Temporal trends in non-indigenous freshwater species records ... - USC

Biodivers Conserv (2010) 19:3471–3487 DOI 10.1007/s10531-010-9908-8 ORIGINAL PAPER

Temporal trends in non-indigenous freshwater species records during the 20th century: a case study in the Iberian Peninsula Fernando Cobo • Rufino Vieira-Lanero • Enrique Rego Marıá J. Servia

•

Received: 16 March 2010 / Accepted: 6 August 2010 / Published online: 24 August 2010 Ó Springer Science+Business Media B.V. 2010

Abstract Galicia (NW Spain) is a region with a high number of freshwater endemics, and probably the best preserved area concerning fish populations in the Iberian Peninsula, where records of non-indigenous freshwater species are recent when compared to the rest of the Peninsula. Detailed analysis of introductions of those species with records after 1900 present in both areas shows that delays were up to 100 years for species introduced on the Iberian Peninsula at the beginning of the twentieth century, but the tendency adjust to a decreasing linear regression, with species introduced after 1995 being almost immediately present in Galicia. We underline the outstanding role of aquarium trade on these results. Analysis of temporal trends highlights several periods with numerous introductions, and shows a different trend in the last decade depending on the group of organisms, with a clear deceleration in introduction rates of vertebrates, but a continuous growing trend for invertebrates. Recent educational programs might be responsible for the reduction in the inflow of vertebrates, but there is still a need for the control of less conspicuous but equally harmful invertebrates and plants, as it will take longer to make both stakeholders and public aware of their detrimental effects on their new habitats. Keywords Non-indigenous species Freshwater habitats Temporal trends Galicia Iberian Peninsula Aquarium trade F. Cobo R. Vieira-Lanero Departamento de Zooloxıá e Antropoloxıá Fı´sica, Universidade de Santiago de Compostela, Campus Sur s/n, 15782 Santiago de Compostela, Spain F. Cobo R. Vieira-Lanero Estacioń de Hidrobioloxıá ‘‘Encoro do Con’’, Castroagudıń s/n, 36617 Vilagarcıá de Arousa, Pontevedra, Spain E. Rego Avda. das Carolinas 50, 36600 Vilagarcıá de Arousa, Pontevedra, Spain M. J. Servia (&) Departamento de Bioloxıá Animal, Bioloxıá Vexetal e Ecoloxıá, Facultade de Ciencias, Universidade da Corunã, Campus da Zapateira s/n, 15008 A Corunã, Spain e-mail: [email protected]

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Biodivers Conserv (2010) 19:3471–3487

Introduction Organisms have been moved around the world as consequence of human activities throughout History, but some of these species have severely affected their new habitats, changing the composition of the original communities and even their physical habitat. Thus, one of the many examples of the initiatives promoted to achieve a better knowledge on alien species is the European program SEBI2010 (Streamlining European 2010 Biodiversity Indicators). This program includes invasive alien species among the set of biodiversity indicators used to assess and inform about the status of biodiversity in Europe, as they constitute an important threat (EEA 2007). Freshwater ecosystems have been the recipients of many alien species, both by unintentional or deliberate introductions (Gherardi et al. 2008). Some areas, such as the North American Great Lakes or central Europe, have been reported to be severely affected by freshwater invasions, mainly due to the existence of inland navigational routes (Ojaveer et al. 2002). Contrastingly, despite the decades invested in taxonomic and faunistic studies, experts state that it is still difficult to get a good overview of biodiversity of freshwater ecosystems, as available knowledge is largely scattered and focused on a few well-studied groups (Balian et al. 2008). As a consequence, the presence of Non-Indigenous Freshwater Species (NIFS) might introduce important biases on initiatives promoting the biodiversity assessment of certain areas, mainly in groups where inadvertent introductions are frequent (Strong et al. 2008), as they might be considered as indigenous species, or they might be responsible of the extinction of many others. NIFS have already arrived to areas where potential for introduction is apparently low. Galicia (NW Spain) (Fig. 1) is a region that presents clear natural boundaries that isolate it from the rest of the Iberian Peninsula (IP), with the river Minõ on the South and a mountain range on the East. It has a dense river network, with numerous small coastal rivers with high slope and, except for the lower part of the river Minõ, none of them are navigable. Besides, dams are more recent and smaller than those constructed in the rest of Spain, with a delay of almost 15 years on the average date of construction (estimation done using the database of the Spanish Dams and Reservoirs Society, SEPREM 2010). All these reasons might help to explain why detection of many NIFS in Galicia is recent when compared to the rest of the IP, as authors have established a clear association between navigation and river impoundment with the presence of NIFS (see for example Clavero et al. 2004; Filipe et al. 2004; Durań and Anadoń 2008; Ribeiro et al. 2008). Although the presence of NIFS in Galicia is recent, researchers have underlined their steep increase on recent years, and alert against their potential detrimental effects (Gonza´lez and Cobo 2006). Concerns arise as this region presents both a high biodiversity and a high number of endemic species linked to freshwater habitats. Thus for example, although estimates on the number of endemic invertebrates are difficult to make due to the lack of complete inventories (Sańchez-Fernańdez et al. 2008), medium altitude streams of the eastern part of Galicia have been highlighted as habitats with a very rich fauna of aquatic Coleoptera, in particular endemic species, and they have been considered among the habitats to have the highest conservation value in what refers to Iberian aquatic Coleoptera (Ribera 2000). As a consequence, local population extirpations due to NIFS could represent global extinctions. Concerning aquatic vertebrates, Galicia is well known for the high diversity of amphibians (Galań 1999), and it is probably the best preserved area concerning fish populations in the Iberian Peninsula (Elvira and Almodo´var 2001). Thus, this paper aims at (i) making a complete compilation of NIFS in a region with high number of endemics but sparse data on alien species, which represent an obvious

