1 BiOlOgi , ( Vol 83. No 3. pp. 247 25 . 1998 I 1997 Published bs Llsevier Science Ltd Al) rights reserved Printed in Cireat Britain SOO 0 6-3 2 07(4 7)0 0081-5 0006-32117 98 $19.181 « (Jill L SI \ IF I< FLAGSHIPS, UMBRELLAS, AND KEYSTONES: IS SINGLE-SPECIES MANAGEMENT PASSE IN THE LANDSCAPE ERA?

Daniel Simberloff Department of Biological Science, Florida State University. Tallahassee. Florida 323filb.

Abstract needed. Thus, SOIIIC See CCOS.I'Venl Man- agement Because it is so difficult to monitor and manage every as a Trojan horse that would allow continued environmental name of tinnier,' resource aspect of biodiversity, several shortcuts have been pro- destruction in the management. posed whereby we monitor and. or protect single species. The recognition that sothe ecosystem% ho re keysione The indiewor species concept is problematic because there .species whose activities gi wern the well-being id many ii no consensus on what the indicator is supposed to indi- species suggests an appniach that min unite cate and because a is difficult to know which is the best other the best ecosystem management. V indicator species even when ice agree on what it should features of single-species and that indicate. The umbrella species ( a species that needs such we can iilentily keystone species and the inechanisinN came them to how v1(11 Ividc-lallgMg ic e 11 .01/h/ large tracts of habitat that saving it will automatically . 1111pOCIA , save many other species, seems like a better approach. ahnOS/ certainly derive information on tile lunclioning of although men WhCaler 1711111y other species will reallyfall the entire ecosystem that would be foetid in its manage- appro- under the umbrelhi is a matter of faith rather than ment. Some keystone species themselves may be priate targets for management, even when researc 'h. intensive management of an. indicator or an hut, they are not, umbrella specie) tor eNample, by transplant or supple- our understanding of the ecosystem will be .greatly , non - mental feeding is a contradiction in terms because the increased. Keystone species Mar 1101 he a panacea, (Ter. knoll him l est of the community 10 be miliewed or protected does WC 1101 •I'CI many ecosystems have keystone .species, and the that lead to their not receive such treatment. .4 flagship .s pecies.1101111011.1* evreriment. identification are often very , ditirallUllie large vertebrate. is one lhal can be used to difficult. I /99\ .Pubbsbed - : anchor a conservation campaign because it arouses public by Ilsevier Science Ltd. rights reset I ea interest and .sympathy. but a flap/lip need not be a good indicator or umbrella. And consermtion flagship spe- Keywords: adilptiVC 111:111 42011C111.. CCOS stem hea It h. i ie.% is often very expensive. Further, management regimes ecosystem management, endangered species. flagship of t wo ,flagship species can conflict. Ecosystem manage- species. indicator species. keystone species, landscape ment. open on a landscape scale. is a proposed solution ecology. umbrella species. - to Prublems of.vbigle species management. Keep the Ce0- SySICI11 healthy. according this view. and component species will all thrive. 1 lowever, cwiservationisis have concerns about ecosystem management. First, it IS var- INTRODUCTION iously Mined, and many definitions emphasife the com- modities ecosystems provide for humans rather than how In an era of burgeoning conservation needs and humans can protect ecosystem.s. Second. the term 'eco- tightening budgets. an increasingly loud claim is that the system health ' is ill-delmed and associated with an out- scope of conservation management must be expanded . moded, superorganismic vieW (!i the ecosystem. Third. to achieve economies of scale and efficiency. According it us istem Managelnelll seems focused on processes and so to this view, managing populations of particular species would appear to permit losses ofspecies so long as they of interest will lead us to fall further and further behind ( /id not greatly allect processes like nutrient-cycling. in meeting the challenge of preserving biodiversity. as Fourth, ecosystem management is °Pen implemented by more and more species fall below a threshold of adaptive management. This may make it difficult to study imperilment and funding in no way keeps pace with the underlying mechanisms driving an ecosystem and to their individual needs. The only way to deal with this know when an entirely new management approach is challenge is then seen to be to manage at least entire ecosystems. if not whole landscapes. b■ unified !'resent address: 1)epartnient oF Ecolouv & methods designed to save all their inhabitants at one - I:volution:try . t..itiversitv of I ennessee. K u t viIIc. TN 1799(,. t time. 248 D. Siniberlolf

However. the precise objectives of such methods have Criteria for choosing such indicator species are very not often been articulated beyond vague aims to 'pre- controversial ( Landres al., 1988). at least partly serve the environment' or to 'maintain biodiversity'. and because of confusion over what the indicator should it is not always clear exactly how management of such indicate. Generally, we want an indicator to indicate the high-level entities as ecosystems will supersede manage- 'health' of the system, but different persons view differ- ment of their component species. This paper attempts to ent things as constituting health. For example. whether understand the specific goals of management at the species richness alone. independently of species' identi- ecosystem level and higher. and also to compare pro- ties. contributes to the functional health of a community posed procedures to those of traditional management or ecosystem is hotly debated and currently under focused on individual populations and species. intensive study ( Baskin. 1994: Tilman and Downing. The examples used to elucidate these matters will be 1994). For some persons. species richness itself eco- primarily North American. largely because of the system health - the tacit goal of all conservation should author's familiarity with conservation on that continent. be species richness, and. ipso hiu.to, a rich community is A large fraction of the discussion relates to management a healthy one. For still others, structural diversity and actions aimed at satisfying the Endangered Species Act aspects of cunclion (like nutrient c■cles) are the sine qua (1973) of the United States. This legislation has become non of health. independently of species richness or the major vehicle for protecting biodiversity in the Uni- composition. The reductio alkairdum of this confu- ted States (Mann and Plummer. 