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Clavel J, Julliard R, Devictor V.. Worldwide decline of specialist species: toward

a global functional homogenization? Front Ecol Environ 9: 222-228

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 Frontiers in Ecology
and the Environment
Worldwide decline of specialist species:
toward a global functional
homogenization?
Joanne Clavel, Romain Julliard, and Vincent Devictor

Front Ecol Environ 2010; doi:10.1890/080216

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© The Ecological Society of America www.frontiersinecology.org
REVIEWS REVIEWS REVIEWS

Worldwide decline of specialist species:

toward a global functional homogenization?
Joanne Clavel*, Romain Julliard, and Vincent Devictor

Specialization is a concept based on a broad theoretical framework developed by evolutionary biologists

and ecologists. In the past 10 years, numerous studies have reported that – in many contexts – generalist
species are “replacing” specialist species. We review recent research on the concept of the ecological niche
and species specialization, and conclude that (1) the observed worldwide decline in specialist species is pre-
dicted by niche theory, (2) specialist declines cause “functional homogenization” of biodiversity, and (3)
such homogenization may be used to measure the impact of disturbance on communities. Homogenization
at the community level could alter ecosystem functioning and productivity, as well as result in the deterio-
ration of ecosystem goods and services. We propose community-level specialization as an indicator of the
impact of global changes (habitat and climate disturbances) on biodiversity.

Front Ecol Environ 2010; doi:10.1890/080216

D uring the past decade, several important studies have

revealed declines in specialist species, including
plants (Rooney et al. 2004), coral reef fish (Munday 2004),
ized by differences in their niche width (Figure 1).
Although a long-standing concept, niche theory still
influences the fields of evolutionary and behavioral ecol-
birds (Julliard et al. 2004), and mammals (Fisher et al. ogy (Kassen 2002; Bolnick et al. 2007) and could be useful
2003). Most of these studies have consisted of compila- for assessing the condition of ecological communities.
tions of large datasets, involving long-term observations. Specialization can be addressed in at least two ways: (1)
Researchers suggest that the observed declines were related performing laboratory-based experiments that examine
to disturbances to habitat and climate. Disturbances, the reaction norms, the expression of different genotypes
directly and indirectly, may cause the decline of specialist across a range of environments; specialists and generalists
species: habitat destruction (ie loss of habitat quantity) and would then be characterized according to the array of
degradation may lead to increased competition with gener- resources on which they can survive, as well as their
alists, as well as to extinction or extirpation of specialists growth rate in relation to these resources; and (2) apply-
otherwise unable to adapt to changing conditions. ing habitat-suitability models (through generalized linear
Here, we used arguably the most influential concept of models, generalized additive models, or multivariate
ecology – the ecological niche (Hutchinson 1957) – to analysis), which mostly rely on explicit measurements of
investigate why specialists may be more sensitive than some niche dimensions.
generalists to ongoing global changes. By definition, a In this review, we first describe how recent, fundamen-
niche encompasses all that a species requires to ensure its tal developments in various subdisciplines of ecology
population viability in a given environment, as well as could explain why specialist species may be more vulner-
including its impacts on that environment (Chesson able than generalists to global changes. We then suggest
2000). Specialist and generalist species can be character- that the replacement of geographically local specialists by
geographically local generalists is central to the ongoing
process of functional homogenization (FH), which,
In a nutshell: together with taxonomic homogenization (TH), makes
• Long-term persistence of specialist species is adversely affected up what is known as biotic homogenization (BH) (Olden
by past and current global changes et al. 2004). Functional homogenization is the measure-
• Generalist species have effectively replaced specialist species, ment of the increase in spatial similarity of a functional
causing functional homogenization at the community level
• Functional homogenization could alter ecosystem functioning
variable over time. We argue that, from an ecological per-
and thus ecosystem goods and services spective, FH is of far more concern than TH, and that FH
• Functional homogenization as a measurement of the loss of should not be underestimated. Studies have asserted that
functional diversity could be used as a biodiversity indicator community ecology needs to account for functional traits
in order to understand the mechanisms underlying global
changes (McGill et al. 2006). Finally, we explore how FH
UMR5173 MNHN-CNRS-UPMC, Conservation des Espèces, processes may have consequences for ecosystem function-
Restauration et Suivis des Populations, Paris, France *(jclavel@ ing and discuss the future role of FH in conservation biol-
mnhn.fr) ogy. We believe that FH, because of its strong link to eco-

