 percent of cur-rently listed species are also considered imper-iled by NatureServe. However, among themore than 28,000 U.S. species thatNatureServe tracks, only about 20 percent ofimperiled species (as ranked by NatureServe)are listed. The correspondence is good forbirds, mammals, and reptiles, but the discrep-ancy is huge for most other taxa, includingamphibians, fishes, invertebrates, and vascularplants (Figure 2). Taken together, these assess-ments suggest that there are many morespecies that probably should be listed underthe ESA but are not currently listed.

Other assessments suggest that there is aneven wider gap in the number of species thatlikely need protection under the ESA. Thespecies assessed by NatureServe represent onlyabout 19 percent of the plants, animals, andfungi described in the United States. Theother 81 percent, mostly invertebrates, aregenerally too poorly known to determine their

redundancy, and representation of popula-tions (see Box 2).

The Services currently define recovery interms of sustaining secure populations of aspecies for the long term in the wild and abat-ing threats. The size, number, and geographicdistribution of populations must be largeenough for the risk of extinction due to peri-odic threats such as drought or disease to bereasonably low, and regulatory or other conser-vation mechanisms must provide reasonableassurance that the species will not be placed atrisk again.

Although the Services have the ultimatelegal responsibility for listed species, state gov-ernments, tribal nations, nongovernmentalorganizations, academic researchers, and pri-vate landowners and businesses are all essen-tial partners for species recovery. For example,the ESA requires the Secretary of the Interiorto “cooperate to the maximum extent practi-cable with the states,” including consultationbefore acquiring lands or waters “for the pur-pose of conserving any endangered species orthreatened species” (ESA sec. 6(a)). In addi-tion, treaties with American Indian tribes fre-quently grant them management authorityover endangered and threatened species. In

Amphibians

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Figure 2. The number of specieslisted under the ESA compared

with the number thatNatureServe ranks as imperiled

(as of the end of 2013).

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Box 2. The “3Rs” of Species Recovery

The 3R framework is a science-based approach that the Services currently useto help develop recovery criteria.

Resiliency: Local populations of a species are large enough, have sufficientgenetic variation, and are sufficiently mixed with respect to the age and sex ofindividuals to persist in the face of periodic threats such as drought, wildfire, anddisease.

Redundancy: There are enough separate populations of a species to provide amargin of safety in case catastrophic events eliminate some populations.

Representation: There is sufficient genetic variation among populations of aspecies to conserve the breadth of the species’ genetic makeup and its capacityto evolve and adapt to new environmental conditions.



conservation status. However, based on thenumber of described species, scientists esti-mate that the total number of known speciesat risk of extinction in the United States is atleast 10 times the number of domestic specieslisted under the ESA.

GEOGRAPHY OF LISTED ANDIMPERILED SPECIES

The geographic distribution of U.S. listedspecies and imperiled species (as ranked byNatureServe) is far from uniform. Instead,there is considerable overlap among thesespecies, many of which are concentrated inregional “hotspots.”

Hotspots of Listed Species

We used contemporary species occurrencerecords maintained by NatureServe and itsnetwork of natural heritage programs to evalu-ate the geographic distribution of listedspecies. We found hotspots in Hawaii, in thesouthern Appalachian Mountains, in peninsu-lar Florida, in coastal parts of the Southeastand eastern Gulf states, in CaliforniaMediterranean-climate regions, and in theCascade and lowland mixed forests of thePacific Northwest (Figure 3a). Since the late1990s, scientists have consistently recognizedthese hotspots, despite variation in analyticalmethods and a substantial increase in thenumber of listed species (Figure 1). However,we also identified a new, emerging area oflisted-species concentration associated withthe interior highlands and plateau region ofsouthern Missouri, northern Arkansas, west-ern Kentucky, and southern Illinois andIndiana (Figure 3a). Many regions outside ofthese hotspots contain very few listed species.Overall, 54 percent of the U.S. land area has

no listed species in NatureServe’s databases.The taxonomic composition of listed species

varies among hotspots. Since 1994, plantshave outnumbered animal species listed, andlisted plants are concentrated in areas withhigh levels of endemic species—species thatoccur nowhere else—including Hawaii, theMediterranean climates of California, and theFlorida inland scrub. Invertebrates are a largepart of the listed biota in some regions—insects in Hawaii and California and mollusksin the Southern Appalachians and interiorhighlands. Birds make up many of the listedspecies in Hawaii, peninsular Florida, and thesoutheastern Atlantic coast. Mammals arewell represented in the arid Southwest, the drysteppe of the California Central Valley, theSouthern Appalachians, and the interior high-lands of the East. Amphibians and reptileshave fewer listed species than other verte-brates; the ones listed tend to be in the aridSouthwest, California, and peninsular Florida.More species of fish receive ESA protectionsthan any other vertebrate group, and listedfishes tend to concentrate in the aridSouthwest, Pacific Northwest, and SouthernAppalachians.

Figure 3. Geographicdistribution of (a) listed species;(b) species involved in thesettlement agreement; and (c)species that NatureServe ranksas imperiled but are not on mapa or map b.

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Emerging Hotspots?

Following a legal settlement agreement,FWS is committed to processing a largebacklog of species for listing determinationsby 2018. Species that are likely to be addedto the list are concentrated in existinghotspots (such as the SouthernAppalachians) and some new areas (such asthe southern Great Basin and the Ouachitaand Boston Mountains of western Arkansasand eastern Oklahoma) (Figure 3b).

Figure 3c reflects likely proposed new listingsin the longer term, including species thatNatureServe currently considers imperiled butare not listed under ESA or proposed for list-ing. Accordingly, the southwestern Basin andRange (southern Arizona and New Mexicoand West Texas) and a portion of the ColoradoPlateau (southeastern Utah) are likely toemerge as new hotspots of listed species.

PRIMARY THREATS TO LISTEDSPECIES

Based on descriptions in species’ recoveryplans, the greatest threats to listed species(see Figure 4) are habitat loss and degrada-tion due to factors such as land use conver-sion for agriculture and development, miningactivities, and changes to natural fireregimes. The next most common threats arecompetition with and predation by other

species, especially invasive exotics. Pollutionis also a major threat, especially to fishes andfreshwater mollusks, and transient humandisturbances such as off-road vehicle use andtrampling threaten both animals and plants.Other threats include overharvesting, over-hunting, and natural disasters. Climatechange almost certainly threatens morespecies than recovery plans indicate. As ofJanuary 2010 (the most recent data we usedfor this analysis), climate change was listed asa threat in only 26 recovery plans for animalsand in none for plants. Since 2010, theServices have identified climate change as athreat more often.

Our analysis is consistent with earlierreviews but also shows a higher percentage oflisted species threatened by invasive and otherproblem species and by overharvesting andoverhunting. In addition, many recovery planscite small population sizes and small numbersof populations as demographic threats that cancompound the effects of extrinsic threats suchas habitat loss, invasive species, and cata-strophic events like natural disasters. Further,scientists are increasingly recognizing thatmany listed species are threatened by the lossof other species—such as pollinators, seed dis-persers, decomposers, and keystone preda-tors—that have critical roles in maintainingecosystem processes.

Here we describe historical status trends forlisted species, discuss several factors that cor-relate with these trends, and highlight mod-ern challenges to managing species forrecovery.

HISTORICAL TRENDS

The only source of regularly generated gov-ernment data on the progress of listedspecies toward recovery over time has beenbiennial reports that the Services have sub-mitted to Congress. These reports have pro-vided a 2-year status update on eachspecies, identifying whether listed specieswere presumed extinct, declining, stable, orimproving—or whether their status wasunknown. The reports have not alwaysbeen rigorously verified, but they are oftenthe best information available. Based onreports from 1990 through 2010 (the most

Figure 4. Primary threats to1,421 species, subspecies, and

distinct population segmentslisted under the ESA (621 animaland 800 plant listing units). Data

reflect threats identified inrecovery plans for all species

that had recovery plansapproved as of January 2010

(for 528 animals and 645 plants)and threats identified by

NatureServe (for the remainder).

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RECOVERY TRENDS ANDMODERN CHALLENGES



recent year for which the reports are avail-able), we found that 35 percent of all listedspecies had stable status trends and that 8percent were improving (Figure 5).However, declining taxa (52 percent) faroutnumbered improving ones. Three per-cent of species were presumed extinct, butat least half of these species were probablyalready extinct when they were listed.

In 2012, the Services stopped reporting 2-year status trends. Instead, their biennialreports to Congress will now summarizewhether species have been recommended forreclassification or delisting as part of a morecomprehensive 5-year status review.Furthermore, the Services have begun pro-ducing 5-year reports for many more species,providing more detailed information aboutthe status of and threats to species as well asactions to conserve them. More than 850species have been reviewed since 2009, andFWS has recommended that 37 of these bedelisted or reclassified from endangered tothreatened.

Large gaps remain in scientific knowledgeof the status of listed species, their popula-tion trends, and their life histories.Monitoring programs that track speciesresponses to recovery investments exist foronly a handful of species. Nonetheless, somefactors are correlated: species with recoveryplans are more likely to improve, and thelonger a species is listed, the more likely itsabundance is to increase, although there isconsiderable variation among taxonomicgroups.

Some studies conclude that designatingcritical habitat also helps promote speciesrecovery, but other studies that addressconfounding factors show no correlation.Because critical habitat restrictions applyonly to the activities of federal agencies(under the ESA’s section 7 prohibition offederal actions that “result in the destruc-tion or adverse modification of criticalhabitat”) and because all federal agenciesare also restricted from actions that “take”or “jeopardize the continued existence” oflisted species, some have argued that desig-nating critical habitat is superfluous.Others maintain that protecting criticalhabitat effectively addresses the primarythreat to listed species. In practice, theServices often exempt habitat degradationfrom regulation. As a result, designatingcritical habitat has had limited regulatoryeffect.