1995). It is reactive. sion of goals is the proposition (Noss. 1990) that we rather than proactive, and explicitly targets species and should monitor irtuall■ everything as indicators • a populations, in that it specifically provides protection large group of species. dominance-diversity curves. for species (and. in certain instances, some populations canopy height dkersny. percent co' er. nutrient cycling rather than entire species) that are already felt to be and predation rates. etc. The problem is that this full set doomed to extinction if new action is not taken to of indicators lea% es nothing to he indicated. as opposed redress their decline. However, often the Act has been to measured directl■. Of course the absence of resources invoked to save entire ecosystems because, under some to do all this measurement was the raison d'jtre for circumstances, it provides for protection of the habitat indicator species in the first place! of an endangered species, and that habitat includes the Even if we concede at the outset that all we want the biotic as well as the abiotic habitat. Thus, a recent indicator species to indicate is the presence and popula- interpretation by the Supreme Court says that the Act tion trends of a group of other species in a communit■ can prevent habitat destruction (Baker. 1995) if such of interest, it is not so obvious how to choose the best destruction 'harms' endangered species or populations. species for this purpose. At the ■er least, we would The Endangered Species Act also mandates that, in need a pilot study measuring co-occurrence patterns addition to calling a halt to most activities causing the and correlations of population fluctuations, plus ease of decline of an endangered species. a management plan monitoring. for all species in the group. To my knowl- must be produced that will rehabilitate the species by edge. such a pilot study has never been attempted. The bringing its population size above the threshold of scale of observation would also he important for an endangerment. These management plans have become indicator ( Mee and Carroll. 1994: Weaver. 1995). the testing ground for various ideas on how and at what Species like the large vertebrates discussed below might . level to conserve nature in the United States. be excellent indicators for other species that require massive, continuous tracts of habitat, but they may not Indicator, umbrella, and flagship species be good indicators of species such as insects that might Because monitoring and managing all aspects of biodi- do very well in a landscape fragmented into small pat- versity that might interest us (including species richness ches, so long as the habitat of the patches was appro- and composition. physical structure, and processes) are priate. so difficult, a variety of shortcuts have been proposed Finite de inieux. often vertebrate species are chosen as whereby attention is focused on one or a few species. indicators simply because they are so charismatic that a The most venerable of these approaches is that of the manager feels obliged to monitor them anyway and indicator species. Managers use indicators for two dif- nourishes the vague hope that such a 'flagship species' ferent reasons—first because their presence and fluctua- (see below) will fortuitously reflect the health of the tions are believed (or hoped) to reflect those of other entire system. For example. the US Forest Service is species in the community, and second because they are mandated to use 'management indicator species' to believed to reflect chemical and/or physical changes in assess the impacts of any proposed management proce- the environment (Landres et cd., 1988). However, there dure on the system as a whole and chose the northern is no reason why a species particularly sensitive to che- spotted owl Strix occidentalis caurina to serve this role mical pollution, for example, need necessarily reflect the for the Pacific Northwest region. The specific grounds status of a large number of other species, so I will were that the owl (1) was on the threatened species list restrict my consideration to the first type of indicator for Oregon, (2) is a species of special interest (because it species. is an attractive bird that typifies a beautiful forest type), Single-species and ecosysion ,nanagement 249 and (3) represents other species that depend on old The legal status of the owl as an indicator species growth (Lee. 1 985). There is no inherent reason why the under the National Forest Management Act has led to fact that this bird is threatened and of special interest an undue focus on This particular species to the exclu- would mean that its fate reflects those of other species. sion of all that it is supposed to indicate. For example, It is convenient for the Forest Service to assume that it logging industry representatives frequently suggest does. because they would monitor it anyway because of management procedures specifically targeted at owls, 1 its interest and threatened status. like moving or feeding them, artificially enhancing their The fact that few data support the indicator function prey density, or providing added shelter. in order to of the owl need not mean its choice is completely mis- 'boost their populations so that logging quotas can be guided. The rationale is that the owl is closely tied to raised (e.g. Craig. 1 986). The Forest Service proposed old-growth rain forest, the amount of this habitat has moving owls from site to site. Lost in such suggestions is been drastically reduced by logging, and other species the recognition that single-species management of an requiring this habitat are likely to be threatened also. indicator species is a self-contradiction ( Simberloff. However, because the other species are not charismatic 1 987). After all, if the species' status is artificially vertebrates. they have not been studied enough for us to improved, it no longer indicates the status of all the know how threatened they are. Because the owl requires species it is supposed to represent. Would we also add such large amounts of old-growth for survival and food or shelter for other birds, mammals, amphibians. reproduction (c. 800 ha per pair in the middle of its and insects of the old-growth forest, and move them range ISimberlofr. 