Use of focal species in marine conser7ation and management: a re7iew and critique
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AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)
Use of focal species in marine conser7ation and
management: a re7iew and critique
MARK A. ZACHARIASa,* and JOHN C. ROFFb
a
Land Use Coordination Office, British Columbia, Canada
b
Department of Zoology, Uni6ersity of Guelph, Ontario, Canada
ABSTRACT
1. Focal species (i.e. indicators, keystones, umbrellas, and flagships) have been advocated for the
management and conservation of natural environments.
2. The assumption has been that the presence or abundance of a focal species is a means to
understanding the composition and/or state of the more complex community.
3. We review the characteristics of focal species, and evaluate their appropriateness and utility
judged against conservation objectives.
4. It appears that indicator species (of both composition and condition) may be of greatest
general utility, and that several types of focal species may exhibit useful indicator properties.
Copyright © 2001 John Wiley & Sons, Ltd.
KEY WORDS: flagship species; focal species; indicator species; keystone species; marine conservation; marine
management; marine protected areas; umbrella species
INTRODUCTION
All animals are created equal but some animals are more equal than others (Orwell, 1946).
Focal species are those which, for ecological or social reasons, are believed to be valuable for the
understanding, management and conservation of natural environments. Collectively, they are species on
which our attention is preferentially focussed for one reason or another. Many different types of focal
species have been proposed, but we define them to include indicator, sentinel, keystone, umbrella,
flagship, charismatic, economic and vulnerable species. While there are many names for the various types
of focal species, the ecological concepts and societal rationale behind the nomenclature can be distilled
into four distinct ‘categories’, namely, indicators, keystones, umbrellas and flagships (Simberloff, 1998).
Indicator, keystone and umbrella species are predicated on the expected outcomes of various ecological
concepts, while the flagship species concept relies on human compassion, sense of responsibility, and —to
some extent —self interest. (We use the term ‘concept’ in the sense of a construct that may have heuristic
value, rather than the terms theory or hypothesis which implies rigorous testability). Regardless of their
underlying assumptions, the expectation is that the presence or abundance of any of the four types of
focal species (or in some cases, guilds or taxa) is a means to understanding the composition, state, and/or
function of a more complex community.
* Correspondence to: Mark A. Zacharias, Land Use Coordination Office, Province of British Columbia, PO Box 9426 Stn. Prov.
Gov., Victoria, British Columbia, V8W 9R1, Canada. E-mail: mark.zacharias@gems6.gov.bc.ca
Copyright © 2001 John Wiley & Sons, Ltd. Received 10 April 2000
Accepted 28 October 200060 M.A. ZACHARIAS AND J.C. ROFF
In broad terms, the various focal species may be defined as follows.
Indicator species are species whose presence denotes either the composition or condition of a particular
habitat, community, or ecosystem.
Keystone species are critical to the ecological function of a community or habitat, where the
importance of these species is disproportionate to their abundance or biomass.
Umbrella species are those whose conservation will also conserve other species.
Flagship species are merely tools to garner public support for ‘charismatic megafauna’. However,
similar to the umbrella concept, the ultimate goal of advocating flagships is the protection of their
habitats and constituent species.
Several of the focal species concepts have been recently revisited by Menge et al. (1994), Navarrete and
Menge (1996), Power et al. (1996), Hurlburt (1997) and Simberloff (1998), where all of these authors,
except Hurlburt (1997), suggest that there continues to be merit in the application of these concepts to
conservation and management. Only recently, however, has this discussion focused on the potential value
of focal species for marine conservation and management (e.g. NRC, 1995; Zacharias and Roff, 2000).
However, we recognize that approaches to marine conservation and management at the population level
represent only one of an array of possible ecological approaches, ranging from the genetic to the
ecosystem level of organization (see Zacharias and Roff, 2000 for further explanation).
There has been considerable debate surrounding the value of focal species to the management and
conservation of terrestrial environments (e.g. Launer and Murphy, 1994; Weaver, 1995; Niemi et al., 1997;
Simberloff, 1998). Most criticism centres around (a) the validity of the ecological theory behind the
concepts, (b) the lack of firm definitions for the various types of focal species, (c) the lack of agreed
standards for their application and use, and (d) the observation that their application and popularity is
often more a result of management policy and direction rather than scientific rationale (Simberloff, 1998).
The major issues for conservation purposes are whether we can operationally define each of these terms,
and whether focal species have utility in conservation initiatives.
The purpose of this paper is to review the ecological and social justifications behind the use of
indicators, keystones, umbrellas and flagships, and evaluate their roles in the establishment and practice
of conservation strategies. We see these roles as potentially including: the selection of representative and
distinctive areas for marine conservation (e.g. marine reserves) (Roberts and Polunin, 1994; Meffe and
Carroll, 1997; Allison et al., 1998; Zacharias and Howes, 1998); integrated coastal zone management
(Imperial and Hennessey, 1996); the identification and monitoring of biological communities (Paine, 1992;
Kideys, 1994); habitat characterization and monitoring (Apollonio, 1994; Zacharias et al., 1999); and
marine ecosystem classification (Caddy and Bakun, 1994; Ray, 1996; Zacharias et al., 1998).
