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Hydrobiologia

, Volume 810, Issue 1, pp 45–56 | Cite as

Can introduced species replace lost biodiversity? A test with freshwater molluscs

  • Alexander Y. KaratayevEmail author
  • Lyubov E. Burlakova
  • Dianna K. Padilla
FRESHWATER BIVALVES

Abstract

Human activity has dramatically accelerated both species extinctions and introductions, and the balance of these two processes is generally expected to reduce biodiversity and increase taxonomic homogenization. However, few tests of this hypothesis have been made. We tested whether new macroinvertebrate invaders in North American freshwaters can replace the recent loss of biodiversity, particularly focusing on molluscs. We found that both crustaceans and molluscs are overrepresented among endangered and recently extinct species, as well as among invaders. For molluscs, the number of recently extinct species (79 species) was more than twice that for exotic species (38 species). In addition, molluscan invaders are from different taxonomic families than recently extinct or endangered species. While most extinct and endangered molluscs are from streams and rivers, invaders preferentially colonize lakes and reservoirs. The impact of humans on species introductions and extinctions increases with spatial scale (from local to continental scales), resulting in the increased phylogenetic dissimilarity between introduced species and native communities. Construction of dams and alteration of the flow regimes of lotic systems will continue to lead to the extinction of native species, and promote the spread of invaders, resulting in a loss of biodiversity and taxonomic homogenization.

Keywords

Endangered species Extinct species Invaders Freshwater invertebrates Molluscs 

Introduction

The diversity and species composition observed in biological communities is the culmination of assembly processes (Chase & Leibold, 2003; Cottenie, 2005; Vellend, 2010). Since the work of MacArthur & Wilson (1967) on Island Biogeography, observed community diversity has been recognized as the dynamic result of two continuous ecological processes: immigration (rate of dispersal of new species into the system) and the extinction or extirpation of species already established in the system. Both immigration and extinction are still recognized as important for community structure and composition (Chase & Leibold, 2003; Cottenie, 2005; Vellend, 2010), but the rates of both extinction (or extirpation) and introductions (immigration) are changing as humans have greater impacts on ecosystems and biodiversity (Sax & Gaines, 2003; Butchart et al., 2010; Clavero & Hermoso, 2011; Villéger et al., 2011). The consequences of such species additions and loss can lead to homogenization of communities, and may be scale dependent (Sax et al., 2002; Sax & Gaines, 2003; Villéger et al., 2011; Fig. 1). At the largest scale, species diversity is primarily a function of extinction and speciation, while at local scales diversity is affected by immigration of native species (Wilson, 1992; Sax & Gaines, 2003; Leibold et al., 2004). Human alterations to ecosystems, as well as direct harvesting, has resulted in the extirpation of local native species, and estimated extinctions are at rates higher than at any other time in history (McKinney & Lockwood, 1999; Rahel, 2000; Olden et al., 2004, 2006; Clavero & Hermoso, 2011; Villéger et al., 2011). The global impacts of biodiversity loss are especially evident in freshwater ecosystems, which are considered one of the most endangered ecosystems on Earth due to steeply rising human impacts over the past century (Dudgeon et al., 2006; Strayer, 2006; Strayer & Dudgeon, 2010). At the same time ecosystems, including freshwaters, suffer from the introductions of invaders, which pose major threats to biodiversity (Wilcove et al., 1998; Gurevitch & Padilla, 2004; Dudgeon et al., 2006). Efforts to protect endangered and threatened species as well as activities to control, eradicate, or remove nuisance introductions cost billions of dollars each year (Pimentel et al., 2005; Keller et al., 2007). However, some recent work has suggested that, while at a global scale the loss of biodiversity is evident, at regional and local scales species diversity might be increasing as exotic introductions have outpaced the loss of native species (Hobbs & Mooney, 1998; Sax et al., 2002; Sax & Gaines, 2003; Dornelas et al., 2014; Fig. 1).
Fig. 1

Conceptual model of introduction/extinction processes at different spatial scales. The relative importance of natural processes on biodiversity increases at local scales, while the impact of humans on biodiversity increases with larger scales. The phylogenetic distance between species moving into communities relative to the native diversity will increase as introductions happen across ever greater spatial scales, and the impacts of such introductions likely decrease when species are moved at small rather than large spatial scales