1 9871). saving enough of this habitat around? I will return to this point below. for the owl would almost surely save enough of it for A similar example is that of the red-cockaded wood- other species. Thus, the spotted owl would serve not pecker Picoides horeoli.s of the US Southeast. This bird only as an indicator but as an 'umbrella species' (Shra- resides primarily in forests of longleaf pine Pinu.c pubis- der-Frechette and McCoy. 1 993). a species with such Iris. which have declined largel■ because of logging over demanding habitat requirements and large area the last 150 years from about 28 million ha to only MO requirements that saving it will automatically save many ha of old growth and 4 million ha of second growth other species. Wilcove (1993) has called wide-ranging (Simberlofr. 199,1a). Most of the latter differs substan- vertebrate species such as the owl 'coarse filters' and tially from the primary forest. notably in the relative suggested that their preservation would save entire eco- youth of the oldest trees and the composition of the systems. ground cover. One of the first listed endangered species Perhaps this reasoning is correct, but. without many in the US. this colonial woodpecker is unique among more supporting data. we can question the utility of' the regional woodpeckers in excavating its cavities in old. spotted owl as an indicator or umbrella species. First. diseased trees. there is 'even some controvers■ about the extent to The precipitous decline of this striking bird has finally which the spotted owl absolutely requires old-growth led the Forest Service to organize its management of 11 forest (e.g. Mickey. 1 994). although the great majority national forests totalling 1 3611)00 ha around a recovery of qualified workers believe that it does. Second, plan for the red-cockaded woodpecker (US Department although other threatened species are apparently of Agriculture. 1 995). These I I forests have 31 other restricted to old-growth forest in the Northwest. it is for species listed as endangered or threatened tut: half ani- l'rum certain that they need the same parts of the forest mals and hall' plants) and 71 proposed for such listing. as the owl does, and. although saving the owl should The reason for the precarious status of almost all these help save many of them, it will not save them all. For species is either that the habitat has simpl■ been example. the exact status and habitat requirements of destroyed in one fell swoop or that it is gradu.ill■ chan- three amphibians of special concern are not well known ging because the tires that frequently swept these forests (Welsh. 1 990). Two of these require rather specialized during the growing season are no suppressed. Because aquatic microhabitats that, although often associated the authors of the proposed woodpecker management with habitat used by spotted owls. are obviously not scheme envision both more mature longleaf pine forest identical to it. We might also ask about the 6000 insect (albeit with a time lag) and more growing-season fires. and other arthropod species typical of' the old growth. they see almost no disadvantages and many potential Certainly some old-growth specialist arthropods would benefits for all these other species. No substantial study be protected by large reserves for the owl. but the pre- supports any of these contentions, and only four pages cise habitat requirements of most species are very of the management plan are devoted to this issue. as poorly know ( Lattin. 1993). Unless additional coastal opposed to hundreds that discuss timber production. habitat were added, enormous proposed reserves for the For example. another species typical of longleaf forest owl would not provide adequate protection for anadro- that has undergone a great decline. Sherman's fox mous fish or the marbled murrelet Brachyramphos mar- squirrel Sciurus niger shermani. will be restricted from 'proration, another threatened bird (Franklin. 1994), using some cavities that W...ill he preserved in optimal both or which depend on old-gi'owth forest but for only condition for the woodpecker by a niechanical des ice part of their life history. preventing enlargement. For most species of special 250 Sinther concern, much less is known about their biology, so the for the new. 12001) ha Panther National Wildlife impact of the management plan cannot be guessed with Refuge. Costs have included a journal ( Cool) devoted much assurance. solely to this animal, extensive field management pro- The Florida panther Fells concolor corn i is the quin- jects. and field and laboratory studies. Are the benefits tessential 'flagship species' (Shrader-Frechette and generated by the panther conservation program worth McCoy. I993)—a species that has become a symbol and the costs? Could the funds devoted to it have greater leading element of an entire conservation campaign. conservation benefit if spent otherwise? No significant The panther is identified with Florida (Shrader-Frech- research treats these questions. eue and McCoy, 1993) and has been used as a poster- An irony is that the panther may not survive long animal in both public and private campaigns for even with this expenditure. at least not without success- broader conservation objectives. A disjunct subspecies ful translocation to other regions of Florida (Shrader- of the widely ranging cougar, it is slightly distinctive Frechette and McCoy. 1993: Cox et ill.. 1994). In fact. morphologically and is gravely threatened. Some 40 some might argue that the %ery procedure that has now individuals remain, restricted to undeveloped areas of been adopted to forestall a decline from hypothesized south Florida. among the regions of the US undergoing inbreeding depression kill eliminate the Florida panther the most rapid development and habitat destruction. quickly at least eliminate it as Felts concolor coryi. The main problems for the panther are the dramatic After the discover that one of the two populations decline in its favoured prey animal, the white-tailed deer already contains genes from escaped captive Central or 0(locoileus virginiamts. owing to habitat destruction South American cats ( 0.13rien it a/.. 