Usefulness of the Umbrella Species Concept as a Conservation Tool

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ABSTRACT:
In the face of limited funding, knowledge, and time for action, conservation efforts often rely on shortcuts for the maintenance of biodiversity. The umbrella species concept - proposed as a way to use species requirements as a basis for conservation planning-has recently received growing attention. We reviewed the literature to evaluate the concept's general usefulness. An umbrella species is defined as a species whose conservation is expected to confer protection to a large number of naturally co-occurring species. This concept has been proposed as a tool for determining the minimum size for conservation areas, selecting sites to be included in reserve networks, and setting minimum standards for the composition, structure, and processes of ecosystems. Among the species suggested as potential umbrellas, most are large mammals and birds, but invertebrates are increasingly being considered. Eighteen research papers, most of which were based on hypothetical reserves or conservation networks, have provided evaluations of umbrella species schemes. These show that single-species umbrellas cannot ensure the conservation of all co-occurring species because some species are inevitably limited by ecological factors that are not relevant to the umbrella species. Moreover, they provide evidence that umbrella species from a given higher taxon may not necessarily confer protection to assemblages from other taxa. On the other hand, multi-species strategies based on systematic selection procedures (e. g., the focal species approach) offer more compelling evidence of the usefulness of the concept. Evaluations of umbrella species schemes could be improved by including measures of population viability and data from many years, as well as by comparing the efficiency of the proposed scheme with alternative management strategies.

Full text

Usefulness of the Umbrella Species Concept
as a Conservation Tool
JEAN-MICHEL ROBERGE∗‡ AND PER ANGELSTAM∗†
∗Grims¨o Wildlife Research Station, Department of Conservation Biology, Forest Faculty, Swedish University
of Agricultural Sciences (SLU), SE-730 91 Riddarhyttan, Sweden
†Department of Natural Sciences, Centre for Landscape Ecology, ¨
Orebro University, SE-701 82 ¨
Orebro, Sweden
Abstract: In the face of limited funding, knowledge, and time for action, conservation efforts often rely on
shortcuts for the maintenance of biodiversity. The umbrella species concept—proposed as a way to use species
requirements as a basis for conservation planning—has recently received growing attention. We reviewed the
literature to evaluate the concept’s general usefulness. An umbrella species is defined as a species whose con-
servation is expected to confer protection to a large number of naturally co-occurring species. This concept
has been proposed as a tool for determining the minimum size for conservation areas, selecting sites to be
included in reserve networks, and setting minimum standards for the composition, structure, and processes
of ecosystems. Among the species suggested as potential umbrellas, most are large mammals and birds, but
invertebrates are increasingly being considered. Eighteen research papers, most of which were based on hypo-
thetical reserves or conservation networks, have provided evaluations of umbrella species schemes. These show
that single-species umbrellas cannot ensure the conservation of all co-occurring species because some species
are inevitably limited by ecological factors that are not relevant to the umbrella species. Moreover, they provide
evidence that umbrella species from a given higher taxon may not necessarily confer protection to assemblages
from other taxa. On the other hand, multi-species strategies based on systematic selection procedures (e.g., the
focal species approach) offer more compelling evidence of the usefulness of the concept. Evaluations of um-
brella species schemes could be improved by including measures of population viability and data from many
years, as well as by comparing the efficiency of the proposed scheme with alternative management strategies.
Utilidad del Concepto de Especie Paraguas como Herramienta de Conservaci´on
Resumen: Ante la escasez de financiamiento, de conocimiento y tiempo para actuar, los esfuerzos de con-
servaci´
on a menudo conf´
ıan en m´
etodos r´
apidos para el mantenimiento de la biodiversidad. El concepto
de especie paraguas - propuesto como una manera de utilizar los requerimientos de las especies como base
para la planeaci´
on de conservaci´
on – ha recibido mayor atenci´
on recientemente. Revisamos la literatura para
evaluar la utilidad general del concepto. Una especie paraguas se define como una especie cuya conservaci´
on
conferir´
ıa protecci´
onaungrann
´
umero de especies que coexisten naturalmente. Este concepto se ha propuesto
como una herramienta para determinar el tama˜
no m´
ınimo de ´
areas de conservaci´
on, seleccionar sitios a
incluir en redes de reservas y para fijar las normas m´
ınimas para la composici´
on, estructura y procesos de los
ecosistemas. La mayor´
ıa de las especies que se sugieren como paraguas potenciales son mam´
ıferos y aves may-
ores, pero se est´
an considerando a los invertebrados cada vez m´
as. Dieciocho art´
ıculos cient´
ıficos, la mayor´
ıa
basados en reservas o redes de conservaci´
on hipot´
eticas, han proporcionado evaluaciones de proyectos con
especies paraguas. Estos muestran que una sola especie paraguas no puede asegurar la conservaci´
on de todas
las especies coexistentes porque algunas especies inevitablemente est´
an limitadas por factores ecol´
ogicos que
no son relevantes para la especie paraguas. M´
as aun, proporcionan pruebas de que especies paraguas de un
tax´
on alto determinado necesariamente no confiere protecci´
on a los conjuntos de otros taxones. Por otro lado,
estrategias multiespec´
ıficas basadas en procedimientos de selecci´
on sistem´
aticos (por ejemplo, el m´
etodo de la
especie focal) ofrecen evidencia m´
as convincente de la utilidad del concepto. Se debe mejorar la evaluaci´
on
‡email jean-michel.roberge@nvb.slu.se
Paper submitted October 23, 2002; revised manuscript accepted April 21, 2003.
