Review
Functional Rarity: The Ecology of Outliers

https://doi.org/10.1016/j.tree.2017.02.002Get rights and content

Trends

A framework for the definition and quantification of functional rarity is missing.

We define functional rarity using both species sparseness and trait distinctiveness.

We introduce 12 different forms of functional rarity.

We discuss the effect of each form of functional rarity on ecosystem function.

The necessary linkage between functional and evolutionary rarity is highlighted.

Rarity has been a central topic for conservation and evolutionary biologists aiming to determine the species characteristics that cause extinction risk. More recently, beyond the rarity of species, the rarity of functions or functional traits, called functional rarity, has gained momentum in helping to understand the impact of biodiversity decline on ecosystem functioning. However, a conceptual framework for defining and quantifying functional rarity is still lacking. We introduce 12 different forms of functional rarity along gradients of species scarcity and trait distinctiveness. We then highlight the potential key role of functional rarity in the long-term and large-scale maintenance of ecosystem processes, as well as the necessary linkage between functional and evolutionary rarity.

Section snippets

The Multiple Facets of Rarity

Rarity has fascinated ecologists and evolutionary biologists [1], and has become the cornerstone of many research fields, and especially of conservation biology 2, 3, 4. Why do species become rare? Why are there so many rare species on Earth? Many studies have examined the biological characteristics of species with a view to explaining the reasons for their rarity (e.g., 5, 6, 7, 8, 9) and the potential consequences of their extirpation 3, 4. Rare species perform different functions in

On the Importance of Functional Rarity

The maintenance of scarce and unique phenotypes in communities is a well-known phenomenon because lower frequency and greater distinctiveness limit both intra- and interspecific competition (negative frequency-dependence) [32]. It has also been described as a ‘strategy' for a species to expand its niche width via a release of intraspecific competition or the exploitation of alternative resources [33]. In addition, both microbial experiments and theoretical studies have emphasized the positive

Functional Rarity: A Conceptual Framework

The definition of functional rarity is the most crucial conceptual point before making significant progress in this new ecology of outliers.

For decades ecological rarity has been estimated at the species level using three main characteristics ultimately related to extinction risk [41]: geographical range, habitat specificity, and local abundance. The combination of these three characteristics defines seven forms of species rarity [21], with the rarest species having small range, a high level of

Measuring Functional Rarity

For over three decades a myriad of metrics have been developed to quantify many facets of biodiversity 57, 58, 59, 60, 61, 62, 63. However, this prolific field has poorly integrated the measurement of functional rarity versus commonness.

To combine the different facets of rarity (Table 1 and Box 1) into a single index, we propose an ‘integrated' view of functional rarity that accounts for both the functional distinctiveness/uniqueness of a species (based on traits, Box 2) and its taxonomic

Functional Rarity and Ecosystem Functioning

Assessing the importance of functional rarity in BEF will require appropriate design to disentangle the effects of species functional distinctiveness and species scarcity. To this end, we propose hypothetical scenarios wherein the influence of biodiversity loss on the shape of BEF relationships (Figure 1) depends on species functional rarity according to the four categories identified at local scale in Figure I. Indeed, if ecosystem functions such as productivity are expected to decrease with

Functional Rarity Across the Tree of Life

An evolutionary perspective on functional rarity can shed light on the processes that are at the origin of functional rarity across the tree of life and allow its maintenance. Although no work has been done so far following our suggested framework, there is a long tradition in evolutionary biology to investigate how ecological specializations evolves (e.g., 71, 72). Pioneering work by Futuyma and Moreno [73] has focused on specialization for resource in terms of diet and feeding behavior.

Concluding Remarks

Our framework for measuring functional rarity paves the way for an ecology of outliers, which allows a deeper understanding of the role of individuals, genotypes, or species bearing distinct trait values within populations, ecosystems, or biomes. A conservation strategy for ecological outliers can also emerge beyond the identification of areas where functional and evolutionary distinctiveness tend to aggregate [79]. For instance, the effectiveness of protected areas for ecological outliers is

Acknowledgments

This research is supported by the French Foundation for Research on Biodiversity (FRB; www.fondationbiodiversite.fr) in the context of the CESAB project ‘Causes and consequences of functional rarity from local to global scales’ (FREE). CV is supported by the European Research Council (ERC) Starting Grant Project ‘Ecophysiological and biophysical constraints on domestication in crop plants’ (Grant ERC-StG-2014-639706-CONSTRAINTS). WT acknowledges support from the European Research Council

Glossary

Ecology of outliers
a research area that studies how and why species (or organisms) are outliers given their local or regional abundances and trait distinctiveness, and the consequences of the persistence of those outliers for the structure and dynamics of communities and ecosystems.
Functional distinctiveness (or trait distinctiveness)
local-scale characteristics of a species (or an organism) having traits dissimilar from those of other species (organisms) in the community. A metric of functional

References (100)

  • W. Kunin et al.