INDICATOR SPECIES
The indicator species concept is perhaps the broadest and most poorly defined of all the focal species, and
has often been used as a catch-all term for other types of focal species. On one hand, authors such as
Landres et al. (1988), Noss (1990) and Faith and Walker (1996) view indicators as an all encompassing
term to capture approaches/techniques to monitor biodiversity, and the term would include keystones,
umbrellas, sentinels and charismatic species. These authors’ definitions of indicators are what we and
others have termed focal species. The alternative view, expressed by Kremen (1992), Dufrene and
Legendre (1997), Simberloff (1998) and others suggests that the indicator species concept is substantially
different from other focal species and warrants separate treatment.
The confusion over this concept results from its myriad of definitions and applications; these can,
nevertheless, be considered to fall into two categories. The first application resulted from the realization
Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)FOCAL SPECIES IN MARINE CONSERVATION 61 that the presence, absence, or abundance of certain species can be used to identify other less easily identified species and their associated habitats (Clements, 1916). One of the first applications of the term was by Kolkwitz and Marsson (1908), who noted that certain species could indicate such variables as soil type, climate, and the presence of other species. The use of indicators to indicate a particular habitat, community or ecosystem continues to be an important part of ecology, and for the purposes of this paper, we have termed this type of indicator species as a composition indicator. A composition indicator (Table 1) has also been colloquially referred to as an ‘ecological’ or ‘environmental indicator’, whose presence or abundance is used to characterize a particular habitat or biological community. This type of indicator may also be used to estimate biodiversity (often ‘hotspots’) for the selection of candidate protected areas (Faith and Walker, 1996). Over time, the concept has been expanded to include a second application, namely to indicate the condition of a habitat, community, or ecosystem (Meffe and Carroll, 1997). These condition indicators (Table 1) form the basis of biological monitoring of environmental change as a result of anthropogenic and natural disturbances. Incorporated into condition indicators are what have been termed ‘bio-indicators’. Our definition of the condition indicator is also analogous to the use of the term ‘sentinel species’ (Meffe and Carroll, 1997). Much of the confusion surrounding the definition and application of indicators is a result of amalgamating composition and condition indicators. This is seen in many definitions, including those from Landres et al. (1988), who described indicators as ‘. . . species that, by their response of certain environmental conditions are thought to be useful to quickly infer the effects of those conditions on other, non-indicator species’. Niemi et al. (1997) implied a condition indicator when suggesting that the purpose of indicators is to monitor habitat quality that is required by other species. Block et al. (1987) referred to composition indicators when suggesting that indicator species are plants and animals that are closely associated with specific environmental factors. Meffe and Carroll (1997) begin to make the distinction between composition and condition in their definition of ‘A species used as a gauge for the condition of a particular habitat, community, or ecosystem. A characteristic, or surrogate species for a community or community ecosystem’. There is also a functional differentiation between composition and condition indicators. In relation to conservation and management, composition indicators are often used in the identification of representative or distinctive areas, areas of high biodiversity, endemic species, or critical areas (spawning, feeding etc.). In contrast, condition indicators are only used once specific habitats or communities have been identified and there is a requirement to monitor the effectiveness of conservation and management strategies. Therefore, the composition indicator is most relevant to efforts to determine areas or priorities for conservation, while the role of condition indicators in marine conservation falls under the evaluation of conservation efforts. This paper focuses on composition indicators, as these are most relevant to conservation efforts, and the literature surrounding their application is considerably smaller than condition indicators. Certain characteristics of marine environments necessitate rethinking the application of composition indicator species. Composition indicators can be further separated into what Meffe and Carroll (1997) term indicators of habitat, community, and ecosystem. Community composition indicators can be used to characterize an assemblage, guild, taxon, releve, series, biocoenoses or community. Ecosystem composition indicators are used to characterize predominantly abiotic (e.g. habitat) ‘structures’ that may include salinity, temperature, nutrients, substrate, upwellings or productivity. There are a number of potential benefits to using indicators in marine conservation and management. First, given the cryptic nature of most marine environments, the ability to predict community composition based on a few observable species is invaluable. For example, the presence of the giant kelp Macrocystis spp. indicates potential sea otter habitat, as otters are currently repopulating vast areas of habitat where Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)
62
Table 1. Characteristics exhibited by the various types of focal species
Composition indicator Condition indicator Keystone species Umbrella species Flagship species
species species
Exhibit a specific niche or Provide an assessment Exert a disproportionate Demonstrate fidelity to a Garners public support
a defined range of over a range of stress influence on community particular set of habitats and affection
Copyright © 2001 John Wiley & Sons, Ltd.