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Fig. 1 Study area, with Galicia (NW Spain) highlighted

threat to those endemics, and (ii) analysing the temporal trends of NIFS records in Galicia when compared to the IP, as they may help identifying important time intervals and factors for introductions, which might be useful for the establishment of policies for prevention, control and mitigation of impacts in similar small watersheds.

Materials and methods Due to lack of information of NIFS on the area, and with the aim of offering an exhaustive revision and reducing bias on the results, most of the data used in this study have been gathered from scientific literature, but we have included also many references of grey literature and information obtained during extensive sampling campaigns of researchers working at the Hydrobiological Field Station of the University of Santiago de Compostela (Galicia, Spain) during recent years (See Appendix 1). For NIFS on the IP, we have used a recent review by Garcıá-Berthou et al. (2007), although we have reviewed also grey literature from Spain and Portugal in order to confirm dates of introduction. As recommended by the European Environment Agency (EEA 2007), organisms included in this review are grouped into vertebrates, invertebrates (excluding parasites) and macrophytes (excluding helophytes).

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Appendix 1 lists NIFS detected on natural areas. For year of first record, we maintain the year of first publication when no other date was found. For temporal analysis, time intervals such as decades have been replaced with the midpoint. Records that need further confirmation are highlighted. As supplementary information, translocated species to Galicia were included when they were introduced from other areas of the IP. We have not included records already considered as clear failed introductions by the authors (see for example Ribeiro et al. 2009). In order to evaluate the importance of introduction vectors a v2 test was performed, using only those species with known invasive status (categories: invasive, naturalized, naturalized/invasive. See Appendix 1). Temporal trends of introductions have been analysed using the cumulative number of NIFS from 1900 onwards in ten-year intervals; pre-1900 introductions were also estimated (EEA 2007). Delay of arrival to Galicia with respect to the IP for those species with records after 1900 is offered as mean ± S.E. We analysed the differences in trends between both areas using the software TRIM (TRends and Indices for Monitoring data; Pannekoek and van Strien 2005). TRIM is software for the analysis of time series of counts that estimates yearly indices and trends, and assess the effects of covariates on them, using a Poisson general log-linear model (McCullagh and Nelder 1989) and accounting for overdispersion and serial correlation of the data. TRIM permits trends to be established in parts of the time series by using change points, which are time points where a significant change in the slope parameter happens. In order to get the most parsimoniuous model (a model with as few parameters as possible without compromising its explanatory power), TRIM implements a stepwise model selection procedure (Pannekoek and van Strien 2005). This procedure repeats the following steps: 1. Calculation of Wald statistics for the difference of the parameters before and after each change point and their associated significance levels. If the largest significance level exceeds a certain threshold value (default probability: 0.20) the corresponding change point is removed from the model. 2. For all removed change points except the last one, calculation of a score statistic to assess the significance of the difference in parameters before and after the change point. If the smallest significance level is smaller than a threshold value (default probability: 0.15) the change point is added to the model. The procedure stops if no change points can be either removed or added. We took the year 1900 as the starting point of the series and included ‘‘Area’’ as a covariate with two categories (Galicia and IP). We have analysed trends for the whole number of NIFS, as well as for vertebrates and invertebrates independently. Analysis of trends for macrophytes was not possible due to the low number of species and their recent introduction.