© The Ecological Society of America www.frontiersinecology.org

Specialization theory and application J Clavel et al.

response to an environment that is stable

Environmental gradient y
over space and time, whereas generalist
Specialist species strategies are more likely to be favored by
organisms in heterogeneous and per-
Generalist species
turbed environments (Futuyma and
Moreno 1988; Kassen 2002). In other
words, specialization is more likely to
occur in a relatively stable environment
Environmental gradient x
than in one more often subject to
changes (Scheiner 2002). Depending on
Niche width Reaction norm
the environmental grain – the perception
of environmental variation by organisms
relative to the lifetime of an individual
Proxy of fitness

(Levins 1968) – different kinds of gener-

Fitness
alists will be favored. In fine-grained
environments, all individuals experience
environmental heterogeneity within
Environmental gradient x Env 1 Env 2 Env 3 their own life cycle, while in coarse-
grained environments, individuals expe-
Figure 1. Concept of the ecological niche and two different measures of it. Env = rience different states of the environ-
environment. ment more indirectly, for example via
gene flow to other individuals or via their
logical theory and its widespread occurrence, is a reliable progeny. Versatile generalists (ie those that exhibit
indicator of the impact of global change on biodiversity. reversible phenotypic responses to the prevailing envi-
ronmental conditions) might be expected to evolve in
n Vulnerability of specialist species: what does fine-grained environments, whereas plastic generalists
theory tell us? (ie those that exhibit adjustable responses early in
development, but fixed phenotypes thereafter) might be
Specialization: a broad theoretical framework expected to evolve in coarse-grained environments
Ecological niche theory is a synthesis of all of the interac- (Kassen 2002). In a metapopulation model, Marvier et
tions between a species and its environment (Hutchinson al. (2004) found that habitat destruction and fragmen-
1957; Chesson 2000). This concept therefore combines tation favored habitat invasion by generalist species,
the ecological requirements of the species and its func- despite the costs of reduced competitive ability.
tional role in communities. The dichotomy between gen-
eralists and specialists is based on a tradeoff between the Past and current evidence of specialist decline
capacity to exploit a range of environmental conditions
and their ability to use each one (Futuyma and Moreno Paleontology and records of specialist species
1988). For example, a field experiment on coral reef Fossil records provide an incomplete archive of the nat-
fishes (Caley and Munday 2003) showed that specialists ural history of certain taxa, allowing researchers to esti-
grew faster than generalists in one or two habitats, but mate extinction rates. These data show that, over geolog-
the generalists’ growth rate was more consistent between ical time, mass extinction events have been largely
a broader range of habitats. associated with the extinction of specialist species.
In practice, specialization has long been defined as a dis- Specialization in this regard is principally defined as diet
crete variable, depending on the biological model used. specialization quantified according to morphological
For instance, specialization has been measured in terms of parameters. Survival – as estimated from fossil records –
host diversity in organisms such as phytophagous insects varied in a non-random way among species, and the chal-
or parasites (Tripet et al. 2002). Continuous measurements lenge is to understand both the causes and the conse-
of specialization have been developed for different taxo- quences of extinction (Jablonski 2004). Many paleontolo-
nomic groups, including birds (Julliard et al. 2006), spiders gists have pointed out that, during past mass extinction
(Entling et al. 2007), and trees (Fridley et al. 2007), which events, generalists were less prone to extinction than spe-
facilitates the study of this trait in various contexts (eg dif- cialists (McKinney 1997). For example, opportunistic
ferent spatial scales and different trophic levels). species and ecological generalists among the foraminifera
and benthic marine invertebrates outlived other, more
Environmental variation and specialization specialized species in the early Jurassic (Erwin 1998). By
the end of the Cretaceous, more diet-specialized urchin
Environmental variation plays an important role in niche species were extinct than their generalist urchin counter-
evolution. Specialization is thought to be an evolutionary parts (Smith and Jeffery 1998). This suggests that special-