GOVERNMENT FUNDING ISSUES

The amount of government funding availablefor species protection and recovery is one ofthe best predictors of recovery success. Butgovernment spending has long been insuffi-cient and highly disproportionate amonggroups of species.

Insufficient Spending

From 1998 to 2012, total state and federalspending on endangered and threatenedspecies (adjusted for inflation to equal 2013dollars) rose from $547 million to just over$1.364 billion per year. Most spending (79percent in the average year) came from federalsources other than FWS, including NMFS andthe U.S. Department of Defense. Spending byFWS, as provided by Congress, representedjust 13.1 percent of total funding, and spend-ing by the states represented another 8 per-cent. Although state expenditures did not riseappreciably from 1998 to 2012, average FWSexpenditures doubled from $77 million to$156 million per year. Other federal spendingincreased more, from $446 million to $1.164billion per year.

However, much of this spending does not godirectly to on-the-ground species recoveryactions but rather to pay staff and fund activitiesrelated to law enforcement, listings, and consul-tations (such as negotiating mitigation andextinction prevention actions). Nonetheless,even if total government spending on listedspecies over the past 15 years had been strictlyapplied to recovery actions, it still would havelagged far behind the needs stated in the recov-

Improving8%

Presumedextinct

3%

Unknown2%

Stable35%

Declining52%

Figure 5. Trends in recoverystatus for 1,292 listed species,based on a summation of trendsreported in 2-year statusupdates submitted by theServices to Congress from 1990to 2010.



ery plans. Researchers have estimated that totalspending over the past 15 years has covered onlyabout a third of species’ recovery needs.

Disproportionate Spending

Funding for endangered and threatenedspecies is not only insufficient but also highlydisproportionate among taxonomic groups.From 1998 to 2012, over 80 percent of all gov-ernment spending went to support 5 percentof all listed species, whereas 80 percent of alllisted species shared less than 5 percent of allfunds. Most federal spending has gone to just15 fishes: 7 salmonid and 8 sturgeon species.In fact, the 46 species managed by NMFSalone or by NMFS and FWS together—including salmon, sturgeon, seals, andwhales—receive far more funding than otherspecies. From 1998 to 2012, the medianannual expenditure (adjusted for inflation) onsuch species was $1.8 million, including over$197 million per year for Chinook salmon. Incontrast, the median annual inflation-adjustedexpenditure for the species managed solely byFWS was $2,686, ranging from less than $200per year for the seven least-funded species to

$2 million per year for bull trout. Thesespending patterns are well illustrated by 2012expenditures, with 165 listed fishes receiving61.5% of total funds and 778 listed plants andlichens receiving just 3.3% (Figure 6).

In part, disproportionate spending on listedspecies has been a result of congressional ear-marks that limit the Services’ abilities to dis-tribute funds more equitably, and it also reflectsdifferent species’ needs. However, the degree towhich funding is skewed appears to far exceedreasonable expectations for what is required.For example, 7 out of 167 taxa with species-specific reported recovery cost estimatesreceived more than 10 times the funding calledfor in their recovery plans, whereas 18 taxareceived less than 10 percent of their estimatedfunding needs. Underfunded species includeboth well-funded species that require addi-tional investments (such as Guam kingfisher,found only in captivity) and species thatreceive scant funding (such as Hinckley oak).

Without more funding for species recovery,protection for most underfunded species willlikely continue to be limited to consultationsand prohibitions under ESA sections 7 and 9(See “Extinction Prevention” requirements inthe ESA Overview section). Plants in particularare a challenge (see Box 3), partly becauseplants on private land are not usually covered bysection 9 prohibitions. The Services have madegreat strides over the past decade in disseminat-ing documents that describe recovery plans,recovery actions, expenditures, critical habitatdesignations, cooperative agreements, and othermeasures for evaluating ESA outcomes.However, unless the Services do more to docu-ment the outcomes of actions taken under ESAsections 7 and 9, it will remain difficult to tellwhether they are effective in stabilizing andimproving the status of underfunded species.

Spending Priorities

Due to insufficient funding, tradeoffs are nec-essary, and the Services must decide what

Figure 6. Disproportionategovernment spending among

listed taxa in 2012, as depictedby the percentage of total

expenditures (size of wedge)and the number of listed speciesin each taxonomic group (shown

in parentheses in the legend).Total government spending was

approximately $1.364 billion.

Fish (165)

Birds (98)

Mammals (101)

Reptiles (42)

Plants and Lichens (778)

Invertebrates (238)

Amphibians (25)

1.2%2.9%3.3%

4.8%

13.0%

13.3%

61.5%

Box 3. Listed Plants: Bottom of the Funding Food Chain

First added to the endangered species list in 1977, plants now comprise 55 percent of all listedtaxa, far more than any other taxonomic group (Figure 1). From 1998 to 2012, however, plantsaccounted for less than 12 percent of FWS funding for all listed species—and for less than 4 per-cent of total government expenditures on listed species in 2012 alone (Figure 6). From 1998 to2012, the inflation-adjusted median annual government spending per listed plant species was$20,000, well below estimated recovery costs for most listed plants. Moreover, much of the moneyspent on plants goes to pay for ESA section 7 consultations, with relatively little going into recoveryactions or monitoring studies of population status and trends.



recovery actions take priority. For example,investing in habitat restoration for a threat-ened mammal might delay reintroductionplans for an endangered fish, and surveyingpopulations of an endangered bird mightmean postponing a seed germination projectfor imperiled orchids. Accordingly, FWS andNMFS each developed a prioritization systemfor analyzing tradeoffs. The FWS systemincludes 36 ranked categories groupedaccording to 4 factors: degree of threat,potential for recovery, taxonomic uniqueness,and conflict with human activities. TheNMFS system is similar but has only 12 cate-gories and omits taxonomic uniqueness. Toour knowledge, no researchers have evalu-ated how frequently or successfully NMFSuses its prioritization system to allocaterecovery funding, perhaps because NMFSmanages fewer than 5 percent of all listedspecies. However, it is well established thatFWS does not frequently use its system.Instead, FWS’s allocations are more oftendriven by political and social factors, includ-ing congressional representation, the numberof employees in field offices, staff workload,and opportunities to form partnerships andsecure matching funds. In addition, differentregions and field offices often use differentallocation formulas.

Without following a uniform and explicitsystem for prioritizing recovery actions, FWScannot efficiently allocate its funding to meetrecovery needs. That is partly why most recov-ery funding has benefited only a small fractionof listed species. Moreover, FWS cannotclearly articulate to Congress and other stake-holders what recovery actions it will imple-ment with available funding and what addi-tional achievements are possible with morefunding. As a result, the agency is poorly posi-tioned to request additional funding.

MODERN ECOLOGICALCHALLENGES TO MANAGING FORSPECIES RECOVERY

The United States and its ecosystems havechanged dramatically since the ESA wasenacted in 1973. Human populationgrowth, economic activity, and intensiveland uses have rapidly increased. Threats tolisted species such as habitat loss and degra-dation and invasive exotic species haveincreased in severity. Climates have under-gone fundamental change. These trendswill likely continue.

Conservation-Reliant Species

Researchers are increasingly recognizing thatmany listed species face pervasive and persis-tent threats that can be managed but are notlikely to be eliminated. These species areknown as “conservation reliant.”Conservation managers might be able toincrease their populations and sufficiently mit-igate threats to achieve recovery targets, butthe species remain at risk because the threatsthey face require ongoing monitoring andmanagement.

There are two forms of conservationreliance, depending on what kind of man-agement is needed—whether management isdirected toward populations or towardextrinsic threats. For example, the northernIdaho ground squirrel lives in habitatpatches that have become increasingly frag-mented, making it susceptible to loss ofgenetic diversity; its populations thereforeneed to be managed through translocation orcaptive breeding to meet recovery targets. Bycontrast, the Kirtland’s warbler requires thatits breeding grounds, which are almostexclusively in Michigan, remain in an early-successional habitat stage that historicallywas maintained by fire. Human interventionwill likely be needed for the foreseeablefuture to maintain the habitat in an early-successional stage.

The most common management strategiesneeded to mitigate threats to conservation-reliant species are: creating or restoring habi-tat; controlling invasive exotic species; reduc-ing pollution and other human impacts, suchas overexploitation; and increasing the sizeand/or genetic variability of populationsthrough artificial recruitment.

Climate Change

Climate change is expected to increase thenumber of species at risk of extinction, and itwill exacerbate the problem of conservationreliance. Since 1900, global mean tempera-tures have increased by 0.7 degrees Celsius,affecting every major group of plants and ani-mals. Approximately half of all species studiedhave shifted their ranges to higher latitudes(50 to 1,600 kilometers poleward) or eleva-tions (up to 400 meters upslope). About two-thirds of all species studied have shiftedtoward earlier spring breeding, migration, orblooming. Because responses among speciesvary widely in both strength and direction, it



can be difficult to predict how particularspecies will respond to climate change. Thisincreases uncertainty for conservationresearchers and managers.

Nonetheless, climate change is clearly caus-ing biological communities to disassembleand reassemble in new configurations, andscientists can estimate how species will beaffected. In 2009, a large-scale study ofamphibians, birds, and mammals showed howspecies are expected to undergo climate-induced range shifts, producing “turnover” inecological communities as species are gainedand lost (Figure 7). For these groups ofspecies, turnover is likely to be high over thenext century, especially on the west coast andnorthern mountains of Alaska and in penin-sular Florida, southwestern Texas, and thesouthern Great Plains.