Results In terms of numbers, there are clearly less records of non native freshwater species in Galicia than in the rest of the IP, with a total number of 31 NIFS for Galicia and 88 for the IP (See Appendix 1). Detailed analysis of introductions of those species with records after 1900 present in both areas shows that medium delay for their arrival to Galicia with respect to the IP was 12.75 ± 4.64 years for invertebrates, 42.33 ± 27.55 years for vertebrates, and 56.75 ± 17.38 years for hydrophytes. Two species, Haliplanella lineata and Xenostrobus securis, were cited for the first time in Galicia (Ramil 1987; Garci et al. 2007).

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120

Delay (years)

100 y = -0.9476x + 1890.6 R 2 = 0.7659

80 60 40 20 0 -20 1900

1910 1920

1930 1940

1950 1960

1970 1980

1990 2000

2010

Date of introduction Fig. 2 Relationship between the date of first introduction in the IP and the delay for introduction in Galicia (years) of non indigenous freshwater species (NIFS)

A scatter plot (Fig. 2) shows that delays were up to 100 years for species introduced on the IP at the beginning of the 20th century, but the tendency adjust to a decreasing linear regression, with species introduced on the IP after 1995 being almost immediately present in Galicia. Concerning pathways of introduction in Galicia, statistical analysis shows an outstanding role of aquarium trade on the arrival of species (v2 = 12.8, d.f. = 4, P = 0.012, n = 25). Indeed, some of these have become invasive in a short time. Examples are the slider turtle (Trachemys scripta) (Pleguezuelos 2002), or the macrophytes Egeria densa, Eichhornia crassipes and Azolla filiculoides, all of them introduced in the last 20 years. Using the whole number of NIFS in both areas, temporal analysis of their arrival reveals a steep increase in their number after 1970, both for the total number of species and for each of the groups (Fig. 3). However, trends of cumulative number calculated using TRIM software (Fig. 4) show that for total NIFS Galicia presents steeper slopes than the IP during almost all the studied period (Fig. 4a). Differences are clear for the 1931–1970 periods, even if Galicia was incorporating less NIFS than the IP (Fig. 3a). However, as trends reflect changes from the starting point of the series (1900), and the starting number of NIFS in Galicia was lower than that of the IP, small incorporations are shown as big changes. Interestingly, however, this tendency persists for the 1981-2009 periods, when number of NIFS had notably increased. Independent analyses of trends for invertebrates and vertebrates show that changes in introduction rates in invertebrates are non significant for Galicia, which means that the introduction rate has been constant during the whole period (Fig. 4b). As for the IP, the most significant increase in the introduction rate occurs during 1981–1990. In the case of vertebrates (Fig. 4c), more significant changes are detected, with important introductions in the IP during 1901–1910, 1941–1950 and 1991–2000. For Galicia there is a long period of almost 50 years with no introductions, with the first of the century occurring during 1941–1950. A second important change appears also after a period of 20 years with no introductions, in 1981–1990. Especially noteworthy are the divergent results obtained for the two groups during the last decade (2001–2009), since for vertebrates there is a significant deceleration on the introduction rates both for the IP and Galicia, while for invertebrates slopes show no changes in any of the areas.

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b 90 80 IP

70

GALICIA

60 50 40 30 20 10 0

Cumulative number of NIFS


a

40

IP

20

10

0 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2009

1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2009

c

GALICIA

30

d IP

40

GALICIA

30

20

10



20 50

IP

GALICIA

10

0

0 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2009

1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2009

Fig. 3 Cumulative number of non-indigenous freshwater species (NIFS) recorded in the Iberian Peninsula (IP) and Galicia. (a) Total NIFS, (b) invertebrates, (c) vertebrates and (d) macrophytes