www.frontiersinecology.org © The Ecological Society of America

J Clavel et al. Specialization theory and application

ization may have led to increased chances of extinction A high degree of similarity between communities could
when the environment was disturbed. be the result of two scenarios: (1) the occurrence of many
Introduced species of the same species or (2) the disappearance of a large
number of extirpated species (Olden and Poff 2003).
Human activities, such as international trade, maricul- Beyond this BH, “winners” may also have less functional
ture, horticulture, and recreation, have resulted in the diversity, less complementary roles in the ecosystem
introduction of non-indigenous species around the world, process, than “losers”. This overall reduction of ecologi-
and some of these species have become invasive (Jeschke cal functional diversity is equivalent to FH. The replace-
and Strayer 2005). Among introduced species, generalists ment of specialist species by generalist species may pro-
are more likely to become successfully established. Seven vide an illustration of FH (Fisher and Owens 2004).
out of eight comparative analyses show a significant rela- Here, we simplify this concept, moving from the
tionship between establishment success and ecological restricted context of introduction–invasion to the gen-
specialization (in birds and fishes; Fisher and Owens eral context of human-perturbed ecosystems.
2004). This success among generalists may be the result Three mechanisms may dictate the outcome of global
of the higher probabilities of introduction and establish- change in the balance between specialist and generalist
ment, two crucial and interdependent stages in biological species abundances, and therefore, FH: (1) Global
introduction. changes may have direct negative effects on specialists,
Comparative analyses of species introductions have irrespective of the presence of generalists. This happens
mainly focused on birds, and the following examples – when the fitness of a specialist is reduced to the point
from which two key results emerge – all consider bird where it affects the local persistence of that species. For
species. First, populations of generalist species are, on aver- example, many European wetland species are declining
age, more abundant than populations of specialist species because wetlands have been disappearing throughout
(Kattan 1992) and are therefore more likely to be intro- Europe. Species adapted to that habitat are more affected
duced (Blackburn and Duncan 2001); both the number of because they cannot access the kinds of alternative
introductions and the number of introduced individuals resources that generalist species can. (2) Because they are
are crucial to the success of introduced species (Veltman et more flexible and innovative, as discussed earlier, gener-
al. 1996; Cassey et al. 2005). Second, because of their flexi- alist species may have the ability to colonize new niches
bility, generalists are often able to live in diverse habitats that have been created as a result of global change. For
and are thus more likely to establish in “new” ecosystems instance, generalist and specialist species are not similarly
(Cassey 2001). Wherever introduced, non-native general- lagging behind climate warming because they may also
ists have a better chance of finding necessary resources and have different abilities to track land-use change (Warren
appropriate environmental conditions (Duncan et al. et al. 2001). (3) In many cases, global changes may have
2003). Genetic variability is often associated with the the same positive (or negative) effects on both specialists
greater success of introduced species. Because generalist and generalists, but not to the same degree. Competition
species are introduced in large numbers, they may also induced by these differential responses determines the
have greater genetic diversity, and consequently, they may relative success of generalist species. For example, unusu-
be more successful in becoming established. ally warm spring seasons may favor the reproductive suc-
cess of all species, but may be more favorable for general-
n More generalists and fewer specialists: ists, owing to their greater adaptability. When climatic
consequences in natural communities conditions return to “normal”, resampling through
recruitment then favors the relatively more abundant
generalists (Julliard et al. 2004).
Functional homogenization
Finally, combinations of these three mechanisms may
Most species are declining as a result of human activities further promote the success of generalists. The responses of
(“losing species”) and are being replaced by a much smaller specialist and generalist species to additional changes may
number of species (“winning species”). Biotic homogeniza- differ to a greater extent if the surrounding community is
tion refers to the replacement of local species by other, already perturbed, as seen, for instance, in the greater suc-
more widespread species. In effect, this process “reshuffles” cess of introduced species in becoming established in dis-
existing species distributions and reduces spatial diversity. turbed areas (Levine et al. 2004) or in the presence of pre-
Ecologists have long been interested in one component – viously established exotic invasives (Facon et al. 2006).
TH (Elton 1958) – which describes an increased similarity
in community composition with the invasion of “winning The consequences of community changes on
species” and the extirpation of “losing species” (Baskin ecosystems
1998). However, TH is an inappropriate description of the
erosion of biodiversity, because introduced or expanding The phenomenon of FH raises numerous questions about
species can increase species richness and confound the BH the future of disturbed and transformed ecosystems on
concept (Olden and Poff 2003). ecological and evolutionary time scales. Species that are

© The Ecological Society of America www.frontiersinecology.org

Specialization theory and application J Clavel et al.