Climate change also might cause broadshifts in environmental conditions, such aslarge-scale changes in temperature and precip-itation. These changes could expose multiplepopulations of endangered and threatened

species located in different areas to similarenvironmental threats, thereby reducing thechances that declining populations can be res-cued by immigration from more abundantneighbors. In addition, climate change isalready causing sea levels to rise, affectingcoastal areas and their attendant set of imper-iled and listed species.

The ESA provides a flexible framework formeeting the national commitment to listed-species recovery. Given the daunting challengesfacing conservation managers, and in view ofmodern insights from ecology and conservationscience, changes are needed in at least six keyareas, including: setting priorities, strengtheningpartnerships, promoting monitoring and adap-tive management, refining methods to developrecovery criteria, using climate-smart conserva-tion strategies, and evaluating and developingecosystem-based approaches.

SETTING NEW PRIORITIES FORSPECIES RECOVERY

The ESA requires the Services to set prioritiesfor drafting and implementing recovery plans,but it offers limited guidance for how to priori-tize species for recovery measures in the face ofchronic funding shortfalls. When FWS createdits current ranking system for listed species in1983, it did so in good faith and in accordancewith the requirements given in the ESA (sec.4(f)(1)). FWS weighted each of the four factorsit considers for prioritization (degree of threat,potential for recovery, taxonomic uniqueness,and conflict with human activities), but the

Figure 7. Percent turnover inamphibians, birds, and

mammals attributable toclimate-induced range shifts

under two greenhouse gasemissions scenarios devised bythe Intergovernmental Panel on

Climate Change for the 21stcentury: (a) the B1 scenario

projects relatively modestincreases in future emissions;

and (b) the A2 scenario is in the“mid-high” range of futureemissions. (Turnover is the

number of species predicted tobe gained and lost in each 50-

by-50-kilometer area from 2071to 2100, compared to the

number of species in each areafrom 1961 to 1990.) Hawaii is

not shown because there wereinsufficient data to estimate

species turnover.

Box 4. New Zealand’s Prioritization System for SpeciesRecovery

New Zealand’s Department of Conservation lacks sufficient funding to conserveall of New Zealand’s approximately 2,800 threatened species. Until recently, theDepartment also lacked an explicit system to prioritize conservation actions,and its annual budget covered only 188 species, many of which were inade-quately managed. In response, the Department worked with scientists to esti-mate management needs and costs for all of New Zealand’s threatenedspecies, and they developed a ranking system that established funding priori-ties according to the agency’s goal of “securing (over a period of 50 years) thegreatest number of threatened species.” Because the Department now hasmanagement plans and cost estimates for all threatened species, managers areable to efficiently prioritize many more species for conservation with no addi-tional funding. Through its new prioritization system, the Department expects toeffectively manage 273 species with the same level of funding, a 45-percentincrease in species covered.

(a) (b)% Turnover

< = 10>10 – 20>20 – 30>30 – 40>40 – 50>50 – 60>60 – 70>70 – 80>80 – 90>90

N

0 250 500 700 1000

Kilometers

N

0 250 500 700 1000

Kilometers

INCREASING THEEFFECTIVENESS OF ESA

IMPLEMENTATION



system is rudimentary and insufficiently trans-parent, and it has failed to meet FWS needs.

Conservation managers around the worldface the same problem of insufficient fundingto conserve endangered and threatenedspecies. Agencies can best manage the prob-lem by adopting and implementing more sys-tematic and transparent criteria for allocatinglimited funds (see Box 4). As an initial step,the Services need a renewed commitment tousing a priority-setting system that allocatesrecovery funds in order to maximize strategicoutcomes for listed species. The Services couldmore consistently apply the ranking systemthey currently have or use new or additionalcriteria that remain consistent with the recov-ery prioritization factors given in the ESA.

Choosing recovery-funding prioritiesrequires policy judgments about the types ofspecies that the Services seek to prioritize.Science alone cannot identify which or howmany goals to build into a ranking system. Todetermine which criteria to use and how muchweight to assign to each, the Services shouldconsider using a process that engages expertscientists and practitioners to analyze the goalsfor recovery funding, achieve a consensusbased on the objectives of the ESA, and thensubmit the results for public comment.

The outcome of such a process would beconstrained by the Services’ current budgetingpractices and appropriations from Congress.For example, FWS currently uses most recov-ery funds to pay salaries, so staff size deter-mines which regions receive the most funding.A system for allocating recovery funds in a

way that maximizes strategic outcomes forlisted species might require new budgetingallocations for the Services to pay their staffs.

STRENGTHENING PARTNERSHIPSFOR SPECIES RECOVERY

State, private, tribal, and federal entitieshave long played mutually supporting roles inprotecting fish and wildlife species and thehabitat they need. Conservation managerscan build on a variety of partnership tradi-tions for species recovery.

The Role of the States

States can provide funding and pass laws tohelp species recover in ways that are both spe-cific and flexible (see Boxes 5 and 6). Forexample, Florida created dedicated fundingsources for the endangered Florida manateeand Florida panther, and Florida’s legislaturepassed laws authorizing boat speed zones toprotect manatees and car speed zones to pro-tect panthers. Florida has spent about twice asmuch as FWS on manatees and over threetimes as much on panthers. FWS is now con-sidering reclassifying the manatee from endan-gered to threatened, and the estimated pan-ther population has more than tripled sinceconservation began in the 1970s.

State wildlife agencies can also provide“boots on the ground” for research and man-agement activities that foster species recovery.Although many states have limited capacity tomanage endangered and threatened species,

Box 5. Florida’s Imperiled Species Management System

The Florida Fish and Wildlife Conservation Commission (FWC) conserves species on a wide continuum, from extremely rare to abun-dant. Along this continuum, FWC has programs to address federally listed as well as unlisted species.

FWC created Florida’s Wildlife Legacy Initiative to implement and manage the state’s wildlife action plan (SWAP). The Initiative, whichis nonregulatory and incentive-based, has identified more than 1,000 species that are high priority for conservation, and it has explicit5-year goals for maintaining, restoring, and connecting high-priority habitats across the state. In the first 5 years of implementing theSWAP, FWC worked with more than 100 partners to secure $33 million in funding and matching contributions and launched about 150projects on both public and private lands. By managing habitat, stabilizing populations, and reducing and removing threats, these pro-jects have helped prevent the need for federal listings. For example, FWS did not list the Florida black bear because state-level con-servation efforts are working.

In 2010, Florida revised its rules regarding state-listed imperiled species to improve conservation and make the listing process moretransparent, thereby reducing public controversy. Florida’s list includes federally listed species and “state threatened” species that arenot federally listed. FWC decides whether to list a species based on criteria similar to those developed by the International Union forConservation of Nature. All listed species are covered by a management plan developed with public input. FWC is currently working ona single unified management plan for 60 species to avoid the need for federal listing.

Florida also works with FWS to conserve federally listed species. Close cooperative relationships are maintained through annualcoordination meetings involving state and federal staff, regular coordination calls involving interagency leadership, collaborative field-work, and joint press releases. A cooperative agreement signed in May 2012 has created a framework that could allow the state toauthorize incidental take for federally listed species, the first such program in the nation.



all states have agencies dedicated to managingwildlife, and most have longstanding relation-ships with key stakeholder groups—includinghunters, anglers, outdoor recreationists,landowners, and farmers—enjoying a level oftrust that the federal government often doesnot. Trust is essential for developing publicconsent to and acceptance for the actionsneeded to recover listed species.

Moreover, state wildlife agencies can con-duct broad proactive conservation planningthrough their state wildlife action plans(SWAPs). In 2005, all 50 states, the Districtof Columbia, and 5 U.S. territories developedSWAPs in order to receive federal fundsthrough the Wildlife Conservation andRestoration Program and the State WildlifeGrants Program. Congress funded these pro-grams to help conserve species of greatest con-servation need—before they need to be listedunder the ESA. However, many states directSWAP funding primarily to sport fish andgame, instead of broadly addressing all speciesat risk. For example, most SWAPs fail to ade-quately conserve plant species because statesare not required to consider plants in order toreceive SWAP funding; only 8 SWAPsinclude plants among the species of greatestconservation need. In addition, many statesspend SWAP funding disproportionately onthe most iconic or charismatic at-risk species.Statewide systems are needed for assessing allat-risk species as part of a comprehensive pro-gram to conserve species diversity and ecosys-tem health.

Partnering with PrivateLandowners

More than two-thirds of all listed speciesoccur on private lands, and about one-thirdoccur only on private lands. By restricting theuse of lands that support listed species, theESA can create disincentives for speciesrecovery. Landowners might be motivated topreemptively destroy habitat for listed speciesor otherwise hinder their conservation.

Over the past 20 years, the Services havedeveloped tools to reduce disincentives forconserving listed species and provide incen-tives for protecting them (see Box 7), includ-ing safe harbor agreements, habitat conserva-tion plans, candidate conservation agreements,candidate conservation agreements with assur-ances, and conservation banks. Most of thesetools include “no surprises” assurances thatincrease regulatory certainty by ensuring thatunforeseen circumstances do not trigger unex-pected restrictions on private landowners orrequire them to commit new resources.

The Services’ incentives for landowners doincrease landowner flexibility, but it is difficultto evaluate their effectiveness. Informationabout landowner compliance is limited, as isbiological monitoring to establish the outcomesfor listed species. To date, habitat conservationplans (HCPs) are the best evaluated program,although conclusions are mixed and most stud-ies are based on small sample sizes and do notinclude rigorous statistical evaluation. Oneevaluation concluded that HCPs have aided

Box 6. Multispecies Cross-Jurisdictional Conservation in California

California leads all states in the number of listed animal species and is second only to Hawaii in the number of listed plant species.Although half of the state is public land, many listed species depend on private lands or on water sources with heavy human use. Forexample, the state’s $45 billion agricultural sector encompasses 43 million acres of cropland and rangeland (43 percent of the stateland area) and uses up to 80 percent of the available water supply. Protection and recovery of listed species has engendered costly andpolitically charged conflicts.