ecological tolerances structure relative to its
abundance or biomass
Demonstrate fidelity to Differentiate between Substantially change the Limited change in Requires large tracts of
community type or natural and anthropogenic structure and/or community or habitat relatively natural or
habitat type stress composition of a structure if removed unaltered habitat
community or habitat upon
its removal
Relatively independent of Relevant to ecologically Lower the number of Non-migratory Migratory or
sample size significant change species in a community non-migratory
upon its removal
Independent of spatial Independent of sample Prevent a single species Exhibit low inter-annual Amenable to traditional
scales size from becoming the or decadal population management practices
competitive dominant variation (e.g. fisheries
M.A. ZACHARIAS AND J.C. ROFF
management)
Exhibit low temporal and Independent of spatial Specialists rather than
spatial variability scales generalists
Compatible with national Exhibit low temporal and Do not thrive in disturbed
and international spatial variability or anthropogenic habitats
indicators
Cost effectively observed Compatible with national Require large tracts of
and censured and international relatively natural or
indicators unaltered habitat
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)FOCAL SPECIES IN MARINE CONSERVATION 63 they had been previously extirpated (Estes and Palmisano, 1974). Trawl data are often characterized using indicator species at small scales, such as the Canary Islands (Falcon et al., 1996) as well as oceanic scales (Pearcy et al., 1996). Second, indicator species are often suggested as potential conservation tools because they can identify representative and distinctive habitats, communities or ecosystems. They have been advocated for conservation and management purposes as being more effective than other methods, such as species richness, where areas of high diversity do not necessarily address the conservation of rare or threatened species and habitats (Lambeck, 1997). The concept of conserving representative and distinctive areas in marine environments has gained momentum in recent years. This in turn has required cost effective methods of identifying the presence of particular communities (i.e. assemblages, taxa, guilds, functional groups, biocoenoces etc.) and habitats (Webb, 1989; Cousins, 1991; Roff and Taylor, 2000; Zacharias and Roff, 2000). Consequently, measures of species richness —while still useful approaches for conservation —are not good measures of representativity, whereas indicator species are ideally suited to the task. Third, there are few leaps of faith required in the use of the indicator species concept. Relative to keystones and umbrellas (see below), the notion that certain species are found in certain communities and habitats is intuitive, and there is little disagreement that the indicator concept is valid. While there may be discussion surrounding which species or guilds indicate what habitats or communities, the concept has never been disproved and, therefore, the indicator species is the most ecologically concrete of all the focal species. Fourth, there has been nearly 30 years of effort to identify both indicator species and the communities and habitats they represent. Numerous clustering and ordination techniques have been developed to statistically define communities and habitats, including correspondence analysis (CA), detrended correspondence analysis (DCA), principal coordinates analysis (PcoA), and nonmetric multidimensional scaling (NMS). The best known site (Q mode) and species (R mode) ordination program is the two-way indicator species analysis (TWINSPAN) developed by Hill (1979) (see also Dufrene and Legendre, 1997). The program includes (a) a simultaneous sorted data table for both sites and species, (b) indicator species at each level of the hierarchy, (c) the capability to produce dendrograms, and (d) low computational requirements (Kremen, 1992; Carleton et al., 1996; Dufrene and Legendre, 1997; Simberloff, 1998). To date, there are no mathematical programs to identify keystone, umbrella, or flagship species. There are a number of disadvantages to using composition indicators for marine conservation and management. First, there have been a number of studies suggesting that no one species fulfils the requirements of an indicator for conservation (e.g. Landres et al., 1988). This observation is especially pertinent in marine environments, where food webs generally support more trophic levels, and where predators are more often generalist feeders than in terrestrial environments (Rickleffs and Schluter, 1993). Consequently, the ability of any single species to signal either the structure or functioning of a community may be diminished. Indicators may be more efficient when used to indicate the presence of species from a specific guild (Block et al., 1987). This concept has potential in marine environments, where —for example —a certain rockfish or reef fish could indicate the presence of less readily identified species of a guild. Functional groups have also been used as indicators of environmental conditions related, for example, to wave exposure and oceanographic conditions (Bustamante and Branch, 1996). Second, given the fluid nature of marine environments, marine indicator species may not be as geographically or temporally persistent as terrestrial ones. With the exception of birds, flying insects and some mammals, most terrestrial species are confined within a watershed, biome, or other mostly impermeable boundary. Most marine boundaries are semi-permeable; therefore, indicator species may be distributed over great distances and are often not endemic. This wide distribution may be part of a species’ natural habitat range, or a result of transport by storms, oceanographic events, or shifts in prey distribution. This instability is compounded by large scale oceanic variations (e.g. El Niño–Southern Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)
64 M.A. ZACHARIAS AND J.C. ROFF
Oscillation) over years to decades. Terrestrial environments are also subject to these vagaries, but in
marine environments, entire communities may move great distances.
Third, marine species are notoriously difficult to observe and census; therefore, the absence of an
indicator species may be the result of incomplete observation rather than lack of a certain community
type. This notion is especially critical, as most of the best known species are migratory and, therefore, can
only be observed in an area at certain times of the year. With the exception of intertidal and nearshore
subtidal environments, indicators will generally comprise of vertebrates and invertebrates. Phytoplankton
can and have been used as indicators, but the difficulty in their identification may be onerous.
Finally, Simberloff (1998) cautions that an indicator subject to single species management is no longer
an indicator. This observation has substantial implications in marine systems, because the majority of
species that are readily observable are generally harvested by humans to some degree and, therefore, make
poor indicators. For instance, herring (Clupea spp.) has been proposed as an indicator and has also been
proposed as a keystone species. Herring, however, is consumed by birds, fish, marine mammals and
humans; therefore, an increase or decrease in herring abundance may be the result of a number of
interconnected factors. The types of marine species that would make the best composition indicators are
those not adversely affected by pollution, habitat loss, alien introductions or global climate change.