76
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Roberge & Angelstam Umbrella Species and Conservation 77
de los proyectos de especies paraguas incluyendo medidas de viabilidad poblacional, datos de muchos a˜
nos,
as´
ıcomo comparando la eficiencia del proyecto propuesto con estrategias de manejo alternativas.
Introduction
Following the emergence of the concept of biological
diversity, conservation biologists showed growing inter-
est in developing shortcuts to the conservation of whole
biota. The umbrella species concept has been proposed
as a way to use species requirements to guide ecosystem
management. Its main premise is that the requirements
of demanding species encapsulate those of many co-
occurring, less demanding species (Lambeck 1997). By
directing management efforts toward the requirements
of the most exigent species, one is likely to address the
requirements of many cohabitants that use the same habi-
tat. The umbrella species concept is intuitively appealing
and offers a simple, ecologically based shortcut for the
management of communities. Yet the assumption that
providing for the requirements of a few species results
in the protection of most species present in the same
area rarely has been addressed rigorously. Indeed, many
authors have recently made a plea for the empirical valida-
tion of this concept (Caro & O’Doherty 1999; Simberloff
1999; Angelstam et al. 2001; Fleishman et al. 2001).
Although the umbrella species concept has been dis-
cussed in the biological conservation literature, no com-
prehensive review has been made that allows assessment
of its general utility as a conservation tool. Some authors
have discussed this concept more thoroughly than others
(e.g., Simberloff 1998; Caro & O’Doherty 1999; Zacharias
& Roff 2001; Caro 2003), but their accounts—although
rich in insight—do not cover all its variants or extensively
examine the empirical evidence for its utility. We sought
to (1) review the history of the umbrella species concept
and distinguish its different uses, (2) evaluate the extent
to which the concept has been validated empirically, and
(3) suggest directions for using umbrella species in con-
servation planning.
History and Uses of the Umbrella Species Concept
The exact origin of the umbrella species concept is neb-
ulous. To our knowledge, Frankel and Soul´e (1981) were
the first to use the term umbrella to suggest that con-
servation measures directed at the largest species could
confer protection to what they called “denser species.”A
few years later Wilcox (1984) proposed that management
focus on those species whose habitat requirements are
“at least as comprehensive as that of the rest of the com-
munity,”thus providing a “protective umbrella”for other
species. Other authors had put forward the same basic
idea before that, although without using the term um-
brella (Eisenberg 1980; East 1981; Mealy & Horn 1981).
Therefore, this concept was probably used implicitly be-
fore it was defined (Caro 2003). The biological conserva-
tion literature from the 1980s includes a number of ref-
erences to the umbrella species concept (e.g., Ehrlich &
Murphy 1987; Murphy 1988; Peterson 1988), but most of
these papers only state the theoretical appeal of that con-
cept without evaluating its validity. Since the beginning
of the 1990s, attention to the umbrella species approach
has grown. Instead of merely discussing the appeal of
this idea, many researchers have critically examined the
potential usefulness of proposed umbrella taxa for man-
agement (e.g., Ryti 1992; Beier 1993; Launer & Murphy
1994; Berger 1997; New 1997; Fleury et al. 1998), and
others have suggested ecologically based methods or cri-
teria for the selection of umbrella species (e.g., Lambeck
1997, 1999; Caro & O’Doherty 1999; Fleishman et al.
2000, 2001).
Definitions
A large number of definitions have been proposed for
umbrella species that emphasize different uses and prop-
erties (Zacharias & Roff 2001). This has resulted in some
confusion about the meaning of the term. Fleishman et al.
(2000) recently suggested a broadly applicable definition
for an umbrella species: a “species whose conservation
confers a protective umbrella to numerous co-occurring
species.”This definition is somewhat tautological, how-
ever, because it includes the term umbrella. A potentially
consensual alternative could be a species whose conser-
vation confers protection to a large number of naturally
co-occurring species. We use this general definition as a
basis throughout this review and define narrower vari-
ants of the concept in context-specific applications. We
use the phrase umbrella scheme to describe any pro-
posed conservation plan based on one or several umbrella
species. The co-occurring species that are likely to be pro-
tected by conservation activities directed at the umbrella
species are hereafter referred to as beneficiary species.