The magnitude of the challenge has led the state to pursue cross-jurisdictional ecosystem-based planning over large areas. TheCalifornia Natural Community Conservation Planning Act, passed in 1991 and revised in 2003, provides a mechanism for permittingdevelopment and incidental take. The program creates large habitat preserves for multiple species through cooperative agreements,relying on voluntary enrollment by private landowners in conservation banks (see Box 8) that are purchased over time and fundedlargely by land developers. Eight natural community conservation plans already cover 3.4 million acres and 18 more are planned.Together, they will cover about a third of the state.

It is too early to tell whether the regional plans will reverse the decline of listed species. Many habitats are already degraded and frag-mented by development, and the natural community conservation plans are generally designed for mitigation rather than recovery.Information about the ecology and habitat requirements of species covered by the plans is often minimal, and funding is limited.Climate change also poses a challenge to this kind of blueprint planning based on fixed development areas and reserve boundaries.

However, there is some evidence that large habitat conservation plans of the type being implemented in California benefit listedspecies compared to species without such plans or in smaller plan areas. In addition, the planning framework brings multiple organi-zations and stakeholders to the table, and it provides an opportunity for scientifically guided systematic conservation planning to avoidunnecessary impacts on listed species while encouraging species protection and mitigation for unavoidable impacts.



species recovery and that benefits increase withthe size of the area covered. However, theresearchers did not find that plans coveringmultiple species provided additional benefits.

The Services encourage landowners to usemultispecies HCPs to gain flexibility, reducelogistical burdens, and increase the biologicalvalue of individual plans. Lack of supportingevidence for such benefits might be an artifactof their limited use. There are no multispeciesHCPs (covering five or more species) in theareas where listed species are concentrated inthe eastern United States (Figure 8). Theirtrue usefulness therefore remains to be seen.

Moreover, most HCPs are designed to meetregulatory requirements, allowing landowners tomitigate the impacts of development withoutrequiring actions that provide a net benefit tolisted species. More plans that directly link man-agement actions to species benefits are needed.

Processes for implementing landowneragreements are often time consuming and lacktimelines for completion. By reducing thecomplexity of agreements and the timerequired to complete them, the Services mightincrease landowner interest in participatingwhile freeing up more agency staff time. Better

integration of landowner programs into otheraspects of ESA implementation, includingrecovery planning, would allow programs tohave a greater impact.

FWS continues to develop new landownerincentives and funding mechanisms to pro-mote listed-species recovery. (See Table 1 for asummary of landowner incentives and

Table 1. Landowner Incentives and Intended Benefits

Benefits Incentives

Reduces disincentives for SHAconservation

Provides regulatory certainty for SHA, HCP, CCAA, habitat credit programslandowners

Reduces constraints on land use HCP, CCAAby providing a legal pathway for incidental take

Helps avoid the need for species CCA, CCAA, habitat credit programslistings

Provides revenue or financial Conservation banks; habitat credit assistance for conservation programs; Working Lands for Wildlife

initiative; ecosystem service markets

Note: CCA = candidate conservation agreement; CCAA = candidate conservation agreement with assur-ances; HCP = habitat conservation plan; SHA = safe harbor agreement.

Box 7. Incentives for Landowners

Safe harbor agreements (SHAs) are appropriate for landowners who have a listed species on their property and are generally com-fortable having the species there but don’t want the species to generate new regulatory restrictions if its population increases. SHAsare voluntary agreements between the Services and private or nonfederal public landowners who agree to take action to help recoverlisted species. In exchange, landowners receive permits for the incidental take of listed species and formal assurances that theServices will not require anything more, as long as landowners abide by the terms of the agreement. At the end of the agreementperiod, landowners may return the enrolled property to an agreed-upon “baseline” condition. By the end of 2012, FWS had approvedmore than 70 SHAs covering 4.4 million acres and 213 miles of aquatic habitat.

A habitat conservation plan (HCP) is appropriate when landowners know their actions might cause incidental take of a listed species.The ESA requires landowners who intend to undertake otherwise lawful actions that might result in take of a listed species to apply for inci-dental take permits. To receive permits, landowners must submit a conservation plan (CP) (ESA sec. 10(a)(1)(B)), usually a HCP. The plandescribes the anticipated effects of the proposed take, identifies management actions that minimize and mitigate adverse impacts tospecies, and describes how actions will be funded. Most HCPs currently cover a single listed species, with fewer than five percent cover-ing five or more species. By the end of 2012, FWS had approved more than 650 HCPs covering 85.5 million acres and several hundredspecies. NMFS had completed about 34 CPs, mostly HCPs, but some addressing incidental take of listed fishes because of fishing gear.

Candidate conservation agreements (CCAs) are appropriate for landowners who want to help protect “candidate species,” whichwarrant listing but have not been proposed for listing because of resource constraints or other species receiving higher priority. CCAswith assurances (CCAAs) provide landowners with regulatory certainty if the species is eventually listed. Under both types of agree-ment, landowners agree to proactive conservation measures designed to reduce threats to the candidate species. Under CCAAs, theServices provide assurances that landowners who implement conservation measures will not be subject to additional restrictions if thespecies covered by an agreement is ultimately listed. By the end of 2012, FWS had approved more than 100 CCAs and 26 CCAAs.NMFS had not issued any CCAs or CCAAs.

Conservation banking enables private landowners to receive payments for permanently conserving and managing land parcels (conservationbanks) for listed or candidate species. The Services allocate conservation credits to landowners according to a bank’s value for supportingspecies. Landowners can then sell the credits to buyers who need to purchase them in order to compensate for some permitted incidental takeof species in a different location. By the end of 2012, the FWS had approved about 80 conservation banks covering about 48,000 acres.

16 esa © The Ecological Society of America • [email protected]


trator oversees monitoring and verification ofcredit transactions and measures progresstoward conservation goals. The Servicesshould use such market-based funding mecha-nisms more widely to promote species recov-ery, and they should consider other ecosystem-market-based tools similar to those developedby nongovernmental organizations inCalifornia (see Box 8).

All of the Services’ incentives for landown-ers need further evaluation of conservationoutcomes, landowner satisfaction, and strate-gies to increase effectiveness. Research wouldbenefit from greater public access to basicinformation about voluntary landowner agree-ments, including their terms and locations,landowner compliance, and outcomes forlisted species. In addition, a better understand-ing of landowner motivations is needed inorder to design better incentive mechanisms,so the Services could benefit by increasing thesocial science capacity of their staffs.

Recovery ManagementAgreements for Conservation-Reliant Species

Conservation-reliant species require ongoingmanagement following recovery. Recoverymanagement agreements are designed toensure that conservation-reliant species willbe adequately protected and managed afterdelisting. A good example is the Robbins’cinquefoil, a small perennial plant that waslisted due to habitat loss and trampling nearthe Appalachian Trail. After successfullyincreasing the cinquefoil’s population numbersand working to have the trail rerouted, FWSentered into recovery management agree-ments with the USDA Forest Service to pro-tect the cinquefoil’s habitat and with a non-profit organization to monitor trail use andprevent trampling in the future. These agree-ments provided the regulatory assurancesneeded to delist the cinquefoil in 2002.

The regulatory status of conservation-reliantspecies that have met recovery criteria wouldbe more certain if the Services developed anexplicit policy for evaluating proposals todelist these species, similar to their Policy forEvaluation of Conservation Efforts (PECE),which applies only when the Services makelisting decisions. PECE establishes criteria fordeciding when it is unnecessary to list aspecies because federal agencies, state andlocal governments, and private entities havealready agreed to conservation efforts that are

intended benefits.) Under one proposed pro-gram, landowners who take action to help aspecies before it is listed would earn creditsthey can use to mitigate development activi-ties after it is listed. In another program, calledWorking Lands for Wildlife, FWS partnerswith the USDA Natural ResourcesConservation Service in furnishing technicaland financial assistance to farmers, ranchers,and forest landowners who voluntarily imple-ment proven conservation practices on theirland. Working Lands for Wildlife allowslandowners to keep lands in production whilecomplying with the ESA and restoring species’habitats.

Habitat credit exchanges provide anotherexample. Landowners can offset developmentimpacts on listed or candidate species by pur-chasing credits from landowners who create,maintain, or improve habitat through conser-vation actions. A habitat exchange adminis-

Figure 8. The geographicoverlap of listed-species

hotspots with counties that haveHCPs covering at least five

species.

N

0 250 500 700 1000

Kilometers

Number of Species(Formally Listed)

None12 – 45 – 910 – 100

County with HCPcovering ≥ 5 species

Robbins’ cinquefoil.Photo credit: U.S. Fish and Wildlife Service.

likely to be effective. Similarly, when decidingwhether to delist conservation-reliant speciesbased on recovery management agreements, itis crucial to ensure that conservation actionscontinue to be implemented. Accordingly,recovery management agreements require:willing landowners within the species’ rangewho have authority to implement them, tech-nical guidance and assistance for landowners,agreements with landowners and local regula-tors to continue successful managementactions, a monitoring program, mechanismsfor ensuring long-term funding, and triggersfor the Services to reevaluate listing decisionsif species recovery is reversed.

