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Journal ArticleDOI

Patterns of Biological Invasions in French Freshwater Systems by Non-Indigenous Macroinvertebrates

01 Nov 2005-Hydrobiologia (Kluwer Academic Publishers)-Vol. 551, Iss: 1, pp 137-146
TL;DR: The present work gives a list of the 43 French freshwater non-indigenous species, which represent 1.2% of the French freshwater macroinvertebrates, and provides their geographic origins, their distributions among zoological units by comparison with the native fauna and their functional characteristics according to a recent typology based on bio/ecological traits.
Abstract: Freshwater biodiversity is threatened by several mechanisms, of which the introduction of non-indigenous species and habitat alteration are the two most important. Exotic species act at various levels of organisation of macroinvertebrate communities, and are involved in different processes mediating their impacts on biodiversity, such as habitat modification or negative interactions with autochthonous fauna. The present work gives a list of the 43 French freshwater non-indigenous species, which represent 1.2% of the French freshwater macroinvertebrates. We provide their geographic origins, their distributions among zoological units by comparison with the native fauna and their functional characteristics according to a recent typology based on bio/ecological traits. An exponential trend of the cumulated number of non-indigenous species was evidenced, with a clumping of invaders within crustaceans and molluscs. Donor areas of non-indigenous species are in majority European, and the Ponto-Caspian basin is identified as the principal one. This pattern could be explained by a spread along waterways but its origin lies in a process of recolonisation of defaunated areas following several episodes of glaciation/deglaciation in Western Europe during the last 80,000 years. Finally, from a functional point of view, non-indigenous species exhibit a limited diversity, with two functional groups representing 80% of them.

Summary (2 min read)

Introduction

  • Biodiversity is not a static dimension that could be defined once and for all, but is, on the contrary, permanently changing, influenced by natural and anthropic processes.
  • All these impacts are mediated by numerous processes that act at various levels of organisation, from the individual to the community as a whole (Simon & Townsend, 2003).
  • In many countries, biological invasions are heavily studied, with national databases on non-indigenous species present, their dynamics, distributions and impacts (Leppäkoski et al., 2002).
  • Several rivers (Rhone, Meuse, Rhine) flow across several countries.
  • The present study aims to make an inventory of non-indigenous species observed in French aquatic ecosystems and to analyse their geographic origin, their distribution among freshwater fauna and their functional position according to a typology based on bio/ecological traits (Usseglio-Polatera et al., 2001).

Material and methods

  • Based on a huge bibliographic analysis, the authors documented the non-indigenous species that could be found in French freshwater systems.
  • Data on nonindigenous species are quite difficult to collect based on the bibliography.
  • Moreover, very few articles deal with species introductions in French aquatic ecosystems, and when available, such information is often published in local society of natural history bulletins, which are difficult to obtain.
  • The functional classification recently developed for benthic macroinvertebrates based on both biological and ecological traits (Usseglio-Polatera et al., 2001) was used to assess the main characteristics of non-indigenous species.
  • Groups 1 and 2 shared many characteristics, such as living on organic substrates and being -mesosaprobic.

A major phenomenon

  • As a whole, 43 non-indigenous species have been recorded within French aquatic ecosystems.
  • Since these dates, new species in French freshwater fauna have been identified regularly.
  • The actual trend of invasion, if the authors consider the whole territory, could be described by a highly significant exponential function (Fig. 1), suggesting an acceleration of the phenomenon in the last few decades.
  • Among the three European donor areas identified, the authors notice that the Ponto-Caspian basin distinguishes itself (32.5% of whole non-indigenous species, 58% of those with a European origin), and confirms its status as a hot-spot donor area of non-indigenous species.
  • As signalled in the introduction, few data are available for each basin.

A strong dissymmetry between taxa

  • Those non-indigenous species could be found among almost all taxonomic groups.
  • Some of them are more implicated in biological invasions than others (Table 2).
  • Considering the species number, two groups distinguish themselves: molluscs and crustaceans, that represent respectively 26% and 49% of all nonindigenous species found in French hydrosystems.
  • The authors also notice that non-indigenous species are represented among all zoological units, except Porifera, a weakly diversified group.
  • Finally, for 36 species only the functional group is known.