Freshwater habitats are particularly affected by human impacts, especially the macroinvertebrate fauna of these systems. Freshwater molluscs are among the most endangered animals in North America (Bogan, 1993; Lydeard et al., 2004), with over 76% of freshwater bivalves in the families Unionidae and Margaritiferidae and 74% of freshwater gastropods imperiled (vulnerable, threatened, endangered), or recently driven to extinction within the past 150 years. This greatly exceeds imperilment levels for both fishes (39%) and arthropods (crayfishes, 48%) (Williams et al., 1993; Johnson et al., 2013). Although freshwater invaders can be found among most major taxa, freshwater macroinvertebrate invaders are not a random selection of species. Native communities are dominated by insects (hexapods), while invaders are over represented by molluscs and crustaceans (Karatayev et al., 2009a).

We tested whether the freshwater macroinvertebrate groups in North America that are at risk (extinct, endangered, and imperiled) are taxonomically similar to those that are invaders, or whether they represent taxonomically distinct groups. We then asked whether invaders and species at risk, including species that have recently gone extinct (within the past 150 years), have similar habitat preferences. Finally, we determined whether species introductions in North America have compensated for the number of species lost in freshwaters, particularly for molluscs.

Methods

Species compilation

We determined the number of described native and introduced macroinvertebrate freshwater species in North America in each phylum based on published records and databases. There are undoubtedly species in all taxa that have not yet been described; however, we used the best data presently available for all taxa. For the Mollusca, we determined the number of native and introduced species in each family in the classes Bivalvia and Gastropoda. We also determined the number of species at risk (recently extinct, endangered, threatened, or imperiled) in each phylum and, for molluscs, the numbers in each family of Bivalvia and Gastropoda. We used Thorp and Covich (2010) as the source for all species of North American macroinvertebrates, including bivalves, and Johnson et al. (2013) for gastropods. Wetzel et al. (2015) was used for both native and exotic species of oligochaetes (Tables 1, 2). To determine those species that are invaders, we used searches of web-based databases including invasive species databases (primarily USGS Nonindigenous Aquatic Species Database) and for species at risk (considered endangered, threatened, or imperiled) databases that record extinct, threatened, and endangered species (primarily U.S. Fish and Wildlife Service (USFWS) Environmental Conservation Online System; NatureServe, 2015; The International Union for Conservation of Nature (IUCN)’ Red List of Threatened Species). We also searched the primary literature identified through the Web-of-Science (1945–2014), Zoological Record (1974–2014), and books and reports and avoided reports and publications based on “opinion” rather than data.
Table 1

The total number of freshwater native species of macroinvertebrates, as well as those considered introduced and threatened or endangered species in North America

Taxon

All species in North America

Introduced (exotic and native transplant)

Threatened or endangered (USFWS)

Exotic

Native transplant

All introduced

Porifera

32

0

0

0

0

Cnidaria

99

3

0

3

0

Turbellaria

200

1

0

1

0

Gastrotricha

100

0

0

0

0

Rotifera

610

0

0

0

0

Nematoda

400

0

0

0

0

Mollusca

     

 Gastropoda

732a

29

11

40

31

 Bivalvia

341b

9

12

21

82

 Annelida

384

11

0

11

0

 Bryozoa

24

2

2

4

0

Arthropoda

     

 Hydrachnidae

1,500

0

0

0

0

 Hexapoda (Insecta)

10,000

2

0

2

10

 Other Crustacea

1,500

50

51

101

25

Total

15,922

107

76

183

148

For most groups, species are pooled by phylum. For the Mollusca, species are separated into the classes Bivalvia and Gastropoda. For the Arthropods we have data for Hydrachnidae, Hexapoda (Insecta), and other Crustacea

a703 native (Johnson et al., 2013) and 29 exotic species

b332 native (Thorp and Covich, 2010) and 9 exotic species

Table 2

The total number of molluscan native species, as well as those considered imperiled (Thorp & Covich, 2010; Johnson et al., 2013), extinct, and officially listed as threatened or endangered by the USFWS in North America, as well as introduced exotic and native transplant species for families of both gastropods and bivalves

Family

Native species

Introduced (modified from USGS)