Consequently, certain sea birds are potential good candidates for indicators, as are sea grasses,
macroalgae and certain benthic invertebrates.
KEYSTONE SPECIES
The keystone species concept (Table 1) has received considerable attention since its designation by Paine
(1969). He found that removal of Pisaster (a sea star) from an intertidal community resulted in Mytilus
(a mussel) becoming a competitive dominant; therefore Pisaster appeared to exert an influence
disproportionate to its abundance and biomass. He theorized that certain species are either directly or
indirectly responsible for biological community structure, composition and biomass and, therefore,
biodiversity (Paine, 1969). The removal of a keystone species has a significant impact on a community,
and consequently, there is an impetus to identify and conserve them. The concept holds considerable
allure for managers and conservationists, as the notion of protecting and managing just a few species to
the benefit of the entire community or ecosystem could make a seemingly impossible task manageable
(Navarrete and Menge, 1996). A number of criteria should be met before a species can be considered a
keystone. While there is debate surrounding what constitutes a keystone, their general characteristics are
supplied in Table 1.
The keystone species concept has become an accepted and central organizing theme of population level
ecology and conservation, and many species have been proposed as keystones in the marine environment
(Table 2). The concept has, however, been ill defined, which has led to the christening of a number of
species as keystones that are probably not (Hurlburt, 1997; Simberloff, 1998). The Oxford Dictionary of
Ecology defines a keystone species as ‘The species, the presence or abundance of which can be used to
assess the extent to which resources of an area or habitat are being exploited’ (Allaby, 1996).
Roughgarden (1983) defines a keystone species as one ‘. . . whose removal leads to a still further loss of
species from the community’. Terborgh (1986) discussed keystone resources, which are those resources
that comprise a small percentage of diversity or biomass, but are essential to community structure and/or
diversity. Menge et al. (1994) defined keystone predators ‘. . . as only one of several predators in a
community that alone determines most patterns of prey community structure, including distribution,
abundance, composition, size, and diversity’. This uncertainty surrounding the definition and application
of the keystone concept was the impetus behind a workshop in 1994 to review and discuss the meaning
of the term. Results of this workshop were reported in Power et al. (1996) and suggest that keystones are
Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)Table 2. Marine species proposed as keystone species (adapted from Power et al., 1996)
Environment Citation(s) Keystone species Target of direct Mechanism of Evidence
or guild effect effect
Rocky intertidal Paine (1966) Pisaster ochraceus Mussels Consumption Experimental,
(predatory starfish) comparative
Menge (1976) Nucella lapillus Mussels Consumption Experimental
(predatory snail)
Hockey and Branch (1984) Haematopus spp. (black limpets Consumption Comparative
oystercatchers)
Castilla and Duran (1985), Concholepas concholepas Mussels Consumption Experimental
Duran and Castilla (1989) (predatory snail)
Menge et al. (1994) Pisaster ochraceus Mussels Consumption, Experimental,
Copyright © 2001 John Wiley & Sons, Ltd.
(predatory starfish) direct and indirect comparative
Navarrete and Menge Pisaster ochraceus Mussels Consumption, Experimental,
(1996) (predatory starfish) and direct and indirect comparative
Nucella (whelks)
Rocky subtidal Estes and Palmisano (1974) Enhydra lutris (sea otter) Sea urchins Consumption Comparative
Fletcher (1987) Centrostephanus rodgersii Algae Consumption Experimental
(sea urchin)
Ayling (1981) E6echinus chloroticus Algae, sponges and Consumption Experimental
(sea urchin), herbivorous ascidians
gastropods, Parika
scaber (grazing fish)
Pelagic May et al. (1979) Balaenoptera spp. Krill Consumption Historical reconstruction
(baleen whales)
Springer (1992) Theragra chalcogrammai Zooplankton, smaller Consumption Historical reconstruction
FOCAL SPECIES IN MARINE CONSERVATION
(walleye pollock) fish
Coral reef Hay (1984) Herbivorous fish, sea Seaweeds Consumption Experimental,
urchins comparative
Carpenter (1988, 1990) Diadema antillarum Seaweeds Consumption Experimental,
(herbivorous sea urchin) comparative
Hughes et al. (1987) Diadema antillarum Marine plants Consumption Experimental,
(herbivorous sea urchin) comparative
Birkeland and Lucas (1990) Acanthaster planci Corals Consumption Experimental,
(coral-eating starfish) comparative
Hixon and Brostoff (1996) Stegastes fasciolatus Schooling parrotfish Protection of Experimental
(territorial algivorous and surgeonfish seaweeds within
damselfish) territories from
heavy grazing
continued
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)
6566
Table 2 continued
Environment Citation(s) Keystone species Target of direct Mechanism of Evidence
or guild effect effect
Copyright © 2001 John Wiley & Sons, Ltd.