whole system, by decreasing the variability

Regional pool Generalist species in the communities’ responses to distur-
of species bance, and thereby decreasing potential
Specialist species with
specific functional trait landscape and regional buffering (Olden
2006). Indeed, having a range of species
that respond differently to environmental
Human-induced
Disturbance gradient perturbation can stabilize ecosystem pro-
environmental filter cesses (Hooper et al. 2005). Theoretical
studies have suggested the importance of
Locally niche partitioning (Loreau and de
structured Mazancourt 2008), although experimental
communities examples are still lacking (Hooper et al.
Complementarity 2005). Species and communities differ in
Functional homogenization their responses to disturbance. Although a
given specialist species may be more nega-
Figure 2. Diagram describing how loss of specialists engenders loss of functional tively affected by disturbance than a gener-
complementarity and thus functional homogenization. alist species, an entire (meta)community
composed of many specialized species
highly specialized are replaced by generalist species with should be relatively less affected, on account of greater
different or similar functions, yet the former perform less niche complementarity (Figure 2).
efficiently. How do changes at the community level alter Under suboptimal or variable conditions, and if the
ecosystem functioning and ecosystem productivity, and cost of generalization is less than the cost of coping with
do ecosystem services deteriorate in such circumstances? fluctuations, generalist species may also contribute to
Early models segregated species into functional groups more efficient ecosystem functioning (Richmond et al.
and assumed that species within such groups performed 2005). Under heterogeneous conditions, a community of
the same functions (Johnson et al. 1996). These models generalists could outperform a community of specialists
showed that functional characteristics, instead of diver- with respect to ecosystem functioning. In a global change
sity per se, strongly influenced ecosystem properties (Díaz context, the environmental tolerance of generalist
et al. 2007). Generalist species may be considered as species could be a determinant of ecosystem stability and
redundant, owing to their plasticity (Duarte et al. 1995), may also drive the relationship between diversity and
so their diversity is not fundamental to maintaining func- ecosystem functioning. Richmond et al. (2005) also ques-
tions at the ecosystem level, as long as all functional tioned the impact of FH on an ecosystem over an evolu-
groups are present. Some models, ie those that precisely tionary time scale and found that the replacement of spe-
accounted for species traits, assume that each species cialists by generalists changes the equilibrium of the
allows others to utilize resources differently (Tilman et al. ecosystem. How does FH affect adaptive dynamic ecosys-
2001); some species are complementary in their patterns tems? Can the system return to the initial equilibrium?
of niche occupation and can increase average rates of pro- Do generalists facilitate the establishment of other spe-
ductivity. Meanwhile, environmental conditions influ- cialist communities, or do generalist species stabilize the
ence the importance of complementarity for ecosystem ecosystem at a new equilibrium, as suggested by Rich-
productivity, which may be higher in resource-limited mond et al. (2005)? It is necessary to consider local inter-
conditions (Zhang and Zhang 2006) and when, over actions between specialists and generalists in order to
time, the stages of ecological succession advance (Tilman study the evolutionary dynamics of local FH within the
et al. 2001). Complementary responses may therefore be framework of adaptive dynamics theory.
directly linked with niche partitioning, and a species-rich
community composed of specialist species should lead to n Functional homogenization: an indicator of
higher resistance and better resilience than a community biodiversity loss
composed mostly of generalists.
Finke and Snyder (2008) used an aphid–parasitoid There has been considerable interest in the development
wasp–radish community to demonstrate experimentally of biodiversity loss indicators in order to meet the
that resource exploitation improved in the presence of Convention on Biological Diversity’s 2010 target. Ideally,
greater numbers of specialists, but not when generalist a biodiversity indicator should accurately reflect changes
diversity was increased. In this case, the ecosystem func- in biodiversity, link such changes appropriately to spe-
tion (ie parasite regulation) is better performed by spe- cific pressures, and be rooted in sound scientific theory
cialist parasitoid communities. (Balmford et al. 2005). The Marine Trophic Index is an
Functional homogenization should increase the syn- example of a functional indicator in marine ecosystems:
chronization between connected communities facing dis- based on food-web theory, it has proven its usefulness in
turbances. As a result, FH decreases the viability of the summarizing the impact of fisheries exploitation on

www.frontiersinecology.org © The Ecological Society of America

J Clavel et al. Specialization theory and application

Panel 1. Community specialization index: an indicator of functional homogenization