1990). the federal (Shrader-Frechette and McCoy. 1993) and the frag- government and state ha%e now embarked on a plan to mented nature of remaining panther habitat, which import and release individuals of another F. concolor causes individuals to cross highways, incurring substan- subspecies from Texas to increase effective population tial mortality. It would be no trivial matter to sequester size (Dold. 19951. land sufficient for an increased population. as male home ranges average 550 km= and female home ranges But what happens when the flagship sinks or there is no 300 km= (Cox et al.. 1994). and land in Florida is very flagship? expensive. In fact. although Florida has by far the lar- That the Florida panther might disappear or evolve into gest state fund in the US for purchase of conservation another species leads us to question from yet another lands, the budget could easily be exhausted simply by direction the wisdom of hinging an overall conservation purchases of potential panther habitat. strategy on a single charismatic threatened flagship However. Florida has numerous other threatened species. Suppose the population disappears'? Will public taxa. including 51 other mammal, bird, reptile, and emotional investment in this species turn to despair and amphibian species and subspecies (Shrader-Frechette disenchantment with conservation in general? Would and McCoy, 1993). Of course, panther habitat could not the money have been better spent on a combination serve double-duty. Areas proposed specifically for pan- of conservation projects to preserve other species and ther conservation have at least 24 of these 51 taxa, plus educational programs to teach the lay public about the 29 threatened plant species and subspecies (Cox et al., importance and inherent attractiveness of the myriad 1994). Other species may be even better umbrellas. For less dramatic species that dominate any ecosystem? example. proposed conservation areas for the Florida Worse, suppose a region has no threatened species, black bear Ursus americanus floridanus include more charismatic or mundane, to begin with? This is precisely threatened vertebrates and many threatened plants (Cox the situation in the Alaskan rain forest, such as the huge et al., 1994). Of course. to evaluate the relative merits of (6812 000 ha) Tongass National Forest in Alaska. potential umbrella species and to determine how many Although parts of this region are revered for spectacular of them are needed, we would need a full analysis of the vistas as well as large populations of dramatic animals costs of the proposed purchases, the likelihoods of sur- (such as the grizzly bear. Ursu.v arctos), no one forest- vival of each species in the umbrella. etc. At least the dwelling species qualifies for protection under the latter aspect of the analysis would be extremely difficult. Endangered Species Act. The United States has no law No method incorporating all the potential threats to that specifically protects communities or ecosystems. species survival can currently be used with much confi- Thus, the Endangered Species Act has been pressed into dence. service for this purpose because it protects the 'critical The panther is so charismatic that thousands of habitat' of listed species. and the habitat can be con- Floridians pay $66 annually to have an automobile strued as the biotic habitat, such as old-growth trees for license plate with its picture. These funds go towards the spotted owl, as well as the physical context. It is conservation, as do others generated in various private widely recognized that this approach will not suffice for appeals featuring the panther. On the other hand, the all communities and ecosystems, as exemplified by the attempt to preserve the panther at both state and federal Tongass case, and that what is needed is some sort of levels has been enormously expensive, ca $1.4 million (J. 'Endangered Communities Act' or 'Endangered Eco- Cox. pers. comm.) in addition to land-acquisition costs systems Act' (e.g. Hunt, 1989: Metre and Carroll, 1994). Single-species and ecosystem management 251

But the political climate in the United States makes (Ehrlich et al., 1992). The kite needs high water levels, prospects for passage of such an act, at least one in which increase snail production. On the other hand, the which conservation would take precedence over wood stork Alyeieria americana, reduced to perhaps economic considerations, extremely dim in the near 10 000 pairs by swamp drainage and cutting of the cypress future. trees it favors for nesting. would be facilitated by lower It is an irony that the Endangered Species Act itself is water, which concentrates prey populations (Ehrlich et endangered. and the main reason is anger by a segment al., 1992). The US Fish and Wildlife Service opposed a of the public over use of the Act to sequester large tracts proposal by the Everglades National Park to modify of habitat designated as critical habitat for some Water flow to improve stork habitat on the grounds that endangered species (Mann and Plummer. 1995). In fact. the change would be detrimental to the kite. a lawsuit recently decided by the US Supreme Court In California, the giant kangaroo rat Dipodomys (Babbitt vs Sweet Home) sought to prevent use of the Owens depends primarily for food on non-indigenous Act to protect habitat (and therefore entire communi- plants. and these rodents continually disturb the habitat ties) by stating that Congress had never meant the term to the advantage of these exotics and detriment of 'harm' to a species in the Act to mean destruction of native plants. including the endangered Caulanthus habitat, but only direct killing of an animal or plant, say caldarnicus (Schiffman. 1994). Because the native plants by shooting or burning an individual. The Court rejec- used by the kangaroo rat are now rare or even extinct. ted the narrow interpretation of 'harm' by a 6-3 vote there is no obvious management solution to this ( Baker. 