Soft sediment VanBlaricom (1982) Urolophos halleri, Amphipods Consumption, Experimental
Myliobatis californica disturbance
(carnivorous rays)
Oliver and Slattery (1985) Eschrichtius robustus (gray Amphipod mats Consumption, Comparative
whales) disturbance
Oliver et al. (1985) Enhydra lutris (sea otters) Bivalves Consumption Comparative
Kvitek et al. (1992) Enhydra lutris (sea otters) Bivalves Consumption Experimental,
comparative
Estuarine Kerbes et al. (1990) Chen caerulescens Salt marsh vegetation Consumption, Comparative
caerulescens (lesser snow disturbance
geese)
M.A. ZACHARIAS AND J.C. ROFF
Ray (1996) Sea grasses and eel Substrate Comparative
grasses composition
Ray (1996) Crassostrea 6irginica Water quality Filtration in estuary Comparative
(eastern oyster)
Other Willson and Halupka (1995) Anadromous fish Terrestrial wildlife Consumption Comparative
Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)FOCAL SPECIES IN MARINE CONSERVATION 67
‘a less abundant species that have strong effects on communities and ecosystems’. Meffe and Carroll
(1997) probably supply the most comprehensive definition that still retains the intent of the concept by
stating that keystone species are those species which ‘. . . play a disproportionally large role in community
structure’.
Since the work of Paine (1969), a number of different types of keystone species have been proposed,
some of which only vaguely resemble the spirit and intent of Paine’s definition. Other types of keystones
include keystone predators (Paine, 1966), keystone mutualists (Gilbert, 1980), which include plant species
that support animal species, which may in turn support more species, keystone modifiers (Naiman et al.,
1986), such as the beaver (Castor canadensis), the African elephant (Loxodonta africana), or various
species of sea grasses (Carlton, 1996), keystone prey which maintain a population of predators (Holt,
1977, 1984), and keystone diseases (Sinclair and Norton-Griffiths, 1982) which may ultimately play the
largest role in structuring communities. Keystones occur in all the world’s ecosystems, do not necessarily
occupy higher trophic levels, and affect their communities through consumption, competition, dispersal,
pollination, disease, and by modifying habitats and abiotic factors. There is also growing evidence that
small but critical species, such as the mycorrhizal fungi and nitrogen fixing bacteria, should also be termed
keystones (Paine, 1995; Weaver, 1995).
There has been considerable resistance to both the keystone concept and its application towards
addressing conservation objectives. There are five arguments against the use of keystones from a
conceptual and empirical standpoint.
1. Complex communities are rarely controlled by a single species.
2. All species are keystone species to some degree.
3. Identifying keystone species is difficult.
4. Keystone species that demonstrate keystone properties in some regions may not do so in others.
5. Conservation or management of a keystone species does not guarantee that conservation objectives are
met.
The first hurdle facing the keystone concept is that there is little empirical evidence that most communities
are controlled by a single, or relatively few predators, thus casting doubt on the universal applicability of
the concept. The rocky intertidal shorelines of the Pacific northwest USA where Paine (1969) completed
his research are not representative of the more complex composition of most terrestrial and marine
communities, and there is some evidence that while the keystone concept may work in simplified systems,
keystones are not relevant in more complex communities. Tanner et al. (1994) found that communities on
the Great Barrier Reef did not have keystone species because the high species diversity of these
environments reduced the chances of a single species structuring the community, and because the time
required for a species to attain dominance is greater than the average period between natural disturbance
events.
Peterson (1979) found that the exclusion of predators in estuarine and soft bottom systems did not
result in a competitive dominant, thus casting doubt on the universality of the keystone concept. Peterson
(1979) suggested that keystones may be present, but that predators have not been excluded long enough
for a species to become dominant. He also suggested that interference competition and competitive
exclusion —processes which operate on rocky shores —are absent in soft bottom systems as organisms
cannot dislodge or overgrow each other in a three-dimensional sediment dominated environment.
Extrapolating these results into other pelagic and sediment dominated marine systems suggests that the
processes that permit the establishment of a keystone species may be absent in many marine communities.
The second concern is that all species are keystones to some degree. The observation that most
keystones have been identified through either predator exclusion experiments (e.g. starfish), or the
re-colonization of previously extirpated species (e.g. sea otters) suggests that the species we currently term
keystones are merely products of the environments and communities under study (Mills et al., 1993;
Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)68 M.A. ZACHARIAS AND J.C. ROFF Simberloff, 1998). The fact that keystones may be artifacts of research methods and data analysis leads into the third criticism that keystones are difficult to identify, particularly in marine systems. The difficulty in identifying keystones is the third, and perhaps most damning indictment of the concept, particularly in marine systems. Most keystone predators have been identified through experimental manipulation (e.g. predator exclusions) or by observing the recovery of disturbed systems (e.g. reintroduced sea otters). Navarrete and Menge (1996) elevate the requirements for identifying keystones by correctly suggesting that a single predator should first be removed, then the other predators one by one until the entire predatory guild has been removed. Only then can the keystone properties of each species be identified. While the keystone concept evolved out of the manipulation of intertidal environments, the intertidal realm is not representative of most marine environments, where predator exclusion studies are difficult, if not impossible to conduct. The fourth problem is that species may only act as keystones under a certain set of biotic and/or abiotic conditions. Paine (1966, 1969), in concluding that Pisaster comprised a keystone species generated considerable research into testing not only whether Pisaster was indeed a keystone, but also the search for other potential keystone species. Paine (1969) suggested that the Pisaster–Mytilus interactions constituted a keystone relationship as a result of its ubiquity from Mexico to Alaska. Foster (1990) and others, however, suggested that this relationship