Are nonfederal parties, particularly privatelandowners, willing to take responsibility formanaging conservation-reliant species?Studies suggest that landowners are not moti-vated solely by economic considerations andthat some are willing to protect or restorehabitat in exchange for technical assistanceand other incentives. Recovery managementagreements that permit delisting conserva-tion-reliant species can provide privatelandowners and other nonfederal conserva-tion managers with greater certainty in man-aging their lands. Such agreements are predi-cated upon species having increased inpopulation abundance and distribution as aresult of specific management actions thathave proven successful. By demonstrating theESA’s effectiveness, delisting conservation-

reliant species can also increase public sup-port for the law and permit conservationmanagers to celebrate successes.

Partnerships for Data Storage,Management, and Sharing

In 2009, the Obama administration instructedfederal agencies to publish data online in anopen and searchable format to increase trans-parency and foster public participation in gov-ernment decisionmaking. Because many stake-holders are involved in managing listedspecies for recovery, relevant informationshould be readily available and widely shared(to the extent permitted by law and subject tovalid concerns about protecting species).

The most comprehensive system that theServices have developed for managing andsharing information about listed species is theFWS Environmental Conservation OnlineSystem (ECOS), which gives species descrip-tions and information about species distribu-tions, listing status, federal register publications,special rule publications, recovery plans, down-loadable maps of critical habitat, and links toother resources. ECOS also includes an onlineplanning tool, the Information, Planning, andConservation decision support system, whichhelps users avoid adverse impacts on listedspecies and take steps to support their recovery(http://ecos.fws.gov/ipac/). The Services couldfurther increase transparency and facilitate



Box 8. Ecosystem Markets for Species Recovery in California

Not only is California the leader in conservation banking and habitat credit exchanges, but conservation interests in the state are alsoincreasingly looking beyond regulatory solutions to more direct engagement with private landowners and companies in ecosystemmarkets. For example, The Nature Conservancy (TNC) recently launched a program that pays Sacramento Valley rice growers to keeptheir fields flooded during bird migration periods on the Pacific Flyway. The program uses a reverse auction approach: farmers put upsecret bids, setting a price for flooding their fields, and TNC selects which properties to enroll. The approach is far less costly than tradi-tional conservation approaches and could promote sustainable agricultural practices while improving habitat for species of concern. Inthe Garcia River Forest project, The Conservation Fund and TNC are working with state agencies and private timber interests in a non-profit land management scheme that uses revenues from timber harvest and carbon credits to restore habitat for a variety of listedspecies, including the red-legged frog, marbled murrelet, and Chinook salmon. Both programs involve scientists in project design, imple-mentation, monitoring, and adaptive management.

Marbled murrelet. Photo credit: Larry Master.

Red-legged frog. Photo credit: L. Lee Grisner, U.S. Fish and Wildlife Service.

Chinook salmon Photo credit: John R. McMillan, Trout Unlimited.

research by making public searchable electronicdocuments related to listing decisions, consul-tations, and recovery actions. Of particularvalue for assessing the effectiveness of the con-sultation process would be biological opinionsand HCPs, along with the associated incidentaltake permits and monitoring reports. The docu-ments could be posted on ECOS or the federalgovernment’s www.data.gov website.

NatureServe’s databases also include substan-tial information about the status, trends, threats,and distribution of listed species and thousands ofother at-risk species. Though used by every fed-eral agency involved in natural resources man-agement, NatureServe’s databases could be betterintegrated into decisionmaking related to specieslisting and recovery as well as other managementactions. Unfortunately, licensing arrangementsare fragmented and inefficient. A single federallicense permitting multiple agencies to accessNatureServe data would foster greater sharing ofdata both among federal agencies and with stateagencies and private stakeholders that collabo-rate in managing listed species.

PROMOTING MORE MONITORINGAND ADAPTIVE MANAGEMENT

Managing species recovery requires monitoringthe implementation of recovery plans and com-pliance with permits and other agreements; theoccurrence, persistence, distribution, and statustrends of the species themselves; and the con-sequences of management actions in order tosupport adaptive management.

Implementation andCompliance Monitoring

The Services regularly monitor recovery planimplementation to determine whether adjust-ments are needed to recovery plans andwhether additional partners are needed.However, it can be difficult to get the neces-sary data because their partners do not alwayssubmit complete data on time. The Servicesalso monitor compliance with permits andother agreements, such as HCPs, but theircapacity to do so is often limited by insuffi-cient staff and funding.

Monitoring Species

The simplest approach to monitoring listedspecies is to find out where they occur andhow abundant they are in particular areas.Presence/absence surveys can help theServices better target recovery actions, assesshuman impacts, and determine whether con-sultations are needed. Repeated, systematicpresence/absence monitoring can help conser-vation managers assess species’ status, trends,and distribution over time.

However, with few exceptions (such as theCalifornia condor and Florida manatee),listed-species monitoring is rarely rigorous,because a robust monitoring program requiresmore staff time and is usually more expensive.This is a major gap in listed-species manage-ment. Rigorous monitoring programs withclear and consistent protocols are necessary toaccurately assess trends in species’ abundanceand distribution, the threats they face, andtheir responses to management actions.

Adaptive Management

Conservation managers typically have onlylimited information about listed species, andthey often cannot predict species’ responses tomanagement actions, especially in rapidlychanging environments. Through adaptivemanagement, managers can take actions to pro-mote recovery, monitor and learn from theresults, and improve their techniques in light ofnew understanding about the ecological andsocial contexts in which they are working.Unfortunately, managers have not used adap-tive management as frequently as they shouldto recover listed species, largely because of lim-ited staff time, research capacity, and funding.

Adaptive management requires structureddecisionmaking in two phases (Figure 9). In



Assess themanagement

challenge

Design amanagment

strategy

Implement thestrategy

Adaptive Management Cycle

Iterativephase

Deliberativephase

Learning andadjusting decisionsbased on what is

learned

Monitor theresults

Evaluate theoutcomes

Adjust thestrategy

Figure 9. The adaptivemanagement cycle in terms ofdesigning, implementing, and

evaluating managementstrategies, learning from the

outcomes, and increasingmanagement effectiveness.

the deliberative phase, managers assess thechallenge, clarify objectives and alternatives,and design and implement a managementstrategy. In the iterative phase, managers mon-itor the results, evaluate the outcomes, andadjust their strategies accordingly. Throughoutthe process, managers integrate the elementsof the iterative phase into the deliberativephase in an ongoing cycle of learning andadaptation.

Adaptive management typically takes twoforms—passive and active. Passive adaptivemanagement is like systematic trial and error.It involves setting trigger points for reviewand reconsideration of the current manage-ment strategy but rarely limits the number ofvariables tested or establishes controls forcomparison. Consequently, it can sometimesbe inadequate to resolve uncertainty about keyrequirements for species recovery. Activeadaptive management is more rigorouslyexperimental. It usually involves testing man-agement strategies one variable at a time, withcontrols, and evaluating the strategies withmore intensive monitoring. It is generallymore expensive than passive adaptive man-agement, but it has greater potential to iden-tify the necessary elements for an effectiverecovery program.

However, active adaptive management mightnot be appropriate for listed species in somecases, for example, if experiments might harmor even kill species. This is the case for theFlorida manatee, which is threatened by colli-sions with boats. To promote manatee recovery,managers and policymakers closed areas toboating and imposed boat speed limits wheremanatees are known to gather. It would createunacceptable risks to manatees to allow unregu-lated boating in some of these areas for experi-mental comparison, so no one has conducted acontrolled experiment to evaluate the efficacyof boat closures and speed limits. But managershave monitored manatee populations beforeand after the boating regulations were imposed,and this monitoring confirms that fewer mana-tees are killed in the protected areas.

Before using experimental managementstrategies, managers and regulatory authoritiesneed to develop a clear understanding of theknowledge gaps related to the strategies theyare considering, how adaptive managementexperimentation can fill those gaps, and whatconditions would trigger new strategies inlight of new information. However, conserva-tion managers should regularly use at least apassive form of adaptive management, in

which they establish baseline conditions forlisted species, monitor species’ responses tomanagement actions, and adjust managementstrategies accordingly.

Overcoming Obstacles toMonitoring and AdaptiveManagement

The biggest obstacles to monitoring are theneed for long-term commitments, relativelyheavy staff involvement, and equipment thatcan be costly. Given the choice, most man-agers will opt to commit their limited staff andresources to additional recovery actions ratherthan monitoring.

Leaders and funders of conservation agen-cies and organizations need to make strongercommitments to increase monitoring.Scientific researchers can also help by collabo-rating with managers to make monitoringmore efficient—by identifying the minimuminformation necessary to evaluate species sta-tus and trends and by designing protocols forparticular types of species (such as potentialindicator species) or species assemblages.Other practical measures include determiningwhat type of monitoring is most critical whereand designing protocols that can be appendedto existing monitoring efforts, especially bystate and federal agencies (such as theNational Park Service Inventory andMonitoring Program).

In addition, conservation managers can takeadvantage of low-cost citizen science pro-



Loggerhead sea turtle.Photo credit: Larry Master.



grams, such as the North American BreedingBird Survey and state-based natural heritageprogram efforts to enlist members of the publicto monitor species. Citizen science—partici-pation by the public in part of a scientific pro-ject—is growing exponentially and can be use-ful for many types of monitoring. For example,each summer in South Carolina citizen scien-tists volunteer to monitor threatenedLoggerhead sea turtles on beaches. Volunteerskeep track of when the turtles arrive to layeggs, the number and distribution of turtlenests, how many eggs hatch, and other para-meters important for turtle conservation.Researchers evaluating this citizen scienceprogram found that in 2012 volunteers con-tributed $390,000 worth of monitoring effort,which led to more than a million dollars inmatching funds. Although nonprofessionalcitizen monitoring of listed species mightrequire special permitting in some cases, citi-zen scientists can gather essential data for con-servation managers and free up funding foradditional monitoring and management.