Several more or less overlapping subconcepts of umbrella
species can be distinguished, all of which conform to our
general definition.
Umbrella Species with Large Area Requirements
In its classic form and at the local scale, the umbrella
species concept refers to the minimum area requirements
of a population of a wide-ranging species (Wilcox 1984).
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78 Umbrella Species and Conservation Roberge & Angelstam
It hinges on the assumption that providing enough space
for species with large area requirements will also shelter
a whole suite of species with more modest spatial needs.
Because organisms with a large body size also tend to
have large home ranges (McNab 1963), maintaining vi-
able populations of those species requires the conserva-
tion of large tracts of habitat. For that reason, large-bodied
organisms have been favored as prospective umbrellas.
Species in this category are usually vertebrates, typically
large mammalian carnivores (Eisenberg 1980; East 1981;
Peterson 1988; Shafer 1990; Noss et al. 1996; Carroll et al.
2001), herbivores (Mealy & Horn 1981; Wallis de Vries
1995; Berger 1997), or birds (Martikainen et al. 1998;
Suter et al. 2002).
Umbrella Species Used to Select Sites
In addition to its use in determining minimum area for
protection, the umbrella species concept has been pro-
posed as a tool for defining reserve networks at larger
geographic scales. In the site-selection umbrella concept,
the occurrence of single- or multi-species umbrellas, or,
alternatively, the species richness of an umbrella taxon, is
used as a basis for the selection of sites—habitat patches,
ecosystems, planning units, or even large grid squares—
to be preserved in a conservation network. The general
methodology consists of setting aside for protection the
totality or a given proportion of the sites where the um-
brella(s) occur(s) or where species diversity for the um-
brella taxon is high (Kerr 1997). It is presumed that pop-
ulations of a number of beneficiary species should be
protected in the network (Ryti 1992; Launer & Murphy
1994; Kerr 1997; Fleishman et al. 2000, 2001).
The Extended Umbrella Concept
The umbrella species concept builds on the assumption
that the requirements of demanding species should en-
compass those of many other species (Lambeck 1997).
This assumption is stated explicitly for area needs in the
subconcept of area-demanding umbrella species. But why
should this tool be restricted to area requirements? In a
variant that we would like to call the extended-umbrella
species concept, the basic idea is broadened to include
other attributes of landscapes such as habitat connectiv-
ity, the occurrence of various ecosystem processes, or the
distribution of scarce resources. For example, Fleury et al.
(1998) and van Langevelde et al. (2000) used, respectively,
the California Gnatcatcher (Polioptila californica) and
the European Nuthatch (Sitta europaea) as umbrella bird
species for reserve network planning. Instead of using
only the occurrences or area requirements of these birds
for reserve site selection, they also considered their need
for connectivity. Fleury et al. (1998) did so by simulating
movement corridors to link subpopulations, whereas van
Langevelde et al. (2000) used threshold between-patch
distances for allowing dispersal in the umbrella species.
The underlying assumption here is that landscapes that
are sufficiently connected for the umbrella species should
also be functional for many other species.
Lambeck (1997) gave new life to the umbrella species
idea by extending it to a large range of factors that threaten
species persistence in managed landscapes. He proposed
to identify a suite of “focal species”that would be used
to define the spatial, compositional, and functional at-
tributes that must be present in a landscape. Lambeck’s
process involves identifying the main threats and select-
ing focal species among the species that are most sensi-
tive to each threat. The requirements of those species
would then be used to guide conservation or restora-
tion. Thus, the focal species approach is consistent with
the general definition of umbrella species. It simply goes
beyond earlier approaches by addressing habitat quality
and by proposing systematic criteria for the selection of
a suite of umbrella (“focal”) species. Lambeck (1997)
suggests four threat categories for focal species: area-
limited, resource-limited, dispersal-limited, or process-
limited. Each of these categories should be represented
by one or a few focal species.
By reviewing the conservation biological literature on
the umbrella species concept, we assessed the relative
prevalence of (1) the main variants of the concept and
(2) the different taxa proposed as umbrellas. We exam-
ined biological database information and reference lists
from relevant papers. We only considered papers pub-
lished in English. In this review we included 110 peer-
reviewed articles, book chapters, and papers from con-
ference proceedings that discussed the umbrella species
concept. Papers dealing with this concept without using
the term umbrella were included if they complied with
one of the three variants of the concept described above.
Because we addressed an applied science issue, we also
considered published governmental research papers and
technical reports. We evaluated papers that dealt with
one or more of the three main umbrella categories (Ta-
ble 1). Not surprisingly, mammals, birds, and to a lesser
extent—insects dominate as suggested or evaluated um-
brella species. Although mammals have often been pro-
posed as area-demanding umbrellas, birds and insects
seem to have been preferred for the site-selection and
extended-umbrella concepts.