Julliard et al. (2006) have quantified the specialization of species as the coefficient of variation (standard deviation/average) of their den-
sities among habitat classes. This species specialization index (SSI) may be useful in building a sensitive (yet simple) index of biotic
homogenization at the community level. This community specialization index (CSI) could, in turn, be used to test the role played by
human-induced disturbances, such as habitat fragmentation, in functional biotic homogenization.
We used data from the French Breeding Bird Survey and considered 100 common species. We investigated the response of the CSI
to habitat fragmentation and quantified these pressures using a land-cover survey (CORINE Land Cover database; Figure 3). The CSI
was then calculated as the weighted average of the species specialization index in the site j (weighted by the number of individuals at
the j site).

Where N was the total number of species recorded, aij the abundance of
individuals of species i in plot j, and SSIi its specialization index.
Community specialization

(a) Farmland (b) Natural (c) Artificial

4.0 2.0 3.0
1.5 2.0
index (CSI)

3.0
2.0 1.0 1.0
0.5 0.0
1.0
0.0
0.0 –1.0
–0.5
–1.0 –1.0 –2.0
–2.0 –1.5 –3.0
0 5 10 15 20 25 30 0 5 10 15 20 25 30 0 5 10 15 20 25 30

Increasing fragmentation (km)

Figure 3. Relationship between the community specialization index (CSI) and landscape fragmentation within each habitat type.
We tested the relationships between the CSI and fragmentation (in kilometers) or disturbance using point counts monitored in (a)
farmland (n = 5087), (b) natural (n = 3210), or (c) artificial habitats (n = 1544). Smoothed curves were obtained with
generalized additive mixed models, taking into account spatial dependence between samples.

marine ecosystems (see Pauly et al. 1998). In contrast, in a sensitive and interpretable measure of the impact of
terrestrial ecosystems, reliable indicators able to depict global change on communities (Devictor et al. 2008). It
changes in functional processes have not yet been pro- assumes that detectability, specialization, and sites do not
posed. The replacement of specialist species by generalist co-vary. Under these conditions, the comparison could be
species could have severe consequences on community performed relative to change over time – based on a time-
and ecosystem functioning. Therefore, we suggest that series study – or relative to variation in space, based on
FH, measured as the proportion of specialist species in the site comparisons (with comparable sites, such as those in
community, is a good indicator because it measures the the same habitat; Panel 1).
state of biodiversity, which is directly linked to drivers of
global changes. We have attempted to separate FH from n Conclusions
TH, in order to construct a robust indicator. Taxonomic
homogenization is not always a synonym of diversity loss The loss of biodiversity across the planet should be con-
(Rooney et al. 2007). Likewise, similarity indices, which sidered not only as a striking inventory of the poor con-
measure BH, are not always informative about changes in servation status of individual species, but also as a general
community and could suggest either an increase or a biological response to global changes with various mech-
decrease in species richness (Olden 2006). To interpret anisms, some of which remain to be identified.
these changes, researchers must identify the species that Replacement of specialist species by generalist species
are responsible for them (Rooney et al. 2007). results in FH. Here, we have identified FH as a general
Comparing specialization among species in communi- process, one that is present in all ecosystems.
ties is a promising way of studying the ecological mecha- Because specialization is a concept anchored in ecolog-
nisms that drive functional diversity (Ackerly and ical theory, we believe it is a powerful tool that can be
Cornwell 2007). Calculating FH requires standardized used to describe and understand the responses of biodi-
multisite, multispecies monitoring efforts, such as citizen- versity to global change. The recent development of such
science programs, which are already being implemented tools, enabling the quantification of niche width, and
in many countries. For example, measurement of FH – studies incorporating the trait concept (Ackerly and
based on how many species are present in a community, Cornwell 2007), open up interesting new possibilities (eg
whose contributions are weighted according to continu- the construction of a robust indicator of biodiversity and
ous measurement of habitat specialization – appears to be ecosystem functions). There is little doubt that fewer spe-

© The Ecological Society of America www.frontiersinecology.org

Specialization theory and application J Clavel et al.

Duncan RP, Blackburn TM, and Sol D. 2003. The ecology of bird
cialists are indicative of ongoing degradation. An impor- introductions. Annu Rev Ecol Syst 34: 71–98.
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