The biggest obstacles to adaptive manage-ment have to do with its requirement forextensive monitoring and situations thatrequire active experimentation with listedspecies. Conservation managers are under-standably cautious about experimenting withlisted species for fear of losing critical habitator jeopardizing species’ continued existence.Leaders of conservation agencies and organiza-tions can help by rethinking the notions ofrisk and risk aversion, by developing protocolsto evaluate when active experimentation withlisted species can be most useful and to esti-mate the risks to the species involved, and byencouraging and rewarding ongoing learningby individual managers and practitioners.Similarly, private landowners who receiveincidental take permits are often more inter-ested in complying with regulatory require-ments than in ongoing experimental manage-ment and monitoring. All managementagreements (such as HCPs) and recovery plansshould specify clear thresholds and triggersthat signal the need to reassess and potentiallychange management. Scientists should workwith conservation managers to establishappropriate thresholds that can be used toevaluate management outcomes and triggerthe need to modify a strategy before irre-versible harm occurs. Triggers should beenforceable and transparent to all stakehold-ers, and the responsibilities for designing, con-ducting, and funding monitoring programs

should be made explicit up front.Many agencies do not have enough scientists

to design, implement, and evaluate the moni-toring necessary for adaptive management,especially the experimental treatments neededfor active adaptive management. Moreover,monitoring is not generally conducive toresearch leading to peer-reviewed publications,which discourages scientists from contributingto management-oriented monitoring. Morescientists need to partner with conservationmanagement agencies and organizations todesign, conduct, and interpret experimentaltreatments in an adaptive management frame-work. Researchers can also help train skilledpractitioners and support them in the field.

REFINING METHODS TODEVELOP RECOVERY CRITERIA

Recovery plans are supposed to include“objective, measurable criteria” for determin-ing when species can be delisted (ESA sec.4(f)(1)). The Services have generally usedthree types of criteria: (1) thresholds forspecies abundance and geographic distribu-tion, (2) qualitative criteria related to popu-lation trends (for example, recovery plansmight state that populations should be“healthy” or “stable or increasing”), and (3)requirements that threats are sufficientlyabated. However, scientists have often criti-cized the criteria in recovery plans as not suf-ficiently based on the best available science.

Problems with RecoveryCriteria

Reviews of recovery plans have found that cri-teria specifying a given number of individualsor populations usually give a number that istoo low to provide for a high likelihood ofspecies persistence. Conversely, qualitativecriteria related to population trends lack speci-ficity, so it is difficult to determine when theyare met. Further, few species have quantitativecriteria specifying how much habitat is neededand how it should be distributed – eventhough habitat loss and degradation are themost common threats to listed species – andrecovery criteria have varied widely for differ-ent species.

These problems have several sources. TheESA does not precisely define the phrases “indanger of extinction throughout all or a signif-icant portion of its range” and “within theforeseeable future” (ESA secs. 3(6), 3(20)).

Interpretations have ranged from acceptingminimum viable populations to requiring self-sustaining and ecologically functional popula-tions. The Services lack transparent and con-sistent approaches for determiningquantitative recovery criteria, and recoverycriteria unavoidably reflect a wide range ofsocietal values, economic conditions, andcompeting uses for habitat.

Furthermore, the likelihood that a particularspecies will go extinct depends on the typeand severity of the threats it faces as well asvarious biological factors (such as body size,life history, and genetic diversity) and ecologi-cal characteristics (such as habitat specializa-tion, successional status, and the size and dis-tribution of populations). Extinction risk istherefore highly contextual, and methods arestill lacking for using general principles ofconservation science and the often-minimaldata available to estimate probabilities of per-sistence for most listed species.

Strengthening the ScientificFoundation for RecoveryCriteria

For recovery criteria that address the abun-dance and distribution of listed species to beobjective and measurable, they should bebased on numerical measurements, at specifictimes and places, with clearly stated levels ofstatistical confidence. Such recovery criteriashould meet the requirements of individualorganisms for survival and reproduction,reflect the species abundance and densitiesneeded to sustain secure local populations,specify the number of local populations andthe geographic distribution necessary for per-sistent populations across the species’ range,and state the rangewide minimum habitat arearequired for species to survive random distur-bance events (see Box 9). Recovery criteriathat address the mitigation of threats and theadequacy of other regulatory mechanisms toprevent species from declining after they aredelisted might not lend themselves to numericvalues, but they nevertheless should be objec-tive and measurable, e.g., they should identifyspecific regulations and management plansthat will remain in force to reduce threats.

Population viability analysis (PVA)—aquantitative assessment of the probability ofextinction based on several often-interactingfactors—is one useful scientific method forrecovery planning. However, for most species,it is not possible to collect the extensive data

needed for a robust PVA, given limited timeand funding. Scientists often conduct PVAsusing only population-level data, but thismethod also typically requires extensive datacollection, and it is insufficient for addressingthreats to habitat and range. Nevertheless, sci-entists and recovery planners can construc-tively use PVA to develop recovery criteria,even in the absence of extensive quantitativedata, so long as the criteria are based on prob-abilities of persistence over a specified timeand area. As with any recovery criteria, thetimeframe chosen for evaluating populationviability will require value judgments, butdecisions based on estimates of extinction riskhave the advantages of being transparent andallowing comparisons across species.

In addition, the 3R framework—resiliency,redundancy, and representation (see Box 2)—provides a science-based approach to specify-ing recovery criteria for a species rangewideand considers multiple aspects of recovery. Itallows for genetic and ecological diversity inpopulations large enough for resilience underchanging environmental conditions, providingthe redundancy needed to safeguard a specieswhen catastrophic events occur. Using the 3Rframework can lower extinction risk by pro-tecting populations of appropriate size, geneticdiversity, demographic mix, and geographicdistribution. The 3Rs are often incorporatedinto conservation plans developed at thespecies and rangewide level (see Box 10), andthey can be specified in terms that managerscan use on the ground, such as acres, individu-als, or populations in particular locations andspatial configurations.

Nevertheless, the 3R framework alone doesnot provide sufficient guidance for speciesrecovery. For example, representation canmean different things. In the Services’ view,



Box 9. Biological Scales for Conserving Habitat

When estimating the area of habitat needed for species recovery, conservationmanagers should consider habitat needs at three scales:

Individual organism scale: The area needed to provide the resources and phys-ical conditions required for an individual organism to survive and reproduce.

Local population scale: The area needed to support a population large enoughto persist despite short-term inbreeding effects and periodic threats such asdrought, wildfire, and disease.

Geographic range scale: The areas required by multiple local populations sothat different populations are dispersed and will not all be affected by andrespond in the same way to periodic threats such as drought, wildfire, and dis-ease.

representation is important in the sense that aspecies’ genetic diversity should be conserved;other groups argue that species should be con-served across geographic areas representative oftheir historical ranges. Similarly, resiliencymight require population sizes that are onlyminimally viable, or it might require larger,ecologically effective populations (see Box 11).Moreover, two populations technically amountto redundancy, but are the two populations farenough apart that they are not equally vulner-able to localized threats, such as a wildfire ordisease outbreak? In practice, it is difficult tojustify appropriate thresholds for the 3Rs, andit is not yet clear how to translate them into aspatially explicit conservation strategy.

Strengthening the scientific foundation ofthe 3R principles would considerably improverecovery criteria. We strongly encourage sci-entists to work with the Services and otheragencies responsible for implementing theESA to more clearly articulate the 3R princi-ples, paying special attention to recentadvances in population ecology, conservationgenetics, and the role of biodiversity in sus-taining species’ habitats at the ecosystemlevel. Conservation managers need more user-friendly scientific methods and tools that takeboth species biology and extrinsic threats intoaccount to develop integrated measures ofextinction risk. Such methods should allow forassessing the consequences of environmentalchanges or management actions that alter

landscape patterns (resulting, for example, inhabitat loss or restoration), thereby helpingmanagers integrate implementation of ESAsections 7, 9, and 10 into recovery actions.The methods also should allow for evaluatingall types of decline (including populationdecline and loss, habitat loss, and rangedecline) due to threats that conservation man-agers consider when deciding whether to delista species.

USING CLIMATE-SMARTCONSERVATION STRATEGIES

President Obama’s Climate Action Plan(released by the White House in June 2013)directed federal agencies to increase theresilience of ecosystems in an era of climatechange, creating opportunities for improvingESA implementation. For most species in theUnited States, the growing threats associatedwith climate change are more diffuse, lesswell documented, and farther in the futurethan other major threats (see Figure 4), andconservation managers will need more proac-tive conservation strategies to help speciesadapt. Ironically, smart management mightrequire taking greater risks with some of therarest species because they can be the mostvulnerable to extreme climate-related eventsor to total loss of suitable habitat. Managerswill need to determine the best climate



Box 10. The 3Rs and Northern Spotted Owl Recovery

The northern spotted owl was listed as threatened in 1990, primarilybecause of the loss and fragmentation of old-growth forest habitat in thePacific Northwest. In developing the conservation strategy for the owl, sci-entists drew on the fields of population viability analysis, island biogeogra-phy, and other fundamental aspects of conservation biology. They used thefollowing guidelines:

• Species widely distributed across their potential range are less at risk thanspecies with more restricted ranges because they have multiple local pop-ulations whose growth rates and responses to threats can vary (redun-dancy and representation).

• Large patches of habitat supporting many individuals are more likely tosustain populations than small patches because large populations are lesssubject to the adverse effects of inbreeding and catastrophic events(resiliency).

• Populations in habitat patches that are in close proximity—or where theareas between habitat patches resemble suitable habitat—are less at riskbecause it is easier for individuals to disperse and recolonize (resiliency).