Total number

Imperiled

Extinct by USFWS

Listed by USFWS

Exotic

Native transplant

Total

Total Mollusca

1,035

728

79

113

38

23

61

Total Gastropoda

703

515

47

31

29

11

40

Ampullariidae

1

0

0

0

10

1

11

Amnicolidae

18

11

0

0

0

0

0

Assimineidae

2

2

0

1

0

0

0

Bithyniidae

0

0

0

0

1

0

1

Cochliopidae

48

44

0

6

0

0

0

Hydrobiidae

185

170

2

9

1

1

2

Lithoglyphidae

73

47

6

2

0

0

0

Pleuroceridae

162

128

32

7

0

3

3

Pomatiopsidae

6

4

0

0

0

0

0

Semisulcospiridae

11

10

0

0

0

0

0

Viviparidae

21

5

0

3

3

2

5

Neritidae

5

3

0

0

0

0

0

Acroloxidae

1

1

0

0

0

0

0

Lymnaeidae

61

37

0

2

2

1

3

Physidae

47

26

1

1

3

1

4

Planorbidae

52

23

6

1

4

2

6

Valvatidae

10

5

0

0

1

0

1

Thiaridae

0

0

0

0

4

0

4

Total Bivalvia

332

213

32

82

9

12

21

Unionidae

292

210

32a

80b

1

10

11

Margaritiferidae

5

3

0

2

0

0

0

Sphaeriidae

35

0

0

0

5

2

7

Dreissenidae

0

0

0

0

2

0

2

Corbiculidae

0

0

0

0

1

0

1

Taxonomy and data on endangered and extinct species gastropods from Johnson et al. (2013). Data on Unionidae and Margaritiferidae from Thorp & Covich (2010)

aUSFWS considers 32 species extinct, while Thorp & Covich (2010) consider 31 species and 3 subspecies extinct

bUSFWS considers 80 species and 6 subspecies of unionids threatened or endangered

For many freshwater macroinvertebrates, there are insufficient data available to have them formally classified by the IUCN or USFWS as endangered or threatened. As a result, experts have classified many of such species as imperiled (bivalve molluscs—Thorp & Covich, 2010, gastropods—Johnson et al., 2013). We used all available data to classify species at risk as (1) imperiled, (2) extinct, or (3) officially listed by USFWS as endangered or threatened.

We classified invaders based on their geographic region of origin, as exotic species (from a different continent or major biogeographic region) or as native transplant species (introduced by humans from another region on the same continent). We classified each species by phylum, and for molluscs, by family. We did not include mosquitoes because they are generally not considered among aquatic invaders (i.e., they are not included in any aquatic invader databases) and are not always considered in native fauna databases for freshwater.

For molluscan species at risk and molluscan invaders, we also identified the habitat types used by each species. A total of 9 habitat types were used in this study, including lakes and reservoirs, large rivers, medium rivers, small rivers (creeks), wetlands, estuaries, springs, subterranean, and hot springs.

Statistical analyses

A Fisher–Freeman–Halton test (a generalization of the Fishers Exact Test with a Monte Carlo estimate of the P value to test for homogeneity in contingency tables; StatXact-4, version 4.0.1, Cytel Software Corp.) was used to test whether molluscs were over represented among freshwater taxa in terms of the numbers of species at risk (endangered, threatened, or imperiled), as well as among invaders (both exotic invaders and native transplant invaders). Within molluscs, we tested for similar patterns among families for both bivalves and gastropods. We tested whether the number of habitats (habitat breadth) used by invaders and species at risk differed within families of bivalves and gastropods with a Mann–Whitney U test (with continuity correction; STATISTICA, version 12, StatSoft, Inc. 2014), and then used the Fisher–Freeman–Halton test to assess whether bivalves and gastropods were disproportionally represented among habitats. A critical alpha of 0.05 was used to consider statistical significance. When multiple tests were conducted on the same data, we used a sequential Bonferroni correction to adjust the critical alpha considered for statistical significance (Rice, 1989).

Results

Taxon diversity

In North America, there are a total of 15,922 described native species of freshwater macroinvertebrates and 183 total introduced species (Table 1). The distribution of taxa of introduced species (considering phyla and classes) differed significantly from that for native fauna (P < 0.001, Fisher–Freeman–Halton test). Certain taxa have more introduced species than expected by random. Among the introduced species, 107 species were exotic introductions (from other continents) and 76 species were native transplant species (introduced from outside of their range within the continent). The taxonomic distribution of these two groups was significantly different (P < 0.001).