Discussion

  • All freshwater fauna of France could be considered as non-indigenous, going back in time enough, to the last glaciations.
  • Thus, the dominant pattern of invasion could be assimilated to a colonisation process of defaunate areas as an inheritance of the last glaciation, with Eastern Europe being a provider of non-indigenous species and Western Europe as a recipient area.
  • The 43 non-indigenous species identified represent more than one percent of the total macroinvertebrate French freshwater fauna.
  • For intracontinental transfers, besides these two vectors, recreational shipping and natural migration along newly opened waterways could also occur.
  • Thus, it seems that a high majority of non-indigenous species exhibit similar functional characteristics and that, more than a taxonomical clumping, a functional clumping of non-indigenous species take place, which evidenced that particular bio/ecological profiles could enhance invasiveness.

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Patterns of biological invasions in French freshwater
systems by non-indigenous macroinvertebrates
Simon Devin, Loïc Bollache, Pierre-Yves Noël, Jean-Nicolas Beisel
To cite this version:
Simon Devin, Loïc Bollache, Pierre-Yves Noël, Jean-Nicolas Beisel. Patterns of biological invasions in
French freshwater systems by non-indigenous macroinvertebrates. Hydrobiologia, Springer, 2005, 551
(1), pp.137 - 146. �10.1007/s10750-005-4456-z�. �hal-01726819�

1
Patterns of biological invasions in French freshwater
systems by non-indigenous macroinvertebrates
Simon DEVIN
1*
, Loïc BOLLACHE
2
, Pierre-Yves NOËL
3
and Jean-Nicolas
BEISEL
1
1
Université de Metz UFR SciFA - Laboratoire Biodiversité et Fonctionnement des
écosystèmes - Campus Bridoux, Av. du Gén. Delestraint, 57070 Metz, France
2
Equipe Ecologie Evolutive, UMR CNRS 5561 Biogéosciences, Université de Bourgogne,
6 boulevard Gabriel, 21000 Dijon, France
3
Muséum National d'Histoire Naturelle, Département Milieux et Peuplements
Aquatiques, UMR CNRS-UPMC-MNHN BOME 5178, 55 rue Buffon, 75005 PARIS,
France
Key words: biological invasions, exotic species, freshwater macroinvertebrates, French
aquatic ecosystems
Abstract
Freshwater biodiversity is threatened by several mechanisms, of which the introduction of
non-indigenous species and habitat alteration are the two most important. Exotic species act at
various levels of organisation of macroinvertebrate communities, and are involved in different
processes mediating their impacts on biodiversity, such as habitat modification or negative
interactions with autochthonous fauna. The present work gives a list of the 43 French
freshwater non-indigenous species, which represent 1.2% of the French freshwater
acroinvertebrates. We provide their geographic origins, their distributions among zoological
units by comparison with the native fauna and their functional characteristics according to a
recent typology based on bio/ecological traits. An exponential trend of the cumulated number
of non-indigenous species was evidenced, with a clumping of invaders within crustaceans and
molluscs. Donor areas of non-indigenous species are in majority European, and the Ponto-
Caspian basin is identified as the principal one. This pattern could be explained by a spread
along waterways but its origin lies in a process of recolonisation of defaunated areas
following several episodes of glaciation / deglaciation in Western Europe during the last
80,000 years. Finally, from a functional point of view, non-indigenous species exhibit a
limited diversity, with two functional groups representing 80% of them.
Introduction
Biodiversity is not a static dimension that could be defined once and for all, but is, on
the contrary, permanently changing, influenced by natural and anthropic processes. Among
this last category, biological invasions are now considered to be a major driver of change of
freshwater biodiversity (Sala et al., 2000).
Invasions consist of the transfer, establishment and spread of a species within an ecosystem
where it is not naturally present, also called the recipient ecosystem (Vermeij, 1996;
Williamson, 1996; Kolar & Lodge, 2001). In a strict sense, the introduction of non-indigenous
species occurs naturally, and is not exclusively a human-driven phenomenon (Mack et al.,
2000). However, a growing interest is accorded to the human-mediated invasions, since
increasing rates of species establishment have been observed these last decades in many