1995). A prime example of anger at this use of dilemma. the Act is' the spotted owl debate, in which it was abundantly clear to all parties that the stakes were not Ecosystem management the spotted owl, which was only a surrogate for the old- Ecosystem management is a suggested solution to the growth forest it inhabits. It was the eventual listing of problems posed by single-species management focused the bird under the Act and the designation of that forest on indicator, umbrella, and flagship. species. This is a as its critical habitat that greatly reduced logging in the fluid concept that has exploded on the resource man- Northwest but also precipitated the crisis surrounding agement scene following a technical session of the the Act. American Association for the Advancement of Science Annual Meeting in 1991 (Swank and Van Lear. 1992). Species conflicts under species management There is no consensus definition of 'ecosystem manage- Single-species management. of flagships. umbrellas. ment' (Grumbine. 1994: Soule. 1994): even the various endangered species. or any others. can lead to the odd US federal agencies all have different working defini- circumstance that management of one species conflicts tions (Morrissey et al.. 1994). Several agencies leg. the with management of another species (Committee on Department of Commerce) even forswear an attempt to Scientific Issues in the Endangered Species Act define 'ecosystem management' explicitly, although [CS1ESA. 1995]). these agencies, as do all the others. see ecosystem man- Ash Meadows. a series of deepwater springs on 20 000 agement as a dramatic new approach that will solve ha of desert uplands near Las Vegas. harbors at least 26 many problems. The excitement seems to be engendered endemic plant and animal species and subspecies. many largely by a feeling that ecosystem management will of which are federally listed as endangered. Their man- produce economies of scale. Single-species management agement needs are not identical. For example. the Ash seems costly and inefficient. Expenses lOr activities such Meadows naucorid Ambrysirc amorgosus is the only as building excluders for potential red-cockaded wood- aquatic insect protected under the Endangered Species pecker holes, moving individuals around, and extensive Act. and its population is still declining because of laboratory and field studies of the physiological ecology habitat alteration to favor the Devil's Hole pupfish of individual species would seem to be limitless as spe- Cyprinodon diaholis (Polhem us. 1993). But the pupfish. cies after species is added to the threatened list. II' we which numbers 200-500 individuals restricted to a single keep the entire ecosystem healthy ( Morrissey et al.. 3 m x15 m pool probably for its entire existence. is 1994). would not populations of all its component unlikely ever to be delisted (Middleton and Liitsch- species automatically be health■? wager, 1994). and management is almost certain always There are common elements in virtually all definitions to favor a charismatic fish over an insect. of ecosystem management. The key feature is a focus on In the Everglades of Florida. management plans for ecological processes rather than individual species two extremely charismatic. federally listed birds are in (Meffe and Carroll. 1994). For some workers, ecological conflict ( Graham, 1990). On the one hand. the Ever- processes are seen as keeping an ecosystem healthy (at glades snail kite Rostrhamus sociahilis plumheus, least in some conceptions of ecosystem health). In other reduced to some 600 individuals by wetland degradation words. the processes are not the valued entities per se. and agricultural and residential development. feeds but the processes are believed to maintain the species almost exclusively on freshwater snails of the genus and communities that are valued ( Bourgeron and Jen- Pomucea and is thus an extreme habitat specialist sen, 1993; Franklin, 1994). However. at the level of D. Junberlqll

implementation and management. the processes them- services that ecosystems pros ide to humans (Grumbine, selves often seem to have become the valued elements. 1994). In other words, humans should manage ecosys- For example. among US federal agencies. many list tems primarily in response to human resource needs. maintenance of processes or functions as either the first The Forest Service and some other US agencies have in goal of ecosystem management or the only goal. And an the past attempted to resolve this conflict by the philo- attempted consensus document (Keystone Center. 1993) sophy of 'multiple use', at least since the Multiple Use produced by representatives of many government agen- Sustained-Yield Act of 196(J ( Kessler ei al.. 1992). The cies and private organizations listed maintaining pro- assumption was that the managed land could serve all cesses as the first aspect of ecosystem management. This purposes. although in practice the human resource focus on processes is seen as a Trojan horse by some needs were greatly emphasited. 13ut this as only an conservation biologists, as will be discussed below. assumption. Now that there is public pressure to pay The emphasis on processes automatically leads to a more attention to protection of other species and com- broad spatial scale with a focus on landscapes. One munities. the validity of the enure multiple-use frame- definition of landscape ecology ( Golley. 1993) is "the work is in question (Wagner. 1994). It may well be that study of how land patterns influence processes -. Of ecosystem management. at least in some ecosystems or course. landscape ecology also answers a growing inter- large parts of them. will ha \ e to serve one or the other est in large-scale phenomena. while it is quite clear that goal almost exclusReiy. It 1,1111pol-tam to state explicitly at least some single-species management can he con- that multiple use may not he possible t Grumbine, 1994). ducted without considering the structure and dynamics A final leature common to many conceptions of of the landscape. Thus, ecosystem management, though ecosystem management te.g. Kessler et al.. 1992: Everett not simply the management version of landscape ecol- et al.. 1993) is that adaptive management (Walters. ogy. is very closely related to the latter discipline. 19X6: Walters and Holling. 