continuously changes over time and space, and that the spiny lobster also predates Mytilus in California (Foster, 1990). Paine (1980) agreed that keystones were situation specific, and speculated than in certain instances, Pisaster was ‘. . . just another seastar’. Menge et al. (1994) showed that Pisaster was a keystone only in high wave energy habitats, whereas in habitats with lower wave exposure, they cease to act as keystones. There is also considerable debate whether any species acts as a keystone throughout its life cycle, geographic range and the habitats it occupies. Research to date has not identified any universal keystone predators, but some keystones such as disease or eelgrass beds, probably structure communities and/or habitats in the same manner throughout their range. As a result of attempts to define and identify keystones, Menge et al. (1994) refined the keystone concept by defining diffuse predation, where the control of a competitively dominant species is shared by several predators. Weak predation occurs when predators alone do not control the abundance of a competitive dominant. Navarrete and Menge (1996) further explored these effects in intertidal environments by examining the strength of predation on mussels (Mytilus trossulus) by Pisaster and the whelks of the genus Nucella under various environmental conditions. They found that Pisaster was unaffected by the presence of the whelks, but that whelks were an important controlling influence on mussel distribution in the absence of Pisaster. All the foregoing limitations lead to the fifth objection or conclusion, namely that conservation or management of keystones in the marine environment does not guarantee that conservation objectives are met. Although the keystone concept was developed through the study of intertidal environments, the application of the concept is probably better suited to terrestrial environments for a number of reasons. Marine food webs generally vary over spatial and temporal scales to a greater degree than most terrestrial environments; therefore, the probability that the composition and diversity of a community rests on a single species is low (Nybakken, 1997). Terrestrial communities are generally spatially, and for the most part temporally stable. A tropical or sub-boreal forest, for example, tends to remain the same basic community over geological time scales. In contrast, an entire marine community — from phytoplankton to top predators —may change rapidly over an area, especially in pelagic environments. This variability can be triggered by annual and decadal events, which include regional disturbance (e.g. hurricanes) and climatic fluctuations (e.g. El Niño–Southern Oscillation). Therefore, as demonstrated by Menge et al. (1994) and Navarrete and Menge (1996), a species only exhibits keystone properties under certain environmental conditions, which are, for the most part, more variable in marine systems. This is especially apparent when migratory species are identified as Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)
FOCAL SPECIES IN MARINE CONSERVATION 69
keystones, which can avoid unsuitable areas as a result of changes in oceanic conditions. In contrast, many
tropical environments are believed to be stable with respect to abiotic conditions, which suggests that
keystones should be present. This very stability, however, may lead to the evolution of so many species
that no one species controls a community (Tanner et al., 1994).
Lastly, the important principle with keystones is that they do not change the fundamental community
type in an area or community – habitat relationship. Presence or absence of a keystone simply changes the
relative abundance of member species within a community. Keystones are, therefore, not important for the
recognition of community types, except if they are considered as composition indicators. However, their
presence or absence may be significant in the sense that they may be condition indicators of community
composition or diversity. Where keystones are commercially exploited, management decisions can affect
resultant expressions of diversity. The keystone concept is, therefore, currently not a globally useful concept
for marine conservation in the same manner as indicator species.
UMBRELLA SPECIES
The umbrella species concept (Table 1) hinges on the assumption that the presence of a certain species in
a geographical area indicates that other species will also be present. In this sense, it could also be considered
as a composition indicator species. However, umbrella species are distinct from composition indicators
because composition indicators indicate the presence of a community type, and cannot be used to make
assumptions on the state of that community. The conservation of a composition indicator does not assume
that other species in the community will also be conserved. In contrast, conservation of an umbrella species
is believed to protect other species, even if relationships between the umbrella and the community type are
poorly established.
The umbrella concept is particularly appealing to the conservation community, because the implication
is that the management, conservation or protection of an identified umbrella species will protect not only
the habitat and community required to support itself, but also the habitat for other species as well. The
concept has been used in the selection of sites for protection, where communities and habitats could be
identified through the identification of umbrella species. Unfortunately, the relationships between an
umbrella species and communities are usually ill-defined, especially in marine environments, where such
species may span broad geographic ranges encompassing several habitat types. Umbrella species as a whole
are, therefore, liable to be uninformative about the geographic limits of either representative or distinctive
marine communities or species diversity. An umbrella species may in fact ‘indicate’ habitat or community
types at some higher (but undefined) level of the ecological hierarchy (Roff and Taylor, 2000).
The umbrella concept is differentiated from the keystone concept in that protection of an umbrella can
lead to the protection of communities and habitats, although these entities will continue to exist and
function in the absence of the umbrella. In contrast, the removal of a keystone species may fundamentally
change community composition. Certain terrestrial species could be considered as both umbrella and
keystone species, but few marine species exhibit characteristics of both. Sea otters (Enhydra lutris) could
potentially be considered as both an umbrella and a keystone, as otters modify community composition
from invertebrate (e.g. urchin) dominated to kelp dominated systems, which in turn provide shelter and
habitat for the juvenile life stages of a number of anadramous, meroepipelagic and demersal fish species.