2
aquatic ecosystems (The Great Lakes, Ricciardi, 2001; San-Francisco Bay, Cohen & Carlton,
1998) as a consequence of the removal of natural geographic barriers and the expanding
transport by waterways. The disappearance of autochthonous species in human-altered
freshwater ecosystems, the poverty of the fauna remaining and their inability to adapt to new
local conditions (Sax and Brown 2000) have favored the permeability of to repeated
introductions of exotic species (decrease in biotic resistance as defined by Elton 1958). Many
impacts of invaders have been referenced, and among them the threat for biodiversity they
represent (Sala et al., 2000; Mooney & Cleland, 2001; Rahel, 2002). Effectively, invasive
species can have major ecological consequences on faunal composition, community structure
and ecosystem functioning (Mack et al., 2000). All these impacts are mediated by numerous
processes that act at various levels of organisation, from the individual to the community as a
whole (Simon & Townsend, 2003).
In many countries, biological invasions are heavily studied, with national databases on
non-indigenous species present, their dynamics, distributions and impacts (Leppäkoski et al.,
2002). When performed for freshwaters at a large scale (bij de Vaate et al., 2002; Leppäkoski
et al., 2002), such studies do not take into account French territory. However, thanks to the
high diversity of French ecoregions, non-indigenous species already referenced in southern,
eastern and northern Europe could potentially be found there. Moreover, with regards to its
geographic position and its high connectivity with main European waterways and other
continents due to the presence of many harbours (Bordeaux, Le Havre, Marseille-Fos, Nantes-
Saint-Nazaire, Rouen), France could constitute an important platform of fauna exchange. The
territory includes six main basins, corresponding to the largest rivers: Garonne, Loire, Seine,
Rhone, Meuse and the upper Rhine. Several streams along the Atlantic coast directly flow to
the ocean and are not connected to one of the main rivers. Several rivers (Rhone, Meuse,
Rhine) flow across several countries.
The present study aims to make an inventory of non-indigenous species observed in
French aquatic ecosystems and to analyse their geographic origin, their distribution among
freshwater fauna and their functional position according to a typology based on bio/ecological
traits (Usseglio-Polatera et al., 2001). These results are discussed in terms of non-indigenous
species origins and potential consequences of introductions.
Material and methods
Based on a huge bibliographic analysis, we documented the non-indigenous species
that could be found in French freshwater systems. Only free-living macroinvertebrates were
considered in this study, i.e. parasites and invertebrates below 3-5 mm in their adult size
(microinverbertebrates as defined by Tachet et al., 2000) were excluded. Data on non-
indigenous species are quite difficult to collect based on the bibliography. French national
agencies perform bioassessment using a global method that requires identification to the
family level only, thus are unable to provide such data. Moreover, very few articles deal with
species introductions in French aquatic ecosystems, and when available, such information is
often published in local society of natural history bulletins, which are difficult to obtain.
Thus we kept only data signalling a new species if at least one scientific article is
available (i.e. referenced in an international review or in a national review included in
PASCAL database). For each species, we defined the date of the first observation, its origin
and its major ecological and biological characteristics. Species distribution among the major
French basins is estimated with bibliography, but it does not always reflect the true
distribution. Consequently, it will not be possible to describe the dynamics of colonisation
and dispersal of non-indigenous species within French aquatic ecosystems. For most of the
species, vector of introduction is not known, even if numerous studies have already detailed