1990) will be the scientific Another feature shared by many definitions of eco- basis for it. Adaptive management is essentially project- system management is that it is holistic, a trait seen as as-experiment, and the 1.e■ aspect that seems to attract clearly distinguishing it from single-species manage- many adherents in ecosystem management circles is that ment. This feature might seem trivial- after all. !lutists management goals and methods are changed in the study systems as systems. However, it is important to course of the project. The aegis for adaptive manage- realize that holists are committed to the view that it is ment is that the ellects of a procedure are cry uncertain impossible to understand the components of a system because mechanistic understanding of a system is rather 1990). except as parts of the system. Thus, they would argue poor (Walters and [lolling. This state of affairs that insightful. effective single-species management is certainly obtains for many components of proposed not only expensive and inefficient, but is impossible, plans for managing ecosystems. Adaptive management because the species exists only as part of the ecosystem. has had some successes, as. for example. in some Yet another aspect of ecosystem management in most fisheries in which simply adjusting y'earl' limits in definitions is that humans are part of the ecosystem, or accord with the catch has prevented overfishing. at least of most ecosystems. There are two subtle con- without any detailed understanding of the mechanisms sequences of this view. of the underlying population dynamics (l'olicansky. First. although this point is rarely articulated in sci- 1986). entific publications, this conception of ecosystem man- A contentious aspect of adapti‘e management is agement casts into doubt the very idea of excluding whether the changing procedures and goals really per- humans from selected areas, as somehow antithetical to mit improved mechanistic understanding of the system. the nature ()Ian ecosystem. Of course. this is an extreme Walters and Hulling (1990) contend that adaptive man- view (which is probably why it is rarely written down), agement leads to scientific understanding. but their but the implication is clear that such restricted areas defense of the proposition that this understanding is should play at best a limited role in conservation. The scientific, even if it is not the customary analytical type title of a recent exposition of ecosystem management for oh' scientific knowledge. suggests the contention is con- forests (Shepard, 1994) says it all: "Modern forest troversial. Is an 'experiment' for a short enough time to management: it's about opening up, not locking up-. be considered adaptive (in the ecosystem-management Second, humans use resources, and such resource use sense of subject to modification in the course of the is conceived as a natural process not inherently danger- project) really a scientific experiment? And is there ade- ous to ecosystem health. Biologists and environmental- quate replication and control, especially if the project is ists, if they advocate ecosystem management at all, tend at an ecosystem or landscape scale? Many studies in to see its key goal as maintaining biodiversity (e.g. ecology are called 'experimental' that do not really Meffe and Carroll, 1994). In short, humans should qualify for this status (Underwood, 1990). The impor- manage ecosystems to protect other species and com- tance of this problem for conservation is that the term munities. However, many people, especially in manage- 'experiment' has a scientific cachet and may suggest a ment agencies, have a very different focus (e.g. Overbay, kind of rigor that is, in fact, absent from a management 1992: Jensen and Everett, 1993), namely the goods and scheme. Wiens (1992) has pointed to a distressing lack Single-species and ecosystem nianagement 253 of experiment in landscape ecology. So the combination vation concern could be consigned to oblivion on the of an adaptive management approach in a framework grounds that it is not a part of an ecosystem that is that is often at a landscape scale should force us to pay being managed, or that the ecosystem is just another close attention to whether a proposed plan is scientifi- representative of a type already well-represented in a cally grounded. refuge system. Another problem with adaptive management is that. The absence of a consensus definition for ecosystem with its continual modification of procedures in light of management also worries conservationists, as does the observations, there is no clear stopping point, no fact that many working definitions appear to emphasize moment of truth at which we can say that a particular what humans can get out of the ecosystem rather than hypothesis is rejected. Is there any way. then, to decide how they can aid its other component species. The that an entire management approach should be rejected absence of a consensus definition is, in fact, part of a (Simberloff, 1994h)? larger problem. The entire concept of 'ecosystem health' is quite fluid, and, as observed above, there is no con- Is ecosystem management a panacea or a Trojan horse? sensus about what constitutes a healthy ecosystem. Some conservation biologists have argued that ecosys- There is a spectrum from utilitarian ideas to ecosystem- tem management is leading to 'species-bashing' (Soule centered ones (Wagner. 1994.) An example of a utilitar- 1994). that valuable, scientifically tested management ian view is that of the USDA Forest Service (1993): procedures are being jettisoned on the grounds that "Forest health is a condition where biotic and abiotic they are outmoded remnants of a discarded paradigm. influences on the forest ... do not threaten resource single-species management. management objectives now or in the future-. For the Also, from the standpoint of species conservation, it Forest Service, a forest ecosystem provides commodities is disturbing that many ecosystem processes can be pre- to humans, and management objectives reflect this con- served even as the component species normally respon- ception. An ecosystem-centered view of health envisions sible for them are lost (Tracy and Brossard. 