Evaluating the Umbrella Species Concept
If the umbrella species concept is to be promoted from an
interesting management hypothesis or social hook (Lin-
denmayer & Fischer 2003) to an actual conservation tool,
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Roberge & Angelstam Umbrella Species and Conservation 79
Table 1. The main variants of the umbrella species concept in the biological conservation literature.∗
Number of papers suggesting or evaluating different taxa
Total no. of papers
Umbrella species category Field of application discussing concept mammals birds herptiles fish invertebrates plants no suggestion or evaluation
Area-demanding umbrella setting the minimum size for
a nature reserve
56 23 6 1 0 0 1 29
Site-selection umbrella prioritizing of patches to be
included in a reserve
network
15 4 7 1 1 6 3 2
Extended umbrella concept,
including the focal-species
approach
setting minimum values for
landscape composition,
configuration, resources, or
processes
48 8 16 3 1 12 1 24
All categories 110 31 26 5 2 18 4 51
∗Based on 110 reviewed papers. Rows and columns are not additive because one paper may discuss several umbrella categories and suggest or evaluate species from several taxa.
it is crucial that the approach be validated empirically. A
common remark is that the umbrella species concept has
rarely if ever been tested (Simberloff 1999). Contrary to
classic scientific hypotheses, the umbrella species con-
cept is not subject to falsification (Lindenmayer et al.
2002). Obviously, lack of support for the validity of the
concept in certain conditions does not constitute a proof
of the general invalidity of the tool. Moreover, the results
of such “tests”usually cannot be classified simply as suc-
cesses or failures in a binary manner, but must rather be
evaluated according to some quantitative measure.
To be considered for empirical evaluation of the um-
brella species concept (Table 2), a study had to fulfill two
criteria. First, it had to present an evaluation of a hypo-
thetical or actual conservation scheme (e.g., spatially de-
limited reserve or network) based on an umbrella species.
Merely describing general patterns of co-occurrence over
an entire region provides information on the indicator
value of the different species but is not sufficient for con-
stituting an evaluation of the umbrella function. Second,
the study had to provide a quantitative measure of the
level of protection conferred to beneficiary species, such
as the number of species represented in the conservation
network or the probability of beneficiary species main-
taining viable populations. Among the 110 research pa-
pers we included in this review, only 18 evaluated the
performance of an umbrella species scheme according to
these criteria.
Evaluations of Area-Demanding Umbrella Species
Most empirical evaluations of the umbrella species con-
cept based on area requirements suggest that it has a lim-
ited effectiveness (Table 2). Noss et al. (1996) investigated
the umbrella value of proposed grizzly bear (Ursus arc-
tos) recovery zones by looking at how many species of
different taxa would have more than 10% of their state-
wide distribution captured by the conservation plan (i.e.,
a surrogate for population viability). Although birds, mam-
mals, and amphibians would be well covered, other taxa
such as reptiles would be underrepresented. A recent
study by Carroll et al. (2001) based on modeling habitat
suitability for the grizzly bear, fisher (Martes pennanti),
lynx (Lynx canadensis), and wolverine (Gulo gulo) il-
lustrated the need for a multi-species approach if those
carnivores are to be used as umbrella species. Unfortu-
nately, these authors only assessed the overlap in prior-
ity areas among those four carnivores and did not evalu-
ate the umbrella function for other species. In an evalua-
tion of the black rhinoceros (Diceros bicornis)asanum-
brella species, Berger (1997) used a different approach.
He examined the umbrella value of the rhinoceros for six
large herbivore species by calculating the frequency with
which the mean population size for each species would
be maintained at a given level within the area needed by
the rhinoceros population. Annual differences in rainfall
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80 Umbrella Species and Conservation Roberge & Angelstam
Table 2. Evaluations of the usefulness of different types of umbrella species for conservation planning.
Umbrella species Investigated umbrella
category and citation Ecosystem type taxon/taxaaTargeted beneficiary taxa Protection conferredb
Area-demanding umbrella
Noss et al. 1996 Rocky Mountains, northern
U.S.
grizzly bear, Ursus arctos
(S)
amphibians, reptiles, birds,
mammals, and plant
communities
limited
Berger 1997 African desert black rhinoceros, Diceros
bicornis (S)
six large herbivore species limited
Martikainen et al.
1998
boreal forest, Fennoscandia White-backed
Woodpecker,
Dendrocopos leucotos
(S)
threatened saproxylic
beetles
limited
Andelman & Fagan
2000
diverse regions of the
continental U.S.
large carnivores of concern
(S,M)
species “of concern”from
various taxa
limited to ineffective,
depending on databases
and on surrogate scheme
Andelman & Fagan
2000
diverse regions of the
continental U.S.