    The Biology of Rarity: Causes and Consequences of Rare-Common Differences

    (1997)
  • M. Soulé

    What do we really know about extinction?

  • B. Murray

    How plant life-history and ecological traits relate to species rarity and commonness at varying spatial scales

    Ecology

    (2002)
  • S. Lavergne

    Do rock endemic and widespread plant species differ under the leaf-height-seed plant ecology strategy scheme?

    Ecol. Lett.

    (2003)
  • K. Gaston et al.

    Rarity and body size: generality is important

    Conserv. Biol.

    (1996)
  • E. Espeland et al.

    The value of structuring rarity: the seven types and links to reproductive ecology

    Biol. Conserv.

    (2011)
  • M. Jain

    The importance of rare species: a trait-based assessment of rare species contributions to functional diversity and possible ecosystem function in tall-grass prairies

    Ecol. Evol.

    (2014)
  • B. Walker

    Plant attribute diversity, resilience and ecosystem function: the nature and significance of dominant and minor species

    Ecosystems

    (1999)
  • M. Bracken et al.

    Realistic losses of rare species disproportionately impact higher trophic levels

    Ecol. Lett.

    (2012)
  • K. Lyons

    Rare species and ecosystem functioning

    Conserv. Biol.

    (2005)
  • J. Chase

    An inordinate foundness of rarity

    PLoS Biol.

    (2013)
  • R.M. Pendleton

    Loss of rare fish species from tropical floodplain food webs affects community structure and ecosystem multifunctionality in a mesocosm experiment

    PLoS One

    (2004)
  • L. Godet

    Dissociating several forms of commonness in birds sheds new light on biotic homogenization

    Global Ecol. Biogeogr.

    (2015)
  • S. Calba

    Measuring and explaining large-scale distribution of functional and phylogenetic diversity in birds: separating ecological drivers from methodological choices

    Global Ecol. Biogeogr.

    (2014)
  • S. Naeem

    The functions of biological diversity in an age of extinction

    Science

    (2012)
  • H.M. Pereira

    Essential biodiversity variables

    Science

    (2013)
  • D. Rabinowitz

    Seven forms of rarity

  • B. Shipley

    From Plant Traits to Vegetation Structure. Chance and Selection in the Assembly of Ecological Communities

    (2010)
  • C. Violle

    The emergence and promise of functional biogeography

    Proc. Natl Acad. Sci. U.S.A.

    (2014)
  • D.C. Laughlin

    Applying trait-based models to achieve functional targets for theory-driven ecological restoration

    Ecol. Lett.

    (2014)
  • M.W. Cadotte

    Predicting communities from functional traits

    Trends Ecol. Evol.

    (2015)
  • D.U. Hooper

    Effects of biodiversity on ecosystem functioning: a consensus of current knowledge

    Ecol. Monogr.

    (2005)
  • S. Diaz

    Functional diversity – at the crossroads between ecosystem functioning and environmental filters

  • M.W. Cadotte

    Beyond species: functional diversity and the maintenance of ecological processes and services

    J. Appl. Ecol.

    (2011)
  • M.E. Power

    Challenges in the quest for keystones

    BioScience

    (1996)
  • F. Isbell

    The biodiversity-dependent ecosystem service debt

    Ecol. Lett.

    (2015)
  • J. Levine et al.

    The importance of niches for the maintenance of species diversity

    Nature

    (2009)
  • J. Roughgarden

    Evolution of niche width

    Am. Nat.

    (1972)
  • M. Loreau

    Biodiversity as spatial insurance in heterogeneous landscapes

    Proc. Natl Acad. Sci. U.S.A.

    (2003)
  • E. Low-Décarie

    Community rescue in experimental metacommunities

    Proc. Natl Acad. Sci. U.S.A.

    (2015)
  • M. Solan

    Extinction and ecosystem function in the marine benthos

    Science

    (2004)
  • J.P. Grime

    Benefits of plant diversity to ecosystems: immediate, filter and founder effects

    J. Ecol.

    (1998)
  • A. Ricciardi et al.

    Extinction rates of North American freshwater fauna

    Conserv. Biol.

    (1999)
  • R.A. Myers et al.

    Rapid worldwide depletion of predatory fish communities

    Nature

    (2003)
  • D. Mouillot

    Rare species support vulnerable functions in high-diversity ecosystems

    PLoS Biol.

    (2013)
  • P.G. Harnik

    Long-term differences in extinction risk among the seven forms of rarity

    Proc. R. Soc. B

    (2002)
  • M. Westoby

    Plant ecological strategies: some leading dimensions of variation between species

    Annu. Rev. Ecol. Evol. Syst.

    (2002)
  • S. Lavorel

    A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services

    J. Veg. Sci.

    (2013)
  • S. Lavorel et al.

    Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail

    Funct. Ecol.

    (2002)
  • C. Violle

    Let the concept of trait be functional!

    Oikos

    (2007)
  • Cited by (228)

    View all citing articles on Scopus
    View full text