3
the major role of shipping traffic, and particularly ballast water transport, in the spread of
aquatic exotic species throughout the world (see Gollash et al., 2002 for a review).
The functional classification recently developed for benthic macroinvertebrates based
on both biological and ecological traits (Usseglio-Polatera et al., 2001) was used to assess the
main characteristics of non-indigenous species. This classification has lead to the definition of
6 functional groups, 9 subgroups and 43 units according to a biological versus ecological
ordination. For species not referenced before, P. Usseglio-Polatera performed a new analysis
that allowed us to integrate and classify them. The present study is based on the subgroup
level and French non-indigenous species belong to 6 of them (called 1, 2, 1, 2 and by
Usseglio-Polatera et al., 2001). Most species of the group exhibits small to medium sizes,
an omnivorous regime and a scraper or shredder feeding behaviour. They live in coarse
mineral substrates and are oligo to -mesosaprobic. Groups 1 and 2 shared many
characteristics, such as living on organic substrates and being -mesosaprobic. They tend to
be predator, feeding on macroinvertebrates, and exhibit small to medium sizes. Species of the
groups 1 and 2 live on mineral or organic substrates and are -mesosaprobic. The feeding
habits of these medium-sized taxa are similar to that of group . Finally, group is
constituted of filter- or deposit-feeders that fed on microphytes and fines detritus, with
variable body sizes and microhabitat preferences. All taxa of these 6 functional groups are
eurythermous.
Finally, the proportion of non-indigenous species among the different zoological units
that could be found in French rivers was analysed in order to assess whether some taxa have
greater roles in biological invasions than others. Nematomorpha were excluded, because we
did not get enough data to reliably estimate the proportion of non-indigenous species within
this group. All species occurring in surface freshwaters were taken into account for this
analysis.
Results
A major phenomenon
As a whole, 43 non-indigenous species have been recorded within French aquatic
ecosystems. It is difficult to identify the first species that invaded these hydrosystems, because
the knowledge and the study of freshwater macroinvertebrates is not an old discipline.
However, the history of species establishment can be made for the last 175 years, beginning
with the description of Atyaephyra desmaresti in the Loire basin in 1832 (Dhur & Massard,
1995), and Gammarus roeseli in the vicinity of Paris in 1835 (Jazdzewski, 1980) (Table 1).
Since these dates, new species in French freshwater fauna have been identified regularly. The
actual trend of invasion, if we consider the whole territory, could be described by a highly
significant exponential function (Fig. 1), suggesting an acceleration of the phenomenon in the
last few decades.
Geographic origin of non-indigenous species and distribution
Species introductions are strongly dominated by intra-continental transfers (25 of 43
species are of European origin, Table 1). Among the three European donor areas identified,
we notice that the Ponto-Caspian basin distinguishes itself (32.5% of whole non-indigenous
species, 58% of those with a European origin), and confirms its status as a hot-spot donor area
of non-indigenous species. The two others main donor areas are North America and South-
Eastern Asia. It is noteworthy that, excepting Potamopyrgus antipodarum, all non-indigenous
species came from the northern hemisphere.
The description of the present distribution of non-indigenous species in France
represents a hard task. As signalled in the introduction, few data are available for each basin.