most widespread species
of concern, from diverse
taxa (M)
species “of concern”from
various taxa
limited to ineffective,
depending on databases
and on surrogate scheme
Caro 2001 East African deciduous
forests, floodplains, and
fields
large mammals (M) small, nonvolant mammals ineffective
Suter et al. 2002 alpine coniferous forests,
Switzerland
Capercaillie, Tetrao
urogallus (S)
birds effective for red-listed
mountain birds;
ineffective for bird
diversity in general
Caro 2003 East African deciduous
forest
large mammals (M) large and middle-sized
mammals, small
carnivores, small native
rodents and insectivores
effective for large and
middle-sized mammals as
well as small carnivores;
ineffective for rodents
and insectivores
Site-selection umbrella
Murphy & Wilcox
1986
high-elevation boreal
habitats separated by
arid scrub; canyon
riparian habitats,
western North America
birds and mammals (M) butterflies limited to effective,
depending on spatial
scale
Ryti 1992 islands and canyons of
southwestern U.S.
plants and birds (M) plants, birds, mammals,
and reptiles
limited (birds) to effective
(plants)
Launer & Murphy
1994
serpentine soil-based
grasslands, southwestern
U.S.
bay checkerspot butterfly,
Euphydryas editha
bayensis (S)
plants limited
Kerr 1997 North America north of
Mexico
mammalian carnivores (M) invertebrates ineffective
Andelman & Fagan
2000
diverse regions of the
continental U.S.
habitat specialists of
concern, from diverse
taxa (M)
species “of concern”from
various taxa
limited to ineffective,
depending on databases
and on surrogate scheme
Fleishman et al.
2000
mountain canyons in the
Great Basin, western U.S.
butterflies (M) butterflies effective
Fleishman et al.
2001
coastal chaparral
shrubland; eastern
broadleaf forest; xeric
shrub steppe, North
America
butterflies and birds (M) butterflies and birds effective within taxa;
limited across taxa
Poiani et al. 2001 mixture of grassland and
forest, northern U.S.
Greater Prairie Chicken,
Tympanuchus cupido
(S)
rare plants and animals,
natural communities
limited
Rubinoff 2001 coastal sage scrub,
southwestern U.S.
California Gnatcatcher,
Polioptila californica (S)
three specialized insect
species (Lepidoptera)
ineffective
Bonn et al. 2002 southern Africa threatened and/or endemic
birds (M)
birds limited
Extended umbrella species concept
Fleury et al. 1998 coastal sage scrub,
southwestern U.S.
California Gnatcatcher (S) plant and animal species of
concern
limited
Watson et al. 2001 temperate woodland
remnants, southeastern
Australia
Hooded Robin,
Melanodryas cucullata,
and Yellow Robin,
Eopsaltria australis (M)
woodland birds effective with ideal
guidelines; limited with
less stringent guidelines
adapted to the social
context
aAbbreviations: S, single-species umbrella; M, multispecies umbrella.
bInterpretation (by the authors of this review) of the original authors’conclusions. The protection conferred by the umbrella scheme was
summarized in three classes: effective, limited, and ineffective.
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Roberge & Angelstam Umbrella Species and Conservation 81
caused fluctuations in population size and movements
for the six species, but the rhinoceros populations did
not vary accordingly. Berger (1997) concluded that the
population of 28 rhinoceroses was unlikely to assure the
populations of the other species in excess of 250 individ-
uals.
In East Africa, Caro (2001, 2003) observed that pop-
ulations of edible ungulates and small carnivores were
lower outside than inside a national park designed for
large mammals. On the other hand, average species diver-
sity and abundance of small mammals were greater out-
side than inside the reserve. Based on these observations
he concluded that delineating a reserve using umbrella
species may benefit populations of some background taxa
but by no means all. As discussed by Caro (2001), in such
studies it is crucial to consider the identity of the potential
beneficiary species in addition to their richness and abun-
dance. Attention should be given to the species of con-
cern that are sensitive to human disturbances (e.g., Fleury
et al. 1998; Lambeck 1999; Andelman & Fagan 2000). In
an assessment of the potential of the Capercaillie (Tetrao
urogallus) as an umbrella species, Suter et al. (2002) ex-
amined separately the umbrella effect for all bird species
and for mountain species of concern included in the Swiss
Red List. The distribution of the capercaillie was related
to high species richness in mountain birds of concern,
but this was not the case when ubiquitous bird species
were included in the analyses.
Suter et al.’s (2002) study provided one of the few ex-
amples of substantial support for the concept of area-
demanding umbrella species. This is explained by the
fact that they considered variations in vegetation struc-
ture in their study area and addressed the question of
whether the potential beneficiary species had, as a group,
specialized habitat requirements similar to those of the
umbrella species. Similarly, Martikainen et al. (1998) pro-
vided evidence for the potential umbrella value of the
White-backed Woodpecker (Dendrocopos leucotos)for
threatened beetles dependent on the same resources—
that is, decaying deciduous wood within successional
deciduous forest. Contrary to the approaches of Suter
et al. (2002) and Martikainen et al. (1998), however, most
other approaches to the concept of area-demanding um-
brella species have been based coarsely on the area re-
quirements of the purported umbrella species without
attention to the habitat needs of the potential beneficiary
species.