Across all taxa, 148 species of macroinvertebrates were listed by the USFWS as threatened or endangered (Table 1). The distribution of threatened or endangered species differed significantly from that for native fauna (P < 0.001). Among freshwater macroinvertebrates, hexapods (primarily insects) are by far the most diverse taxon, composing 63% of all of the species diversity in North America (Table 1). However, in North America there are only 2 known exotic species of freshwater insects (the beetle Tanysphyrus lemnae and the moth Acentropus niveus) and 10 species that are considered endangered or threatened. Among introduced species, the most diverse groups were non-hexapod crustaceans (50 exotic species and 51 species of native transplants, 55.2% combined of all introductions in North America) and molluscs (38 exotic species and 23 species of native transplants, 33.4% combined of all introduced species).

Molluscs were the dominant taxon of threatened and endangered species (113 species, 76.4% of all threatened and endangered species), followed by non-hexapod crustaceans (25 species, 16.9% of all listed species) (Table 1). Over seventy percent (728 species) of the 1,035 native species of molluscs were considered imperiled, 8% (79 species) were recently extinct, and 11% (113 species) were listed as endangered and threatened (Table 2). The total number of recently extinct molluscs was more than twice the total number of exotic molluscs found in North America (79 vs. 38 species).

The relative frequency of gastropod species at risk (imperiled, extinct, and threatened) differed significantly among families from that of exotic species (all P < 0.001) and native transplant species (all P < 0.001). In addition, the frequency of exotic species vs. native transplant species differed among families (P < 0.001). Among gastropod families, Hydrobiidae and Pleuroceridae had the largest number of imperiled and endangered and threatened species, and 72% of recently extinct gastropod species. In contrast, the Ampullariidae had the highest diversity of introduced species (10 species, 35% of all exotic gastropods), but only one native species in North America. Although almost 50% of all native North American freshwater gastropods belong to the Hydrobiidae and Pleuroceridae, only one exotic and 4 native transplant species were in these families.

As for the gastropods, the distribution of bivalves at risk (imperiled, recently extinct, and listed) differed significantly from that for exotic species among families (all P < 0.001, Table 2). Again, the distribution of exotic bivalve species by family was different from that of native transplants (P < 0.001). All bivalve species at risk or recently extinct belong to two families, Unionidae and Margaritiferidae. In contrast, all but one species of exotic bivalve (Sinanodonta woodiana, Unionidae) were in three families, Sphaeriidae, Dreissenidae, and Corbiculidae, none of which has any species at risk in North America. There are no native North American species in the families Dreissenidae and Corbiculidae.

Habitat use

Recently extinct and endangered freshwater molluscs use different habitats in terms of waterbody types than either native transplant or exotic species (Figs. 2, 3). On average, recently extinct gastropods occurred in fewer habitat types (1.20 ± 0.07, SE here and elsewhere) than currently endangered gastropod species (1.88 ± 0.13, P < 0.001). In addition, recently extinct gastropods used significantly different types of habitats than endangered gastropods (P < 0.001); medium-sized rivers were the major habitat for over 91% (42 of 47 total species) of recently extinct gastropods with known habitat types. Endangered and threatened gastropods were largely found in running waters, and the greatest number of species lives in small rivers, creeks, and springs rather than medium-sized rivers (Fig. 3). Recently extinct gastropods used significantly different habitat types than either native transplant (P < 0.001) or exotic species (P < 0.001). A similar pattern was found for endangered and threatened species vs. native transplants (P < 0.001) and exotic species (P < 0.001). Exotic species of gastropods use significantly more habitat types (5.22 ± 0.22) than do native transplant species (4.13 ± 0.35, P = 0.017), but there was no difference in their overall use of different habitat types (P = 0.089). Both native transplant and exotic gastropods were much more common in lentic environments. Of the 29 exotic and native transplant species of gastropods with sufficient data on habitat use, 23 (79%) are found in lakes and reservoirs, while only two species of recently extinct and one endangered species of gastropod are found in these habitats.
Fig. 2

Average number of waterbody types (±SE) used by gastropod and bivalve mollusc species in North America. Habitat types considered included: lakes and reservoirs, large rivers, medium rivers, small rivers (creeks), wetlands, estuaries, springs, subterranean, and hot springs

Fig. 3

Percentage of gastropod and bivalve mollusc species that inhabit different types of waterbodies

Unlike gastropods, recently extinct bivalves and endangered bivalves have similar habitat breadth (2.09 ± 0.15 vs. 2.24 ± 0.07, P = 0.44, Mann–Whitney test) (Fig. 2). Similar to gastropods, recently extinct and endangered bivalves use far fewer habitat types than either exotic (3.75 ± 0.30, recently extinct vs. exotic, P < 0.001; endangered vs. exotic, P < 0.001) or native transplant species (4.22 ± 0.43; recently extinct vs. native transplant, P = 0.006; endangered vs. native transplant, P = 0.004). For bivalves, however, there was no difference in the habitat breadth of exotic and native transplant species (P = 0.15).