• Long-term sustainability for a species requires evaluating its demographicprocesses at three spatial scales: the individual territory, the local popula-tion, and the collection of interacting populations (redundancy and repre-sentation).

Northern spotted owl in Pacific Northwest old-growthforest.Photo credit: Courtesy of Resources for the Future.

change adaptation strategies for listed specieson a case-by-case basis. Here we discuss andrecommend several options that can beapplied within the framework of the ESA.

Increasing HabitatConnectivity

Conservation managers, policymakers, andother stakeholders need to conserve naturalhabitats and increase habitat connectivityacross large areas. When people modify naturalhabitats, for example by clearing land for farmsand urban development, the remaining habitatpatches are typically much more fragmentedand disconnected than they would be undernatural conditions. Habitat fragmentationimpedes species’ natural movements acrosslarge areas by isolating individuals and popula-tions. Increasing connectivity among frag-mented habitats benefits a wide variety ofspecies because it facilitates their naturalmovements. Habitat fragmentation is a leadingcause of species decline and extinction aroundthe world, and it is a major component of thehabitat degradation that commonly threatenslisted species in the United States (see Figure4). As habitats have become more fragmentedand scientific evidence has accrued, a broadconsensus has emerged that natural resourcemanagers need to substantially increase con-nectivity among terrestrial, freshwater, coastal,and marine habitats, for example by maintain-ing and restoring habitat corridors and remov-ing dams from rivers. Climate change addsurgency to the need to facilitate the naturalmovement of species as they attempt to keeppace with rapidly shifting climate conditions.

Reducing Other NonclimateStressors

Reducing impacts from other nonclimatestressors—such as exotic invasive species,pollution, atypical fire regimes, and overex-ploitation—will help many native species bemore resistant and resilient to climatechange. There is increasing evidence thatmanaging these nonclimate stressors is essen-tial to help species adapt to climate change.Managers who adopt these strategies are see-ing positive results for ESA-listed speciesand other imperiled species in a variety ofecosystems.

Integrating Climate Changeinto Vulnerability Assessmentsfor Listed Species

Conservation managers should more thor-oughly integrate climate change into vulnera-bility assessments for listed species. Many toolsare available. Both the International Unionfor Conservation of Nature and the U.S.National Wildlife Federation, in collaborationwith FWS, have recommended a three-factorframework for assessing species’ vulnerabilityto climate change: (1) the species’ exposure toclimate change (based on the extent of pastand projected future climate change); (2) thespecies’ biological sensitivity (using physiolog-ical or ecological studies or long time seriesdocumenting species’ responses to climatevariability); and (3) the potential adaptivecapacity of the species and their habitats. Onestudy of 16,857 birds, amphibians, and coralsfound that only when a species was vulnerable



Box 11. Ecologically Effective Populations as a Recovery Criterion

Conservation researchers and practitioners often distinguish between recovery criteria definedstrictly by demographic considerations, such as minimum viable population sizes, and criteriadefined by ecologically functional roles, such as ecologically effective population sizes. Anecologically effective population size for a species is the population size below which thespecies is so rare that it cannot perform one or more ecosystem functions, such as predationor seed dispersal. Without ecologically effective populations in ecosystems, critical interac-tions among species are lost, and overall biodiversity can decline. This is especially true forhighly interactive species, such as top predators like wolves.

Setting recovery criteria to achieve ecologically effective population sizes departs from howthe Services have historically administered the ESA, and it could be politically controversial.Moreover, quantifying such criteria might be difficult because it would require extensive eco-logical analysis. Nonetheless, scientists generally agree that conserving ecosystems that sup-port endangered and threatened species requires conserving ecologically effective populationsof species that have key functional roles in those ecosystems. To conserve ecologically effec-tive populations of listed species, recovery plans would need to address the species’ func-tional roles in ecosystems as well as the genetic diversity, resilient population sizes, and geo-graphic distributions needed to sustain those functional roles.

Gray wolf.Photo credit: Gary Kramer, U.S. Fish and WildlifeService.

in all three regards—with high exposure toclimate change, high biological sensitivity,and low adaptive capacity—was it at high riskdue to climate change. Species that are rela-tively insensitive to climate shifts or have anatural suite of adaptation options will likelybe climate resistant or resilient even if climaterapidly changes. In light of uncertainties aboutclimate futures for particular species, ongoinglearning about management options in arapidly changing environment is especiallyimportant. The Services’ 5-year reviews oflisted species should consistently include judg-ments as to whether recovery plans adequatelytake climate change into account and recom-mend adaptive management actions to betteraddress climate change.

Conservation managers can sometimesassess species’ vulnerability to climate changeeven without species-specific information bycharacterizing the projected climate changeaccording to more generic metrics such aschanges in temperature and precipitation, cli-mate variability, and extreme weather events.Managers can use such approaches to identifycontinental-scale gaps in protected areas andin connectivity among habitat areas.

Protecting Future SuitableHabitats

Conservation managers, policymakers, andother stakeholders will also need to protectareas that are projected to become suitablehabitat for listed species as climates change.Unfortunately, modeling tools do not cur-rently provide high consistency among projec-tions: different biological models producelarge differences in results. For any givenspecies, carefully designed regular surveys out-side its range might indicate the areas that it islikely to move into. Managers could integratethe surveys into adaptive management plans.Although conducting such surveys might seemdaunting, managers can use species distribu-tion models as a first step to search for poten-tial new areas that are outside of species’ cur-rent ranges but might become climaticallysuitable.

Using Assisted Colonization

Actively helping species move beyond theirhistorical ranges to areas that are projected tobe more climatically suitable has been vari-ously called assisted colonization, transloca-tion, relocation, or migration. Conservation

managers will need to consider using thisapproach more frequently. The ESA permitsit (ESA secs. 3(3), 10(a)(1)), and FWS pro-grams have already helped establish new pop-ulations of a number of species, including theCalifornia condor in Arizona and the graywolf in Idaho and Wyoming (both within thespecies’ historical ranges) and new popula-tions of the Pahrump poolfish outside of itshistorical range in Nevada. FWS has alsointroduced Guam rails to two Pacific islandswhere they never occurred before, Rota andCocos.

Assisted colonization can be expensive, andit can fail. Theoretical models for predictingclimate suitability typically harbor too muchuncertainty to be used alone, but they canserve as a useful first step. The differencesamong model outputs can be used to definethe likely range of possible futures and pointto areas for further study as potential assistedcolonization sites.

Conservation managers should consider notonly the likely effectiveness of assisted colo-nization for the species that could be relocatedbut also the potential impacts on the ecologi-cal community at the colonization site.Assisted colonization might be most appropri-ate for species that are highly sensitive to cli-mate change, have low dispersal ability (sothey are at high risk of extinction), are weakcompetitors and poor predators (and thereforeunlikely to be invasive species or to otherwiseharm the ecological community), and can beeasily and inexpensively established as newpopulations.

Engineering Habitat

Conservation managers can sometimes designand create entirely new, functional ecosystemsin previously degraded areas. For listed specieswith very small ranges and narrow habitatrequirements, conservation managers mightchoose to create new habitats and perhapseven new ecological communities that are bet-ter adapted to future climate conditions. Likeassisted colonization, habitat engineering isrelatively expensive, and proposed projectswould need to withstand scientific and publicscrutiny. Geographic regions like Californiathat already have multispecies HCPs associ-ated with large tracts of land might have suffi-cient flexibility to change land use designa-tions and implement habitat engineeringprojects to improve recovery prospects forsome species.



EVALUATING AND DEVELOPINGECOSYSTEM-BASED APPROACHES

The large numbers of endangered and threat-ened species and limited resources for recov-ery have prompted renewed interest in mov-ing beyond single-species management andfinding more efficient, ecosystem-basedapproaches to conservation planning. Onesuch approach is to focus management effortson surrogate species that simultaneously ben-efit multiple listed species; another is to use“coarse ecological filters” to identify andmanage ecosystems rich in listed species.

Using Surrogate Species

One species can serve as a conservation surro-gate for another if the species are closelyrelated or have similar ecological require-ments, biological traits, or responses to envi-ronmental change; if the species are interde-pendent, such as predator and prey; or if thesurrogate species is an umbrella species, withbroad ecological requirements or geographicranges that include those of multiple species ofconcern. The FWS Strategic HabitatConservation approach and LandscapeConservation Cooperatives use surrogatespecies in their conservation planning process,based on the premise that surrogate speciesrepresent the habitat and/or managementneeds of larger groups of species.

However, surrogate approaches to managinglisted species are not well supported byresearch. Studies have generally found poorcorrespondence between surrogates and targetspecies in terms of biological traits, presenceand abundance, and patterns of decline.Selection of conservation sites based on onetaxonomic group rarely represents othergroups well, and the degree of spatial overlapbetween groups is idiosyncratic. FWS will testits surrogate species approaches by evaluatingthe underlying assumptions and monitoringboth the surrogate species and the targetspecies. In practice, this might require a returnto more intensive species-specific manage-ment. Moreover, setting recovery criteria andevaluating progress toward recovery will stillbe required for all listed species.

Nonetheless, if appropriate surrogates can befound, using surrogate species to manage forlisted species could allow conservation plan-ning without full knowledge of every speciesor ecosystem element, and it could facilitatedecisionmaking within policy- and manage-

ment-relevant timeframes. Conservation man-agers have already used surrogates in a widerange of situations, including systematicreserve selection, forest management, andecosystem management and monitoring, andresearchers continue to explore new methodsto identify surrogate species. But surrogateapproaches to managing listed species needmore evaluation, and managers should becareful only to implement approaches that arescientifically credible.