4
The Rhine basin is better studied than the others, and exotic species arrivals are particularly
well documented there, due both to its position among Western Europe waterways and
numerous programs of rehabilitation. The Rhone basin is second in terms of available data
concerning macroinvertebrates communities. It is harder to get detailed information for basins
such as that of the Loire and Garonne rivers.
A strong dissymmetry between taxa
To date, 1.2 % of French freshwater macroinvertebrates is of exotic origin considering
species introduced in the past 200 years. Those non-indigenous species could be found among
almost all taxonomic groups. However, some of them are more implicated in biological
invasions than others (Table 2). Considering the species number, two groups distinguish
themselves: molluscs and crustaceans, that represent respectively 26% and 49% of all non-
indigenous species found in French hydrosystems.
We also notice that non-indigenous species are represented among all zoological units,
except Porifera, a weakly diversified group. The most diverse group of freshwater
invertebrates, the insects, is the one were the proportion of exotics is the lowest. Conversely,
freshwater Polychaeta are only represented by the non-indigenous taxon Hypania invalida.
Molluscs and Crustaceans excepted, it seems that no taxonomical clumping of non-indigenous
species occurred.
Finally, for 36 species only the functional group is known. The large majority of non-
indigenous species belong to two bio/ecological groups: 2 and (respectively 9 and 19
species in each group). Four other functional groups are represented, but by a lower number
of species (2 species in each group), and, except for group , by species that do not have
spectacular population explosions within French freshwater systems (see Table 1 for species
and references).
Discussion
All freshwater fauna of France could be considered as non-indigenous, going back in
time enough, to the last glaciations. During the Würm glaciation (80,000-10,000 BP), the
major part of Western Europe was covered with ice. Thus, at the end of this period, defaunate
freshwater ecosystems appeared, colonised or recolonised by species having survived in
refuge areas that were outside ice range extension (according to Oberdorff et al., 1997). We
can not define whether a recolonisation or a colonisation process occurred (i.e. did the species
were the same before and after the glaciations or not?), because the fauna present before the
Würm glaciation is poorly known (few invertebrate fossil records). The two main refuge
areas in Europe are Mediterranean Europe and the Danube basin (Persat & Keith, 1997). The
process of colonisation, which is well documented for fish, probably also took place for
macroinvertebrates.
Thus, the dominant pattern of invasion could be assimilated to a colonisation process
of defaunate areas as an inheritance of the last glaciation, with Eastern Europe being a
provider of non-indigenous species and Western Europe as a recipient area. This process
could be illustrated with the establishment of many Ponto-Caspian amphipod species in
France. Based on the data provided by the Limnofauna Europea (Illies, 1978), 23
autochthonous species could be found in France, 7 of them inhabiting essentially brackish
waters and 10 being restricted to small geographic areas in southern France. Thus, amphipod
assemblages are essentially constituted of 6 species versus 63 in the Ponto-Caspian basin: this
dissymmetry could be explained by an original pattern of amphipod invasions along a
longitudinal European gradient from East to West. Another consequence of this geological

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  • ...…species beyond their natural ranges (reviewed in Kolar and Lodge 2001) and caused rising economic and ecological costs, which revived interest in the topic in freshwater research (e.g., Ricciardi and Rasmussen 1998, Clarke et al. 2004, Devin et al. 2005, Leprieur et al. 2008, Statzner et al. 2008)....

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  • ...Devin et al. (2005) considered the diversity (Shannon) of functional groups as a measure of functional diversity and recorded changes in the values of a functional diversity index in response to changing abundances of several exotic species....

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Journal ArticleDOI
TL;DR: Given their current scale, biotic invasions have taken their place alongside human-driven atmospheric and oceanic alterations as major agents of global change and left unchecked, they will influence these other forces in profound but still unpredictable ways.
Abstract: Biotic invaders are species that establish a new range in which they proliferate, spread, and persist to the detriment of the environment. They are the most important ecological outcomes from the unprecedented alterations in the distribution of the earth's biota brought about largely through human transport and commerce. In a world without borders, few if any areas remain sheltered from these im- migrations. The fate of immigrants is decidedly mixed. Few survive the hazards of chronic and stochastic forces, and only a small fraction become naturalized. In turn, some naturalized species do become invasive. There are several potential reasons why some immigrant species prosper: some escape from the constraints of their native predators or parasites; others are aided by human-caused disturbance that disrupts native communities. Ironically, many biotic invasions are apparently facilitated by cultivation and husbandry, unintentional actions that foster immigrant populations until they are self-perpetuating and uncontrollable. Whatever the cause, biotic invaders can in many cases inflict enormous environmental damage: (1) Animal invaders can cause extinctions of vulnerable native species through predation, grazing, competition, and habitat alteration. (2) Plant invaders can completely alter the fire regime, nutrient cycling, hydrology, and energy budgets in a native ecosystem and can greatly diminish the abundance or survival of native species. (3) In agriculture, the principal pests of temperate crops are nonindigenous, and the combined expenses of pest control and crop losses constitute an onerous "tax" on food, fiber, and forage production. (4) The global cost of virulent plant and animal diseases caused by parasites transported to new ranges and presented with susceptible new hosts is currently incalculable. Identifying future invaders and taking effective steps to prevent their dispersal and establishment con- stitutes an enormous challenge to both conservation and international commerce. Detection and management when exclusion fails have proved daunting for varied reasons: (1) Efforts to identify general attributes of future invaders have often been inconclusive. (2) Predicting susceptible locales for future invasions seems even more problematic, given the enormous differences in the rates of arrival among potential invaders. (3) Eradication of an established invader is rare, and control efforts vary enormously in their efficacy. Successful control, however, depends more on commitment and continuing diligence than on the efficacy of specific tools themselves. (4) Control of biotic invasions is most effective when it employs a long-term, ecosystem- wide strategy rather than a tactical approach focused on battling individual invaders. (5) Prevention of invasions is much less costly than post-entry control. Revamping national and international quarantine laws by adopting a "guilty until proven innocent" approach would be a productive first step. Failure to address the issue of biotic invasions could effectively result in severe global consequences, including wholesale loss of agricultural, forestry, and fishery resources in some regions, disruption of the ecological processes that supply natural services on which human enterprise depends, and the creation of homogeneous, impoverished ecosystems composed of cosmopolitan species. Given their current scale, biotic invasions have taken their place alongside human-driven atmospheric and oceanic alterations as major agents of global change. Left unchecked, they will influence these other forces in profound but still unpredictable ways.