Recently extinct and endangered bivalves use similar habitat types (P = 0.34, Fisher–Freeman–Halton test) (Fig. 3). Recently extinct bivalves were even more limited to lotic environments than gastropods. Among recently extinct gastropods, two species were known to live in lakes, while all recently extinct bivalves were found in rivers, and most were restricted to large rivers. Again, the habitat use of recently extinct and endangered and threatened species of bivalves was different than that for native transplant and exotic species (all P < 0.001). Like gastropods, native transplant and exotic bivalves use similar habitat types (P = 0.21). Over 75% of all native transplant and exotic bivalves live in lakes and reservoirs, while none of the recently extinct and only one endangered and threatened species of bivalves can be found in those habitats.

Discussion

The impact of humans on natural communities has dramatically accelerated both immigration and extinction or extirpation of species already established in a system. The balance of these processes is generally expected to result in the loss of biodiversity and taxonomic homogenization, and such impacts are likely to differ when considered at different spatial scales (McKinney & Lockwood, 1999; Rahel, 2000; Olden et al., 2006; Villéger et al., 2011). These impacts are especially evident in freshwater ecosystems, which are seeing recent high rates of extinctions as well as high rate of the introductions of invaders (Ricciardi & Rasmussen, 1999; Gurevitch & Padilla, 2004; Régnier et al., 2009; Strayer & Dudgeon, 2010). We found that both extinctions and introductions among freshwater invertebrates are not random. The same taxa, namely crustaceans and molluscs, are overrepresented among introduced species, as well as those that have gone extinct or are in danger of extinction or extirpation (Table 1). Freshwater molluscs are especially diverse in North America, which has half of the world’s known freshwater gastropod diversity and the greatest diversity of known freshwater bivalves in the world; they are also the most imperiled group of animals in North America (Bogan, 1993; Williams et al., 1993; Lydeard et al., 2004; Johnson et al., 2013). This group also includes the highest number of exotic species (Karatayev et al., 2009a). However, for both bivalves and gastropods, the families of recently extinct, endangered, and imperiled species are different than those for exotic species (Table 2). The bivalve family Unionidae (292 species) and the gastropod families Pleuroceridae (162 species) and Hydrobiidae (185 species) are all exceptionally diverse in North America, but are also declining in diversity due to extinction, and are the families with the greatest numbers of threatened and endangered species (Johnson et al., 2013). In contrast, the most common exotic species of gastropods are in the family Ampullariidae, and the families Sphaeriidae, Dreissenidae, and Corbiculidae for bivalves, with the two last families currently spreading at extremely high rates (reviewed in Karatayev et al., 2007, 2015). However, there is little habitat overlap among native species of bivalves and gastropods and invaders.

Two opposite hypotheses have been erected regarding the properties of species that can successfully invade a community. One hypothesis is that species that are physiologically and ecologically similar to native species will be preadapted to local conditions, and can, therefore, successfully invade a community (Li et al., 2015). In contrast, the hypothesis of biotic resistance (e.g., Levine & D’Antonio, 1999; Tilman, 2004) suggests that due to high niche overlap, species that are very similar to local species will be less likely to invade due to competition from native species. Previous work on plants seems to support this latter hypothesis. Strauss et al. (2006) found that highly invasive grass species are, on average, significantly less related to native grasses than are introduced but noninvasive grasses. Similarly, Schaefer et al. (2011) found that introduced plants are more likely to become invasive in the absence of closely related species. Although our results are consistent with this latter hypothesis in terms of the lack of taxonomic overlap between invaders and native freshwater species, our data also support the empty niche hypothesis (Elton, 1958; Levine & D’Antonio, 1999; Fridley et al., 2007), whereby invaders can be successful in habitats where they have low niche overlap with other species.