Discussion Despite the obvious constraint watersheds represent for the spread of freshwater fauna, introductions of NIFS in the IP have been reported in many papers, mainly concerning animals (see for example reviews in Elvira and Almodo´var 2001 or Garcıá-Berthou et al. 2007). In Galicia, at the present moment invertebrate NIFS contribute for 0.91% of the whole freshwater invertebrate fauna (estimated to amount to over 1320 species; Gonza´lez and Cobo 2006), while vertebrates associated to freshwater habitats contribute for about 16.7% (total estimated number: 55 species, De Castro 2002) and macrophytes for 5% (total estimated number: about 120, Romero-Bujań 2008). These figures are well under those already reported for other areas (Gherardi et al. 2008; Keller et al. 2009), and most of these aliens were not reported to be present in the region until the last two decades. Reasons for this are diverse. Thus, as mentioned in the Introduction section, most Galician rivers are not navigable, and rates of river impoundment are well under those of other watersheds. In addition, we should stress also the fact that, in contrast with other areas of the IP, Galicia have never suffered from aggressive programs of introductions. This has been the case for example of lake Banyoles (NE Spain), where numerous species of freshwater fishes have been introduced since the beginning of the XXth century (Garcıá-Berthou and MorenoAmich 2000). Indeed, nonnative assemblages of northeastern Iberian basins have been found to be more similar to those of France than to those of the rest of the Iberian Peninsula, indicating a main introduction route (Clavero and Garcıá-Berthou 2006). Fig. 4 Multiplicative slopes (± 95% CIs) standing for the changes in the cumulative number of non- c indigenous freshwater species (NIFS) recorded in the Iberian Peninsula (IP) and Galicia as calculated by TRIM (see Methods). (a) Total NIFS, (b) invertebrates and (c) vertebrates

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a

3477

1.8 IP GALICIA

Slope

1.4

1.0

0.6 1901-10 1911-20 1921-30 1931-40 1941-50 1951-60 1961-70 1971-80 1981-90 1991-00 2001-09

b

2 IP GALICIA

Slope

1.6

1.2

0.8 1901-10 1911-20 1921-30 1931-40 1941-50 1951-60 1961-70 1971-80 1981-90 1991-00 2001-09

c

3 IP GALICIA

Slope

2.1

1.2

0.3 1901-10 1911-20 1921-30 1931-40 1941-50 1951-60 1961-70 1971-80 1981-90 1991-00 2001-09

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Certainly, some of the literature we have reviewed may contain inaccuracies, and the undersampling of some groups, mainly invertebrates and plants, may have changed some results of our work. Thus for example, an important contribution to the clear increase in records on the IP during 1981–1990 is the work done on Crustaceans by Paulo and Moutinho (1983), Fore´s et al. (1986) and Baltana´s et al. (1996). This fact stresses the sudden changes in records that can occur when important gaps in the knowledge of certain taxa are filled. However, at the present moment aquarium trade seems to be the dominant vector of introduction of NIFS in Galicia, as it has already been shown in other areas (Padilla and Williams 2004; Rixon et al. 2005; Karatayev et al. 2009; Ribeiro et al. 2009), and it has been highlighted as a priority target for legislation (Keller et al. 2009; Strayer 2010). Indeed, the analysis of the delay for the arrival to Galicia of NIFS introduced in the IP after 1900 reveals, as expected, a clear reduction and, interestingly, the decreasing linear regression that best fits the data intersects the x-axis (delay = 0) around 1995, the same year the Schengen agreement opened the international borders to the free circulation of persons and goods. This event has probably facilitated the uncontrolled translocation of organisms, mainly vertebrates, across international borders, and it could also favour the arrival of invertebrates and plants, either deliberately or accidentally transported. Actually, this effect has been observed in Eastern European countries, as their integration to the European Union has boosted the spread of invasive bird species (Chiron et al. 2010). However, the Schengen agreement has been linked to social and economic changes, and more investment on research and therefore more capacity in detecting new species, or more researcher’s awareness on NIFS problems, might have had an important influence on this result. An important outcome of the trends analysis is the deceleration shown for rates of vertebrate NIFS introductions in the last decade, both for the IP and Galicia. Indeed, our study shows few new vertebrate NIFS in the list in comparison with those listed by GarcıáBerthou et al. (2007). However, invertebrates show no changes in recent rates of introduction, neither in the IP nor in Galicia, which indicates a continuous growing trend. Both Portugal and Spain have adopted a number of legislative instruments for the control and mitigation of impacts of invasive species (See for example in Portugal: Decreto Ley 565/1999, in Spain: Ley 42/2007, del Patrimonio Natural y de la Biodiversidad), which include the prohibition of trade with exotics known to be invasive. However, there is still much work to be done for achieving a real control of NIFS trade, as the increasing number of aquarists and the easy communication among them using the numerous forums on the web have increased the exchanging of organisms, with the associated risk of escapes or a final release in natural habitats (Padilla and Williams 2004). Thus, it is probable that the different tendency observed in invertebrates and vertebrates is due to the influence of education programs on exotic species, as at least some vertebrates are already perceived by stakeholders and general public as harmful invasives. Contrastingly, there is still much work to be done on the less conspicuous but equally harmful invertebrates and plants, as it will take longer to make both stakeholders and public aware of their detrimental effects on their new habitats. A step forward will be to evaluate the invasion risk posed by species used in aquarium trade, as it has already been done on the Great Lakes (Rixon et al. 2005), as well as to better understand the impact of NIFS on freshwater endemics. Analysis of trends in geographical areas where introductions of NIFS are also recent might help to better pinpoint the causes of the problem, as well as to efficiently design protective measures against new introductions.