Evaluations of Site-Selection Umbrella Species
The different evaluations of the site-selection umbrella
concept have yielded varied results (Table 2). Murphy
and Wilcox (1986) demonstrated that the validity of
vertebrate-based management for maintaining butterfly
diversity is scale dependent. They concluded that re-
gional management of vertebrates would probably pro-
vide for the requirements of invertebrates, but that inten-
sive fragmentation on a local scale may cause declines in
invertebrates without affecting vertebrates. Kerr (1997),
however, provided evidence that a hypothetical system
of large-scale reserves designed to include all carnivore
species in a minimum of sites would not provide good pro-
tection for invertebrates. For gulf islands and canyons in
California, Ryti (1992) found that a reserve network con-
taining at least one occurrence of all plant species found in
the regional pool covered vertebrates well, whereas such
a network for birds did not provide equivalent protection
for other taxa. However, the plant network required set-
ting aside an area much larger than the area needed for
the bird network. Thus, the relative performance of these
two taxa as umbrellas surely would have been different
had issues of efficiency been considered.
Using occurrence data for species of concern from a
variety of taxa, Andelman and Fagan (2000) evaluated a
variety of site-selection umbrella schemes and compared
their efficiency to that of random sets of species. Only
a few umbrella schemes proved more efficient than ran-
dom schemes made up of similar numbers of species. On
this basis, they concluded that there is little evidence sup-
porting the utility of umbrella species. One limitation of
their study is that they automatically included in a given
surrogate scheme all species in the databases that fulfilled
the selection criteria for that scheme. For example, their
“habitat specialist”scheme was based on the occurrences
of all habitat specialist species found in the databases, re-
sulting in the need to set aside a very large proportion
of the sites. Many such schemes performed well in terms
of species protection but were excessively costly (and
thereby less efficient) because they required too many
conservation areas. Hence, these authors showed that
multi-species schemes might fail to provide an efficient
management alternative if the suite of umbrella species
were selected without addressing issues of parsimony or
complementarity. In Southern Africa, Bonn et al. (2002)
simulated complementary networks representing threat-
ened and endemic birds with the minimum possible num-
ber of conservation areas and assessed whether many
other bird species would be conserved in these areas.
These networks performed better than random schemes,
although they did not guarantee the representation of
overall species diversity.
Fleishman et al. (2001) evaluated different site-selec-
tion umbrella strategies of butterflies and birds and com-
pared their efficiency to that of random schemes. They
ranked species according to their value as umbrellas based
on three criteria: medium rarity, sensitivity to human dis-
turbance, and percentage of co-occurring species (Fleish-
man et al. 2000). Their multispecies umbrella schemes
proved to be efficient conservation tools that allowed the
area to be set aside for achieving a given level of species
protection to be minimized. Launer and Murphy (1994),
Poiani et al. (2001), and Rubinoff (2001) assessed the
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82 Umbrella Species and Conservation Roberge & Angelstam
validity of a butterfly, a tetraonid bird, and a passerine
bird as single-species umbrellas for plants, rare animals
and plants, and invertebrate species, respectively (Table
2). They came to a common conclusion: single species are
unlikely to function as effective site-selection umbrellas
for the protection of other taxonomic groups.
Most of those researchers used the occurrences of the
umbrella species as a basis for reserve site selection and
assumed complete data sets. It is possible that some of the
recorded absences of the umbrella species were due to
imperfections of the inventory technique. In such cases,
the planner would fail to include some of the sites that
should actually be set aside for protection. On the other
hand, incomplete data sets on the occurrences of the po-
tential beneficiary species would result in an underesti-
mation of the efficiency of the umbrella scheme.
Evaluations of the Extended Umbrella Concept
The extended umbrella concept has rarely been eval-
uated (Table 2). Fleury et al. (1998) designed a hypo-
thetical reserve for the California Gnatcatcher, including
corridors to connect subpopulations and buffer zones.
It afforded only limited protection to red-listed animal
and plant species because some species required local-
ized habitat types or had area needs larger than those
of the gnatcatcher. Thus, this species alone cannot pro-
vide the basis from which to derive minimum standards
for landscape attributes in this coastal sage scrub ecosys-
tem (see also Rubinoff 2001). Similarly, proposed re-
serves for the Northern Spotted Owl (Strix occidentalis)
in the Pacific Northwest were insufficient to conserve
Marbled Murrelets (Brachyramphus marmoratus) and
some aquatic ecosystems (summarized in Franklin 1994;
Wilcove 1994), which is not surprising given that the
owl lives on land. Bonn and Schr¨oder (2001) and Ranius
(2002) partially evaluated the potential of carabid beetles
as umbrella species. Although these researchers provided
evidence for the indicator value of their target beetle
species, they did not (contrary to the studies included in
Table 2) evaluate any hypothetical conservation scheme
based on their prospective umbrella species.