Exotic and native transplant molluscs not only differ taxonomically from recently extinct, endangered, and imperiled species, but they also occupy different habitats (Figs. 2, 3). Native species that have gone extinct were found primarily in creeks and rivers, while introduced species preferentially inhabit lakes and reservoirs. Therefore, for freshwater molluscs the introduction of exotic species will not compensate for the loss of biodiversity. This “taxonomic clustering of losers and winners,” when evolutionarily shared traits bias some groups towards extinction and others towards range expansion or invasion, enhances the effect of homogenization (McKinney & Lockwood, 1999). Native mussels in North America attain greatest diversity and density in streams and rivers with strong currents. Although questions about diversification and the biogeography of molluscs in freshwaters remain, some studies have suggested that rivers were probably the original habitats for bivalves which invaded freshwater, while their transition to lentic habitats came later (Parmalee & Bogan, 1998). Most freshwater gastropods associated with lotic habitats are endemics with very small distributions, and are often isolated within individual springs, river reaches, or geographically restricted river basins (Johnson et al., 2013). During the twentieth century in the Unites States alone, humans have constructed over 75,000 dams over 2 m in height. Dams are now found on average every 70 km along 5.2 million km of streams and rivers in the US. As a result, there are currently only 42 large rivers (over 200 km in length) with flow regimes unaffected by dams (reviewed in Poff et al., 2007). Continued construction of reservoirs will increase habitat for invaders and reduce habitat for both native range-restricted molluscs and the fishes used by many freshwater bivalve larvae as hosts, promoting taxonomic homogenization and a continued decline in diversity (Havel et al., 2005; Poff et al., 2007; Burlakova et al., 2011; Clavero & Hermoso, 2011).

Negative impacts of exotic molluscs on native species are well documented for gastropods (reviewed by Karatayev et al., 2009b). The introduction of a single exotic bivalve, Dreissena polymorpha, has been associated with large declines in populations of native unionid species (reviewed in Burlakova et al., 2014; Lucy et al., 2014); however, no extinctions in freshwater macroinvertebrates has been directly attributed to species introductions (Gurevitch & Padilla, 2004). Direct competition between native and introduced molluscs is likely to be rare as these taxa often reside in completely different habitats (natives in lotic and invaders in lentic habitats), suggesting that habitat loss associated with human activity has by far a stronger negative impact on molluscan diversity than introduced species.

The consequences of species additions and loss and the level of diversity homogenization will likely be scale dependent (Sax et al., 2002; Sax & Gaines, 2003; Villéger et al., 2011; Fig. 1). At the global scale, species diversity is only affected by extinction and speciation (Sax & Gaines, 2003). At a local scale (e.g., lakes or rivers within a watershed), local communities are connected through the dispersal of multiple species forming metacommunities (Wilson, 1992; Leibold et al., 2004). At this scale, diversity is positively affected by immigration of native species from the same metacommunity, the introduction of native transplant species from a nearby region outside the metacommunity (e.g., from another watershed), and the introduction of exotic species. Also at the local scale, the decline in diversity due to the local extirpation of a species typically will not cause a species extinction, as the system could be recolonized by that same species from a nearby waterbody. However, for species that are endemic to a particular lake or river, extirpation from one system may lead to extinction (e.g., Miller et al., 1989). Local extinctions may be especially evident for taxa at the centers of species radiations, which have large numbers of endemics. North America is the center of diversity for unionid bivalves, as well as hydrobiid and pleurocerid gastropods. These groups also have the greatest number of recently extinct, and threatened and endangered species, and are thus most vulnerable to continued anthropogenic impacts.

On a regional scale, immigration of a native transplant species from a watershed outside the metacommunity with no coevolutionary history with the local community may result in negative ecological consequences. Extirpation of a species from an entire watershed may cause extinction if its range is limited to that particular watershed (e.g., regional endemics) which is quite common as many species of freshwater invertebrates are limited to a single drainage system (Strayer, 2006). At a continental scale, the introduction of exotic invaders from a different continent usually means that the invader is distinct phylogenetically and has no recent coevolutionary history with native species or communities. Therefore, such an introduction has a high probability of significant ecological impacts. Extirpation of a species from a continent typically results in species extinction (with the exception of cosmopolitan species), and a loss in global diversity.