6,195 citations

Journal ArticleDOI
TL;DR: Although restricted to few taxa, these studies reveal clear relationships between the characteristics of releases and the species involved, and the successful establishment and spread of invaders.
Abstract: Predicting which species are probable invaders has been a long-standing goal of ecologists, but only recently have quantitative methods been used to achieve such a goal. Although restricted to few taxa, these studies reveal clear relationships between the characteristics of releases and the species involved, and the successful establishment and spread of invaders. For example, the probability of bird establishment increases with the number of individuals released and the number of release events. Also, the probability of plant invasiveness increases if the species has a history of invasion and reproduces vegetatively. These promising quantitative approaches should be more widely applied to allow us to predict patterns of invading species more successfully.

2,698 citations


"Patterns of Biological Invasions in..." refers background in this paper

  • ...Invasions consist of the transfer, establishment and spread of a species within an ecosystem where it is not naturally present, also called the recipient ecosystem (Vermeij, 1996; Williamson, 1996; Kolar & Lodge, 2001)....

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Book
06 Jan 2012
TL;DR: The first book on invasion biology, and still the most cited, Elton's masterpiece provides an accessible, engaging introduction to one of the most important environmental crises of the authors' time.
Abstract: Much as Rachel Carson's "Silent Spring" was a call to action against the pesticides that were devastating bird populations, Charles S. Elton's classic "The Ecology of Invasions by Animals and Plants" sounded an early warning about an environmental catastrophe that has become all too familiar today-the invasion of nonnative species. From kudzu to zebra mussels to Asian long-horned beetles, nonnative species are colonizing new habitats around the world at an alarming rate thanks to accidental and intentional human intervention. One of the leading causes of extinctions of native animals and plants, invasive species also wreak severe economic havoc, causing $79 billion worth of damage in the United States alone. Elton explains the devastating effects that invasive species can have on local ecosystems in clear, concise language and with numerous examples. The first book on invasion biology, and still the most cited, Elton's masterpiece provides an accessible, engaging introduction to one of the most important environmental crises of our time. Charles S. Elton was one of the founders of ecology, who also established and led Oxford University's Bureau of Animal Population. His work has influenced generations of ecologists and zoologists, and his publications remain central to the literature in modern biology. "History has caught up with Charles Elton's foresight, and "The Ecology of Invasions" can now be seen as one of the central scientific books of our century."-David Quammen, from the Foreword to "Killer Algae: The True Tale of a Biological Invasion"

2,530 citations

Frequently Asked Questions (1)
Q1. What contributions have the authors mentioned in the paper "Patterns of biological invasions in french freshwater systems by non-indigenous macroinvertebrates" ?

The authors provide their geographic origins, their distributions among zoological units by comparison with the native fauna and their functional characteristics according to a recent typology based on bio/ecological traits. This pattern could be explained by a spread along waterways but its origin lies in a process of recolonisation of defaunated areas following several episodes of glaciation / deglaciation in Western Europe during the last 80,000 years.