1994). As the sustenance of all the components per se. indepen- an example. second-growth forest of low diversity often dently of whether the ecosystem as a whole can provide has greater primary productivity than does the diverse commodities: ".4 forest in good health is a fully func- old-growth forest it replaces. Is it therefore an accepta- tional community of plants and animals and their ph)- ble substitute for the original? Similarly. energy will sical environment. A healthy forest is an ecosystem in flow and nutrients will cycle in ecosystems of very few balance- ( Monnig and Byler. 1992). species: does it really suffice to maintain just the pro- Thus. although 'health' seems at first blush to be such cesses? It seems likely that many threatened species. a universal virtue that no one could object to it as a including flagship species like the spotted owl, red- goal. in practice. a goal of ecosystem health could be cockaded woodpecker. and Florida panther. could dis- used to the detriment of conservation of particular spe- appear entirel■ from an ecosystem without major or cies. This paradox could arise, for example. if sustain- even detectable change in key processes. Many of these able production of a commodity like a certain kind of charismatic vertebrates are top carnivores, thus of low wood could be prevented by maintenance of a bird like total biomass and primary productivity. Unless their• the spotted owl or the red-cockaded woodpecker. I n the preferential feeding controls a species that would other- utilitarian conception. such a bird would he inimical to wise be dominant (see Keystone species management. ecosystem health. Of course, the exact meaning of 'sus- below), their absence would probably not substantially tainable' and how we would assess sustainabilit■ is cen- affect the rest of the ecosystem. tral to this potential problem. But here again we have a The fact that various ecosystem processes are main- concept that has many definitions about which there is tained even as species disappear is but one aspect of an no consensus (Metre and Carroll. 1994). This debate is important difference between conserving ecosystems well enough known and sufficiently complex that I will and conserving species. Species and even entire guilds not summarize it here. can disappear. and they need not be replaced by others Founding a management paradigm on ecosystem that share many of their traits. But if a particular type health is hound to lead to disputes and misunderstand- of ecos■stem disappears. some other one will replace it. ings. This is because it is appropriate to the metaphor of and the high-level functions such as energy flow and the ecosystem as superorganism, a metaphor with nutrient cycling will still take place. even if details and ancient roots but one that is imperfect (Simberloff, rates change. 1980). Although there are analogies between an indivi- Another concern with ecosystem management as a dual organism and a community or ecosystem, there are guiding paradigm for conservation is that. whereas a many sorts of integrity that typify organisms but that species is usually easy enough to define, the boundaries communities and ecosystems lack (Simberloff. 1980: of an ecosystem are not so apparent. and which ecosys- 1992). Of course, the view that communities or ecosys- tems are so similar as to be representatives of the same tems are superorganisms was greatly influenced by hol- type is often not a trivial question (Tracy and Brussard. ism (Simberloff. 1980). and the commitment to holism 1994). It seems entirely possible that an area of conser- in many working definitions of ecosystem management. 54 D. Sim/wool/ noted above, can now he seen as associated with a pro- (1980) termed 'keystone mutualists' plant species that blematic criterion for assessing management success. support many animal species %■, hose activities may Even determining the health status of an individual themselves support many other species. And species organism is difficult. Determining, at least to the satis- may serve as keystones by virtue of how they change the faction of all parties. whether an ecosystem is healthy is physical structure of the environment. as do beavers hopeless. We have seen that different people have dif- Castor canadensis with their dams ( Naiman et al.. 1986: ferent definitions of health and different conceptions of Pollock et al.. 1995). Many species provide shelter for ecosystems, and that even the physical boundaries of an numerous other species. In the longleaf pine forest. ecosystem are often in doubt. Truly. ecosystem health is gopher tortoise Goph(rus polvphemus burrows are home not a workable goal. to 332 other species (Jackson and NI ilstrey. 1989). some Further, the integral relationship of adaptive man- of which use this microhabitat obligatorily. w hile the agement to many conceptions of ecosystem manage- holes that red-cockaded woodpecker clans laboriously ment is worrisome to conservationists. There are two excavate in longleaf trees are the only such holes present problems. First, the possible absence of a clear criterion and are used by at least 22 other species (Harlow and for rejection of a hypothesis and the continually chan- Lennartz. 1983). including the fox squirrel as noted ging management practices may make it impossible to above. proceed by normal scientific means to study the under- The expansion of the ke■ stone species concept has led lying mechanisms of the system and thus to conceive of some researchers to criticize it as so Fuzzy that it is entirely new ways to manage it or its component species. impossible to say w hat is and what is not a keystone Second, the focus is on the entire ecosystem rather than species; they go so far as to charge that it is dangerous on individual species. This fact suggests that ecosystem to apply the concept to management ( Mills el al.. 1993). management would not nurture the sorts of experiments However. to discard the idea would be to throw the and observations on single species that have often pro- baby out with the bathwater (deM a nadier and Hunter. vided great insight into not only their own biology but 1994). It seems more reasonable to refine it. A recent the structure and function of entire systems (examples such effort ( Power et al.. 1996) aims to quantify the cri- given below). teria for designation as a ke■ stone species and attempts Finally. it is often said that single-species manage- to separate the concept from that of the 'ecological ment 'doesn't work' (see. for example. Cushman. 