The focal species approach has been only partially val-
idated. The focal species selection process has been ap-
plied in a few case studies in Australia (Lambeck 1999;
Brooker 2002), Italy (Bani et al. 2002), and the United
States (Hess & King 2002), but these investigations did
not include evaluation of the umbrella function of the se-
lected species. In eastern Australia, Watson et al. (2001)
proposed concrete guidelines for conservation planning
based on the needs of sensitive birds and modeled the
probability of occurrence of different species in rem-
nants of various size and habitat complexity. They con-
cluded that their revegetation guidelines would provide
habitat for about 95% of the resident woodland birds in
the region.
Synthesis
Evaluations of the subconcept of area-demanding um-
brella species provide little support for its utility for the
conservation of biodiversity as a whole. Conservation
schemes based uniquely on area requirements will in-
evitably be flawed unless they also incorporate the needs
of sensitive species requiring specialized habitat types.
The site-selection umbrella species concept, on the other
hand, appears more useful. The umbrella value of single
species is generally low because some species are lim-
ited by ecological factors that are not relevant to the
umbrella species. However, rigorous assessments using
multiple species and systematic selection criteria show
that umbrella species can be an effective tool for pri-
oritizing remnants to be included in conservation net-
works (e.g., Fleishman et al. 2000, 2001). The extended-
umbrella species concept has rarely been evaluated. Lam-
beck’s (1997) focal species approach has been assessed
only partially, and it remains to be seen whether land-
scapes designed for the most sensitive suite of species
can retain nearly all co-occurring species.
What would constitute a robust, empirical evaluation
of the umbrella species concept? The examples provided
above stress the need to measure the efficiency of the
umbrella scheme—that is, to present the results in the
form of a ratio of the benefits (e.g., number of species or
habitat types protected) to the costs (e.g., total area or
number of sites required). This allows for comparison of
the efficiency of the umbrella scheme with that of alter-
native strategies. A number of researchers have looked
at whether the umbrella schemes performed significantly
better than random schemes or null models (Andelman
& Fagan 2000; Fleishman et al. 2001; Poiani et al. 2001).
Although this makes sense from a statistical point of view,
one may wonder whether more ecologically relevant cri-
teria could be used instead. For instance, comparing the
effectiveness of an umbrella scheme with that of measures
based on general ecological principles would be much
more informative from a management perspective (Poiani
et al. 2001). Examples of such measures could be restora-
tion of a nominated proportion of a landscape to create a
variety of patches of the main native land types, planning
for corridors between isolated patches, and restoration of
watercourses and associated riparian vegetation (Hunter
1999; Lindenmayer et al. 2002).
Another limitation of many evaluations of the umbrella
species concept is that they often rely on presence and
absence “snapshot”data without distinguishing between
viable or extinction-prone populations (Ryti 1992; Andel-
man & Fagan 2000; Fleishman et al. 2001; but see Berger
1997; Fleury et al. 1998; Bonn et al. 2002). In landscapes
where fragmentation is a relatively recent phenomenon,
some populations in remnants may be sinks or transients
(Watson et al. 2001). Moreover, metapopulation theory
predicts that a number of suitable patches are unoccupied
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Roberge & Angelstam Umbrella Species and Conservation 83
at any point in time (Hanski 1999). Therefore, data cov-
ering many years is preferable for assessing the viability
of the (sub)populations and increasing the likelihood of
including all suitable habitat in the conservation network.
Moreover, because many species vary in their habitat re-
quirements at different times of the year, surveys should
ideally cover more than one season.
Finally and most important, none of the studies listed in
Table 2 (except Caro 2001, 2003) provides a direct evalu-
ation of the basic assumption of the umbrella species con-
cept, to show that the conservation measures directed at
the umbrella species actually protect many other species.
Their conclusions are based on hypothetical reserves or
conservation networks derived from current species dis-
tributions, which in turn are dependent on the current
structures of landscapes. Hence, they do not demonstrate
that the implementation of the conservation schemes in
the real world would give the same results. This remains
the greatest challenge in evaluating the umbrella species
concept. In that respect, investigations such as Caro’s
(2001, 2003) based on data from existing protected ar-
eas and their surroundings are of great interest.
Directions for Using Umbrella Species
in Conservation Planning
A frequent criticism of the umbrella species concept is
that it is improbable that the requirements of one species
would encapsulate those of all other species (Noss et al.
1997; Basset et al. 2001; Hess & King 2002). Evaluations
of the utility of single-species umbrellas have shown con-
vincingly that they do not offer total coverage for whole
communities (Table 2). Hence, there is a need for multi-
species strategies as a means to broaden the width of
the protective umbrella (e.g., Miller et al. 1998; Fleish-
man et al. 2000, 2001; Carroll et al. 2001). Among the
different multi-species approaches, Lambeck’s (1997) fo-
cal species approach seems the most promising because
it provides a systematic procedure for selection of um-
brella species (Lambeck 1999; Watson et al. 2001; Bani et
al. 2002; Brooker 2002; Hess & King 2002).