The protection of sea otters, therefore, also protects numerous other fish species. Other marine species
considered as keystones, including the grey whale (Eschrichtius robustus), probably fail the critical test of
an umbrella species, as the actions of grey whales —while maintaining a seral successional state through
benthic foraging — are probably not ‘protecting’ other species as a result of grey whale conservation. There
is also the consideration that grey whales — along with most other marine mammals —are generalist feeders
and migratory, and like keystones, may only act as umbrellas part of the time (Oliver and Slattery, 1985).
Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)70 M.A. ZACHARIAS AND J.C. ROFF It is generally acknowledged that there are three types of umbrella species. The first are the classic ‘single-species umbrellas’, generally comprising the larger vertebrates that require large territories to survive (Wilcox, 1980; Peterson, 1988). The conservation of these species is thought to protect other species with smaller habitat requirements. The single-species umbrella concept has been applied to ungulates, terrestrial carnivores and sea otters (Noss et al., 1996). The second type of umbrella species identifies ‘mesoscale species’, which are affected by the scales of human disturbance (Kitchener et al., 1980; Holling, 1992). The usefulness of this concept in marine systems is suspect, because the concept assumes that the habitat ranges of marine species is understood, to an extent, where a nested system of habitats can be identified. The reality, as discussed previously, is that putative marine umbrella species frequently cross both habitat types and communities to a much greater extent than their terrestrial counterparts. A third type of umbrella species is what Ryti (1992) terms ‘focal taxa’, which have also been termed by Hager (1997) as ‘umbrella groups’. This concept uses a speciose taxon to ensure that in the presence of these species, most of the larger community is protected. Ryti (1992) found that plant species proved to be better umbrellas than bird species on selected islands and canyons in southern California. This concept was further explored by Lambeck (1997), who identified a suite of ‘focal species’ within which each species is the most sensitive to a particular threat to its existence. The combination of a number of species keyed to each threat provides management direction for the conservation or management of their associated habitats and communities. Lambeck (1997) outlines a procedure to identify a number of species that must be present ‘. . . if a landscape is to meet the needs of its constituent flora and fauna’. The disadvantage of this approach is that considerable effort may be required to identify the focal species, and that if numerous focal species are identified, then there is no efficiency in using the concept. In addition, the critical question of whether the number of species protected within the range of an umbrella species is greater than would be protected within a similar range selected at random, has not been tested. The use of umbrella species as focal taxa in marine environments is intuitively appealing, but the application of the concept is fraught with difficulties. A primary limitation concerns the considerable unexplained spatial and temporal variation in many marine communities. While a terrestrial forest, for example, may be affected by occasional periods of disease, drought, infestations and other processes, the structural habitat in the form of the trees themselves is generally persistent over time (with the exception of fire and other catastrophic events). The marine analogues to trees are the kelps, which often exhibit large inter-annual and inter-decadal variation. As a result, terrestrial vegetation as a basis for focal taxa has no marine equivalent, with the notable exception perhaps of rooted nearshore sea grasses and mangroves. In marine environments, most species — while exhibiting prey preference —are generalist feeders. There is mounting evidence that almost all species, and especially the larger vertebrates, can and do feed on numerous species within a food web. Certain species of tuna are known to feed on over 140 species, and certain species such as Pacific herring (Clupea harengus) are consumed by many different marine mammals and sea birds in the northeast Pacific (Nybakken, 1997). Consequently, the assumption that protecting generalist feeders will protect other species associated with the generalists may be an unwise management approach. There is, however, some value to the approach using umbrella species as focal taxa, not necessarily for the protection of other species, but rather for the protection of the natural order and function of food webs and trophic structures. The harvest of the bowhead whale (Balena mysticetus) to ecological extinction in many arctic environments resulted in the tripling of populations of sea birds and marine mammals that competed for the same krill resource (Nybakken, 1997). Consequently, the protection and subsequent (partial) recovery of bowhead stocks resulted in the decline of these other vertebrate populations. An application of the focal taxon concept in this instance could possibly use bowhead whales and one or more other species to gauge the relative health of the krill resource, while monitoring those Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)
FOCAL SPECIES IN MARINE CONSERVATION 71
populations that depend on that resource. In this sense, however, the whales are being used as a condition
indicator.
A further flaw in the application of the umbrella concept in marine systems is the requirement that an
umbrella species be non-migratory. The migratory nature of most marine vertebrates suggests that the
concept is not as powerful an approach as for other focal species. The flagship concept may be more
apropos for marine conservation strategies.
FLAGSHIP (CHARISMATIC) SPECIES
The affinity of western and other societies for marine mammals is remarkable. The ability of Greenpeace
to halt certain types of commercial sealing and whaling was one of the most successful environmental
campaigns in history. There is no doubt that charismatic species have been used to achieve marine
conservation ends, but there are limitations to the application of the concept. In terrestrial systems,
threats to charismatic species have been used to garner support for conservation efforts. This generally
necessitates the conservation of the habitat required to support them. For example, the conservation of
spotted owls (Strix occidentalis) or grizzly bears (Ursus arctos) is equivalent to the conservation of
habitat. Indeed, the ultimate purpose of the conservation of charismatic species is the preservation of
habitat. This has resulted in recent legal challenges to the US Endangered Species Act, as certain groups
contend that conservation organizations are using the act to preserve habitat rather than the species.