Overall, the impact of humans on species introductions and extinctions increases with the spatial scale from the local to continental, and as a result, the increased phylogenetic dissimilarity of the introduced species with native communities (Fig. 1). At the same time, the importance of natural processes in introductions and extinctions decreases. It has been suggested that while at a global scale the loss of biodiversity is evident, at regional and local scales species diversity might be increasing as exotic introductions have outpaced the loss of native species (Hobbs & Mooney, 1998; Sax et al., 2002; Sax & Gaines, 2003; Dornelas et al., 2014). For example, the net species diversity of vascular plants has increased on islands since the arrival of humans, and within regions on continents since the arrival of Europeans to Australia and North America (reviewed in Sax et al., 2002; Sax & Gaines, 2003). Net increases in species diversity with increasing species introductions on a regional scale have also been reported for reptiles, amphibians, mammals, and freshwater fishes (Wilson, 1997; Hobbs & Mooney, 1998). Freshwater molluscs, however, clearly show the opposite trend; the loss of freshwater molluscs has occurred at a much higher rate than exotic introductions. Of the 40 species of recently extinct freshwater gastropods in North America for which the cause of extinction is known, 34 species were endemic to the Coosa River, Alabama. The damming of this single river (local scale effect) caused extinction of 74% of all officially listed extinct gastropods in the US (US Fish and Wildlife Service Environmental Conservation Online System 2015). At the regional scale, in Texas where there are no naturally occurring lentic waters, only 2 of 14 regionally endemic unionid species are able to survive in reservoirs (Burlakova et al., 2011). In the Rio Grande drainage in Texas, two unionid species have already gone extinct from this region. Damming of the Rio Grande has caused local extirpation of three additional endemic unionids and fragmentation of their population ranges (Karatayev et al., 2012). In contrast, only two exotic bivalves, Corbicula fluminea and D. polymorpha, have colonized Texas thus far (Karatayev et al., 2005; Benson et al., 2016). Finally, at the continental scale, in North America 79 species of molluscs are already extinct, 113 species are listed as endangered or threatened, and 728 species are considered imperiled. Thus, the rate of extinction for molluscs far exceeds the rate of introduction of exotic species (38 species) (Table 2). Therefore, the net outcome of biotic homogenization is not only scale dependent, but also taxon dependent.

Molluscs are the most imperiled group of animals in North America (Bogan, 1993; Lydeard et al., 2004), and clearly show a strong decline in biodiversity that is not compensated by species introduction. In contrast, many other taxa, including plants, mammals, birds, reptiles, amphibians, and freshwater fishes, show net increases in diversity in California and Australia (reviewed in Hobbs & Mooney, 1998). This pattern is also true for freshwater crustaceans. They are the second largest freshwater invertebrate group considered imperiled in North America; however, there are twice as many exotic (50 species) and native transplant species (51 species) than officially listed endangered and threatened species (Table 1).

Both gastropods and bivalves are more diverse in North American freshwaters than any other region globally. They are by far the most striking examples of the loss of biodiversity and homogenization to date, and display the prediction of what happens when “a few winners replace many losers” (McKinney & Lockwood, 1999). Virtually all extinct and the majority of imperiled bivalves and gastropods are lotic species. The construction of dams is one of the most widely distributed human impacts on freshwaters around the globe, causing flow alterations, fragmentation of fluvial networks, and large-scale disruption of sediment transport (Poff et al., 2007; Clavero & Hermoso, 2011). Extreme changes in this habitat can cause extinction of native lotic species, while simultaneously promoting the spread of lentic molluscs, including exotic and native transplant species. Continued human impact will likely cause ever increasing loss of freshwater molluscan diversity, which will not be compensated by the continued introduction of invaders. The impacts of species introductions on freshwater molluscs may be especially acute in North America because it is the geographic center of diversity for this group. The local isolation of freshwater habitats may result in a high degree of speciation and endemism as is seen on islands, where introduced species can have devastating effects on local endemics. Similar patterns may be important for other taxa in geographic regions where endemic biodiversity is especially high.

Notes

Acknowledgements

We thank Drs. F.J. Rohlf and H. Lynch for statistical advice, and anonymous reviewers whose comments helped improve this manuscript. This is contribution number 1249, Department of Ecology and Evolution, Stony Brook University.

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Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Alexander Y. Karatayev
    • 1
    Email author
  • Lyubov E. Burlakova
    • 1
    • 2
  • Dianna K. Padilla
    • 3
  1. 1.Great Lakes CenterBuffalo State CollegeBuffaloUSA
  2. 2.The Research Foundation of The State University of New York, Buffalo State CollegeOffice of Sponsored ProgramsBuffaloUSA
  3. 3.Department of Ecology and EvolutionStony Brook UniversityStony BrookUSA

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