What qualities should a “dream team”of focal species
possess to be a dependable tool of biodiversity assess-
ment and conservation planning? First, it should cover
the main ecosystem or landscape types of concern in a re-
gion (Angelstam 1998a, 1998b; Hess & King 2002). Here
it might be argued that simply conserving all landscape
types would constitute a more straightforward alterna-
tive. However, given the need to establish concrete and
quantitative landscape design criteria, it is essential to re-
fer to the requirements of the species to know how much
is enough (Hansen et al. 1993; Lambeck 1997, 1999; An-
gelstam et al. 2003). For each landscape type, the most
sensitive group of species in terms of resources, area
requirements, connectivity, and natural processes (e.g.,
fire and flooding regimes) should be selected (Lambeck
1997). Depending on the context of application, the suite
of focal species may need to represent a range of spatial
scales from bioregions and landscapes (Lambeck 1999) to
localized habitats and microhabitats (M¨uhlenberg et al.
1991). In forested landscapes, for example, birds and
mammals may include species that are among the most
sensitive to threatening factors operating at landscape and
bioregional scales (Lambeck 1999), whereas species of in-
vertebrates and nonvascular plants could be among the
most sensitive to threats operating at finer spatial scales
(Angelstam 1998a; Ranius 2002).
One shortcoming of the focal species approach lies in
the difficulty of identifying the most sensitive species for
each threat, given that many taxa are still poorly known
(e.g., invertebrates) (Lindenmayer et al. 2002; Linden-
mayer & Fischer 2003). Moreover, there is an obvious
lack of data about requirements that are difficult to study
quantitatively, such as dispersal (Koenig et al. 1996). New
knowledge on habitat thresholds for the persistence of
sensitive species (Fahrig 2001) will contribute to filling
those gaps. In the face of incomplete data, one can use
expert judgment obtained through workshops or surveys
(Lambeck 1999; Hess & King 2002).
Lindenmayer et al. (2002) assert that a ridiculously large
number of species may be needed and that this would ren-
der the focal species approach inefficient. Although this
certainly may be true in ecologically complex landscapes
such as those found in Australia (Clark 1990), develop-
ment of umbrella strategies based on a suite of species
may be attempted in simpler systems, such as boreal re-
gions. Yet it remains that multi-species umbrella strategies
require more data than do classic applications of single
area-demanding umbrellas. In situations where time is lim-
ited, a philosophy of adaptive management should be ad-
vocated (Walters 1986) whereby strategies based on such
multi-species umbrellas are implemented in some case
studies and are later improved or rejected as more knowl-
edge becomes available. In any case, such an approach
would represent a significant conservation shortcut com-
pared with species-by-species management or planning
for habitat re-creation after further destruction.
Conclusions
Species are going extinct at unprecedented rates, even
if we ignore the possibility of a considerable extinction
debt (Pimm et al. 1995; Hanski & Ovaskainen 2002). The
urgency of the situation leaves no room for “paralysis by
overanalysis”(sensu Carroll & Meffe 1994). It is no longer
legitimate to assert that the umbrella species concept has
not been tested and therefore should not be applied.
Although there is little evidence for the usefulness of
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84 Umbrella Species and Conservation Roberge & Angelstam
single-species umbrellas selected only on the basis of their
large area requirements, some multi-species schemes con-
sidering the occurrence of a range of habitat types and
landscape attributes offer promising conservation av-
enues. Using the umbrella species concept could there-
fore provide an appealing and sound approach for rapid
action.
The umbrella species concept is not a panacea. Even
the most sophisticated umbrella schemes probably can-
not guarantee the protection of absolutely all species. The
real issue, however, is whether the umbrella species con-
cept constitutes an effective conservation tool compared
with alternative methods. If used alone, general guide-
lines based on the conservation of the main native land
types would be difficult to implement because they do
not provide clear estimates of how much is needed of
different ecological attributes. On the other hand, the ex-
tended umbrella species concept provides explicit and
quantitative guidelines that could be useful for the as-
sessment of status and trends as well as for conserva-
tion planning. In the face of incomplete knowledge about
species requirements and ecosystem processes, the pre-
cautionary principle advises us to employ a combination
of methods. The umbrella species concept deserves con-
sideration as one of these.
Acknowledgments
A list of references for the literature summarized in Table 1
is available on request from the authors. We are grate-
ful to H. Andr´en, V.-A. Angers, M. B´elisle, T. M. Caro, L.
Gustafsson, L. Imbeau, G. Jansson, E. Main, G. Mikusin-
ski, M.-A. Villard, and two anonymous reviewers for their
comments on the manuscript. Financial support during
work on this review was provided by scholarships from
the Natural Sciences and Engineering Research Council
of Canada (NSERC) and Helge Axson Johnsons Fund to
J.-M.R., as well as grants from the World Wildlife Fund and
Mistra to P.A.
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