In contrast, the preservation of a charismatic species does not necessarily protect either the habitat or
other species in marine systems. Baleen whales, for example, feed on parts of the food chain rarely
extracted by humans; therefore, the benefits of protecting these species are not as great as in terrestrial
species (Oliver and Slattery, 1985). Terrestrial charismatics are threatened by a number of activities, of
which habitat loss is critical. Because of the loosely coupled association between species and habitats in
most marine environments, the charismatic concept lacks the advantages of its use in terrestrial systems.
Another limitation to the flagship concept is that subsequent to the cessation of wholesale slaughter of
marine mammals, the majority of the most threatened marine species have few charismatic properties.
There is little public identification with taxonomic groups such as rockfish, bivalves and krill.
While the umbrella and flagship concepts share several similarities, there are important differences that
affect their utility in marine systems. Flagships (Table 1) are better suited for marine conservation because
(a) migratory species may be considered as flagships, (b) standard management practices (e.g. fisheries
management) can be used to mitigate impacts on flagships over large areas, (c) flagships may be
associated with several distinctive habitats, including the feeding or breeding grounds at the extremes of
migration routes.
A major function for marine flagship species may, therefore, be the same as in terrestrial systems, i.e.
to act as surrogates for habitat protection. Habitats used by migratory marine flagship species may be
relatively discrete, at least seasonally, and may define representative or distinctive areas (which can
subsequently be assessed by habitat characteristics or indicator species analyses) suitable as candidates for
conservation.
CONCLUSIONS
Despite all the above flaws and criticisms levelled at the various focal species, they may all still have useful
roles in marine conservation in terms of their indicator potential. However, the appropriateness and utility
of each of these focal species must be judged against specific conservation objectives. In simple terms,
there are approaches that attempt to conserve spaces (e.g. marine reserves), and those that conserve
Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)72 M.A. ZACHARIAS AND J.C. ROFF
species (e.g. fisheries management). How focal species might be used in the conservation of both spaces
and species is indicated in Table 3 and outlined in the following.
A logical approach for the utilization of focal species in the conservation of spaces is as follows. First,
define the objectives of the conservation strategy. For example, many countries utilize marine reserves as
their primary conservation strategy. From an examination of Table 3, the application of composition
indicators would be well suited to identifying either representative or distinctive candidate marine reserves.
The additional use of condition indicators may yield information on the current state of the candidate
reserve, and whether this state is a result of ecological or anthropogenic processes. This knowledge may
also be required in the application of mitigation, restoration and monitoring strategies once the reserve
has been established. In the identification of a geographical boundary, the use of the umbrella concept
may also be applicable.
A logical approach for the utilization of focal species in the conservation of species is similar to that
for the spaces approach. First, determine which species are the target of the conservation efforts. For
example, many jurisdictions are concerned with populations of harvested fish species. Second, determine
which focal species can be used to design and/or implement a conservation strategy. In our example,
composition indicators may be valuable in determining the habitats of the fish species under
consideration. The predictive nature of these indicators may allow determination not only of where
populations may occur, but where they may have occurred, or where they may occur in the future.
Condition indicators may permit different populations to be evaluated (ranked) as to the degree of
anthropogenic influence or successional stage. If the species of concern has the ability to garner public
support for its conservation, then it becomes a flagship. The umbrella species concept may be applicable
if our example fish is a prey item of a particular marine mammal or seabird, which may then act as the
umbrella.
While there has been considerable criticism of the indicator species concept in terrestrial environments,
and the suggestion that keystone or umbrella species may be more relevant to conservation efforts, the
cryptic and fluid nature of marine environments lends greater support for the use of indicator species. By
focussing on indicator species (or the indicator properties of any focal species), we can ask a number of
fundamental ecological questions (which could also be phrased as testable hypotheses) which have utility
in conservation planning, management, and monitoring.
Table 3. Do focal species provide information for the following marine conservation strategies and initiatives?
Focal species Identify Identify distinct Identify Identify condition Identify condition
representative community and geographical or state as a result or state as a result
community and habitat types extent of of ecological of anthropogenic
habitat types? (e.g. hot spots)? community and factors? factors?
habitat types?
Composition Yes Yes Yes Unknown No
indicator
Condition No No No Yes Yes
indicator
Keystone No No No Yes No
Umbrella No No Yes No Possibly
Flagship No No Yes Unknown Possibly
Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser6: Mar. Freshw. Ecosyst. 11: 59 – 76 (2001)FOCAL SPECIES IN MARINE CONSERVATION 73
1. Does a composition indicator species reliably indicate the presence or absence of a community and its
affiliation with defined habitat types?
2. Does the presence or absence of a condition indicator species reliably indicate the ecological state of
a community (in the absence of demonstrable anthropogenic impact)?
3. Does the presence or absence of a condition indicator species reliably indicate anthropogenic stress of
a defined sort and magnitude?
Finally, in terms of utility for conservation purposes: composition indicator species indicate community
types which can be related to habitat types, which can, in turn, be spatially mapped. This is a fundamental
prerequisite for conservation initiatives based on representativity (e.g. Roff and Taylor, 2000). The
composition indicator is the only focal species that can be used in this way (unless other focal species have
such indicator properties). Similarly, condition indicators (whether they may be additionally considered as
keystones or umbrellas) are the only biological means (using whole organisms) to infer ecological
integrity.
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