1995; dominant', or species whose great biomass and abun- Mann and Plummer, 1995). as witness the fact that sev- dance make it crucial for an entire community and eral listed species managed under the US Endangered allow it often to constitute the physical structure of the Species Act have nonetheless disappeared. Some of community. these species. at the time of listing, were almost certainly Power et al. (1996) are pessimistic about the prospects already extinct (McMillan and Wilcove. 1994). Others for concocting a list of attributes that would a priori that had substantial populations when listed, such as the identify a keystone species inexpensively and efficiently. dusky seaside sparrow Annnodramus maritimus nigres- I agree. It is telling that much of the literature on key- cens, were grossly mismanaged. and non-biological fac- stone species is experimental in either the narrow sense tors. such as lax law enforcement, led to their demise of controlled manipulation (e.g. Paine. 19691 or the (Walters, 1992). It was not the inability of biologists to broader sense of some 'natural experiment' without know enough science to save these species that doomed strict control and replication, like an introduction of a them. Rather, the knowledge was there or could have species (Simberloff. 1991) or a removal of one (e.g. rab- been gathered, but economical, political, or social con- bit Oryetolagus euniculus, Harper. 1969: American cerns came to dominate the programs. chestnut Castanet' dentata. references in Simberlott 1997; and beaver Castor eanatlensis. references in Nai- Keystone species management man et al., 1986; Hackney and Adams. 1992; Pollock et A slightly different orientation to single-species man- al., 1995). In the latter cases. it is more difficult to draw agement might be more effective than the alternatives inferences, but before-and-after comparisons or spatial discussed above. The concept of the keystone species () comparisons between sites where the event occurred and suggests that, at least in many ecosystems, certain spe- those where it did not can often be quite suggestive. cies have impacts on many others, often far beyond Understanding the role of keystone species certainly what might have been expected from a consideration of requires inspired natural history (Paine. 1995), and their biomass or abundance. Paine originally studied a there is no real shortcut for obtaining sufficient insight starfish that selectively preyed on a species that would into the dynamics of an ecosystem. However, because a otherwise have been competitively dominant. The star- keystone species approach is focused squarely on an fish thereby prevented that dominance and allowed understanding of the mechanisms that underlie the numerous other species to coexist. The definition of function and structure of an ecosystem, it appears that 'keystone' has been expanded (see Bond, 1993; Menge et it might suggest entirely new ways of managing a al., 1994), and species not near the top of foodwebs have problem, rather than the successive-approximation also been seen as keystones. For example, Gilbert, approach that dominates adaptive management. For •

Single-species and ecosystem management 255

example. keystone species are sometimes context- stone? Whatever the criterion, it is conceivable that, in dependent (Paine. 1995: Power el al., 1996). The same some ecosystems, there are no species whose fates arc species in what look like two similar ecosystems may he integrally linked to those of many other species. Again, a keystone in one but not the other. Research to under- we would he left with a lot of useful knowledge about stand these differences has led to quite profound under- ecosystem structure and function in this case. even if we standing of the functioning of entire systems (Paine. were not provided with an immediate conservation tool. 1995). Finally, there have not been many' detailed studies of Management of keystone species may combine some keystone species and how to recognize them. Thus, we attractive features of single-species management and .need much basic research just to get started, and such ecosystem management. If the keystone affects many information has not been gathered for many ecosys- other species in its community, it may well be that tems. Nevertheless, it is hard to believe that truly effec- facilitating its growth and reproduction would support tive management plans will ever be forthcoming without the many species it interacts with as well. To the extent such knowledge. that the keystone is functionally crucial to a suite of other species, its management may maintain them. This proposition is a hypothesis rather than a fact. One would want to know the reasons for the keystone role of ACKNOWLEDGEMENTS a particular species: what causes populations of so many other species to depend on this one? Mary Ruckelshaus and Mars Tebo constructively criti- From a scientific standpoint, the appeal of studying cized an early draft of this paper. while comments by keystone species is apparent: such study is in the tradi- Malcolm L. Hunter. .1r Werner Suter. and an anon- tion of normal. analytic science. If this research is ymous referee were very helpful. insightful enough. the knowledge it provides about the functioning of the target ecosystem should lead to an ongoing research program and progressively more pro- found and coMplete knowledge of the ecosystem. Such knowledge could hardl■ fail to aid management even if REFERENCES it should turn out that managing this particular ke- t one will not be a major component in a strateg■ to Baker. 13. (1995) Wrestling with Webster for a definition of maintain the whole system. Further, profound knowl- harm. BioScience 45. 527. Baskin. Y. 11994 ) Ecosystem I unction of biodtversity. species edge of the mechanisms whereby the keystone BleSt //wee 44. 657 660. affects others. %vhether or not it leads to managing the Bond. W. J. (1993) Keystone species . In L, fis t-A/cm t um•fion koystone itself, would certainly provide further insights and Biodivenio. eds E. D. 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