Using Coarse Filters

Conservation managers might be able to movebeyond traditional species-by-species recoverystrategies by using ecosystem-based coarse fil-ters to target geographic concentrations—orhotspots—of listed species (Figure 3). Coarsefilters are broad characteristics of a naturalenvironment, much like the cues used by nat-uralists to generate lists of expected species ina particular habitat. They are easily measuredand often based on existing information suchas satellite images, digital elevation models,and weather station data. As such, coarse fil-ters are simply another kind of surrogate. Theyare environmental cues—such as dominantvegetation and plant community types identi-fied by satellites—that researchers can use topredict the occurrence of species in a particu-lar habitat or ecosystem. Importantly, coarsefilters are defined independently of any partic-ular species’ habitat needs: they are meant tocapture the needs of entire groups of species.

The coarse-filter approach has rarely beentested and only with mixed results. Coarse fil-ters have often led to overestimating the pres-ence of species in a region of interest.Furthermore, they have worked better forspecies that are small and abundant than forones that are large or rare—the ones morelikely to be of conservation concern.

Nonetheless, researchers can develop coarsefilters that identify overall patterns of biologi-cal diversity or concentrations of rare species,and this might increase the efficiency of man-agement efforts to recover listed species. Bycombining information about the geographicdistribution of listed species (Figure 3), theirtaxonomies and life histories, the portfolio ofthreats that triggered their listing, and the bio-logical and physical features of the regionswhere they occur, researchers might developcoarse filters that reliably identify key ecosys-tem units. Conservation managers could thenfocus recovery efforts on those units.



There is evidence in the scientific literaturethat such a strategy has merit, and managersare already taking similar approaches. On theisland of Kauai in Hawaii, FWS has grouped48 listed species based on common factorssuch as shared threats and types of habitat,focusing restoration broadly on habitats andecosystems rather than solely on individualspecies in their last few known locations. Suchthinking is also behind a push for species con-servation across large landscapes under collab-orative adaptive management. For example,the Forest Service has adopted a new planningrule governing biodiversity conservation onlands that it administers based largely on acoarse-filter strategy.

Coarse filter approaches appear to holdpromise for designing management actionsdirected at recovering listed species, althoughthese approaches are still hypothetical. Testingthe hypotheses will require species-level moni-toring to gauge species recovery.

PROTECTING AMERICA’SHERITAGE

“The public is (and the sportsman ought tobe) just as much interested in conservingnon-game species, forests, fish, and otherwild life as in conserving game.” These pre-scient words are as true today as when AldoLeopold wrote them 43 years before Congressenacted the ESA.

As Leopold knew, America’s heritage andidentity are bound up with wild, untamedlandscapes—with the American frontier, fromthe first settlement at Jamestown to the last ofthe great migratory bison herds on the GreatPlains—America’s Serengeti, now lost to pos-

terity. To prevent further loss, conservation-ists formed great systems of public lands andpassed laws designed to protect America’sremaining native species—and with them apiece of what it means to be American. Chiefamong those laws was the ESA.

The ESA has worked remarkably well toshield hundreds of species in the UnitedStates from extinction, and it remains one ofthe country’s strongest environmental laws. Itis also a flexible statute that permits consid-erable innovation in its implementation.Innovation will be key to the ESA’s futuresuccess because the threats to at-risk speciesare pervasive and persistent, many listedspecies are now conservation reliant, and cli-mate change will continue to shuffle the mixof species in ecological communities, increas-ing both extinction risk and managementuncertainty. At the same time, without a dra-matic shift in public priorities, governmentfunding for species recovery will likelyremain insufficient.

Accordingly, we have identified six broadstrategies to increase the effectiveness of ESAimplementation (Box 12). By adopting thesestrategies, conservation managers, policy-makers, scientists, and the public can use theESA more effectively and efficiently to savespecies at risk.

For Further Reading

Association of Fish and Wildlife Agencies(AFWA). 2011. State Wildlife Action Plans:Shaping National Fish and WildlifeConservation. AFWA. Washington, D.C.

Baur, D.C. and W.R. Irvin, editors. 2010.Endangered Species Act: Law, Policy, andPerspectives, second edition. American BarAssociation, Section of Environment,Energy, and Resources. Chicago, IL.

Bottrill, M.C., L.N. Joseph, J. Carwardine, M.Bode, C. Cook, E.T. Game, H. Grantham,S. Kark, S. Linke, E. McDonald-Madden,R.L. Pressey, S. Walker, K.A. Wilson, andH.P. Possingham. 2008. Is ConservationTriage Just Smart Decisionmaking? Trends inEcology and Evolution 23: 649-654.

Glick, P., B.A. Stein, and N.A. Edelson, edi-tors. 2011. Scanning the ConservationHorizon: A Guide to Climate ChangeVulnerability Assessment. National WildlifeFederation. Washington, D.C.

Goble, D.D., J.A. Wiens, J.M. Scott, T.D.Male, and J.A. Hall. 2012. Conservation-reliant species. BioScience 62: 869-873.

Goble, D.D., J.M. Scott, and F.W. Davis, edi-



Box 12. Strategies to Increase the Effectiveness of ESAImplementation

• Establish and consistently apply a system for prioritizing recovery funding tomaximize strategic outcomes for listed species

• Strengthen partnerships for species recovery

• Promote more monitoring and consistently implement and refine approachesfor adaptive management

• Refine methods to develop recovery criteria based on the best availablescience

• Use climate-smart conservation strategies

• Evaluate and develop ecosystem-based approaches that can increase the effi-ciency of managing for recovery

tors. 2006. The Endangered Species Act at 30,Volume I: Renewing the ConservationPromise. Island Press. Washington, D.C.

Joseph, L.N, R.F. Maloney, and H.P.Possingham. 2009. Optimal Allocation ofResources among Threatened Species: AProject Prioritization Protocol. ConservationBiology 23: 328-338.

Male, T.D. and M.J. Bean. 2005. Measuring andUnderstanding Progress in U.S. EndangeredSpecies Conservation. Ecology Letters 8: 986-992.

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Acknowledgments

Funding for this project was provided byCooperative Agreement 12-CA-11221633-096between the USDA Forest Service and theEcological Society of America. Other fundingand services were provided by Resources forthe Future. The authors wish to thank HutchBrown, USDA Forest Service, for editing thepaper. We would like to thank Kevin Bryanand the Meridian Institute for facilitatingworkshops that led to this paper. We alsothank Cliff Duke, Jennifer Riem, and JillParsons at the Ecological Society of Americafor logistical support; and we thank JoshLawler for providing species turnover data forFigure 7. The views expressed in this paper donot necessarily represent the views of the U.S.government or any of its departments. Any useof trade, product, or firm names is for descrip-tive purposes only and does not imply endorse-ment by the U.S. government.

About the Scientists

Daniel M. Evans, AAAS Science &Technology Policy Fellow, Research andDevelopment, USDA Forest Service,Washington, DC 20250Judy P. Che-Castaldo, National Socio-Environmental Synthesis Center, Universityof Maryland, Annapolis, MD 21401Deborah Crouse, US Fish and WildlifeService, Falls Church, VA 22041Frank W. Davis, National Center forEcological Analysis and Synthesis, Universityof California, Santa Barbara, CA 93101Rebecca Epanchin-Niell, Resources for theFuture, Washington, DC 20036Curtis H. Flather, Rocky Mountain ResearchStation, USDA Forest Service, Fort Collins,CO 80526R. Kipp Frohlich, Florida Fish and WildlifeConservation Commission, Tallahassee, FL32399Dale D. Goble, University of Idaho, Collegeof Law, Moscow, ID 83844Ya-Wei Li, Defenders of Wildlife,Washington, DC 20036 Timothy D. Male, Defenders of Wildlife,Washington, DC 20036



Lawrence L. Master, NatureServe, Arlington,VA 22203Matthew P. Moskwik, Integrative BiologySection, University of Texas, Austin, TX78712Maile C. Neel, Department of Plant Scienceand Landscape Architecture and Departmentof Entomology, University of Maryland,College Park, MD 20742Barry R. Noon, Department of Fish, Wildlife,and Conservation Biology, Colorado StateUniversity, Fort Collins, CO 80523Camille Parmesan, Marine Institute,Plymouth University, Plymouth, Devon, UKPL4 8AA; Integrative Biology Section,University of Texas, Austin, TX 78712Mark W. Schwartz, Department ofEnvironmental Science and Policy, Universityof California, Davis, CA 95616J. Michael Scott, Department of Fish andWildlife Sciences, University of Idaho,Moscow, ID 83844Byron K. Williams, The Wildlife Society,Bethesda, MD 20814

Layout

Bernie Taylor, Design and layout

About Issues in Ecology

Issues in Ecology uses commonly understood lan-guage to report the consensus of a panel of scien-tific experts on issues related to the environment.The text for Issues in Ecology is reviewed for tech-nical content by external expert reviewers, andall reports must be approved by the Editor-in-Chief before publication. This report is a publica-tion of the Ecological Society of America. Noresponsibility for the views expressed by theauthors in ESA publications is assumed by theeditors or the publisher.

Editor-in-Chief

Serita Frey, Department of Natural Resources& the Environment, University of NewHampshire, [email protected]

Advisory Board of Issues inEcologyJessica Fox, Electric Power Research InstituteNoel P. Gurwick, SmithsonianEnvironmental Research CenterClarisse Hart, Harvard ForestDuncan McKinley, USDA Forest ServiceSasha Reed, U.S. Geological SurveyAmanda D. Rodewald, Cornell Lab ofOrnithologyThomas Sisk, Northern Arizona University

Ex-Officio AdvisorsValerie Eviner, University of California, DavisRichard Pouyat, USDA Forest Service

ESA StaffClifford S. Duke, Director of ScienceProgramsJennifer Riem, Science Programs Coordinator

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