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Acknowledgements We thank two anonymous reviewers for the helpful comments on the manuscript. Facilities needed for this work were provided by the Hydrobiological Field Station ‘‘Encoro do Con’’ (University of Santiago de Compostela). This study was supported by project CGL2009-10868 of the Ministry of Education and Science (Spain).

Appendix 1 Non-indigenous freshwater species recorded in the Iberian Peninsula and Galicia. Status and Pathway/Vector only listed for Galicia. NR: No record. **: Records that need to be confirmed. \: Before. [: After. Habitat (HB): 1: Streams and rivers (excluding estuaries); 2: Lakes and reservoirs; 3: Ponds and pools; 4: Rice fields; 5: Estuarine or saline waters. Status (ST): U: Unknown; N: Naturalized; I: Invasive; N/I: Invasive only in certain locations. Pathway/Vector (P/V): A: Angling; AB: Angling, bait; AQ: Aquaculture; AT: Aquarium trade; F: Fouling; FE: Farm escapes; FP: Fouling, secondary dispersal from Portugal; IR: Intentional release; U: Unknown (Table 1). Table 1 Group/species

First record IP

Reference

HB

Garcıá-Berthou et al. (2007)

1,2,5

Gonza´lez and Cobo (2006) Garcıá-Berthou et al. (2007)

1,2

ST P/V

Galicia

Cnidaria Cordylophora caspia (Pallas, 1771)

2001

Craspedacusta sowerbyi Lankester, 1880

1968 1994

Gonza´lez and Cobo (2006)

Haliplanella lineata (Verrill, 1869)

1987

1987

Ramil (1987)

5

Blackfordia virginica Mayer, 1910

1987

NR

Moore (1987)

5


1,2

2006

N

F

U

U

N

F

Platyhelmintha Girardia tigrina (Girard, 1850)

U 2006

Gonza´lez and Cobo (2006)

Dendrocoelum lacteum (Mu¨ller, 1774)

1993

NR

Carranza and Giribet (1997)

Gyraulus chinensis (Dunker, 1848)

1979

NR


2,4

Physella acuta (Draparnaud, 1805)

1845

Morelet (1845)

1,2,4

N/I AT

Mollusca

1932

Pardo (1932) (as Physa acuta)

Physella gyrina (Say, 1821) 1988

NR

Altaba et al. (1988)

Helisoma duryi seminole Pilsbry, 1934

NR

Altaba et al. (1988)

1984

N/I U

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3480


Table 1 continued Group/species

First record IP

Reference

HB

Boettger (1951)

1,5

ST P/V

Galicia

Potamopyrgus antipodarum 1951 (Gray, 1853) 1963

Lucas (1963)

Bulinus contortus (Michaud, 1829)

1845

Pomacea canaliculata (Lamarck, 1822)

2009 ** NR

GEIB (2009)

1,2,3

Corbicula fluminea (Mu¨ller, 1774)

1981

Mouthon (1981)

1,3,5

1989

Araujo et al. (1993)

Dreissena polymorpha (Pallas, 1771)

1880

NR

Servain (1880)

1,2

Mytilopsis leucophaeta (Conrad, 1831)

1993

NR


1,2,5

Xenostrobus securis (Lamarck, 1819)

2005

2005

Garci et al. (2007)

5

Branchiura sowerbyi Beddard, 1892

1970s

NR


1,2,5

Ficopomatus enigmaticus (Fauvel, 1923)

1924

NR


5

Hirudo troctina (Johnson, 1816)

1893

1893

Blanchard (1893)

1,2,3

Artemia franciscana (Kellog, 1906)

1980s

NR


5

Wlassicsia pannonica Daday, 1904

1990s

NR


4

Dolerocypris sinensis Sars, 1986 1903

NR


3,4

Ilyodromus viridulus (Brady, 1886)

1996

NR


4

Cypris sp.(=Cypris 1986 subglobosa Sowerby, 1840)

NR


2,4

Isocypris beauchampi (Paris, 1920)

1976

NR


2,4

Stenocypris major (Baird, 1859)

1986

NR


3,4

Strandesia vavrai (Mu¨ller, 1898)

1983

NR


4

Strandesia vinciguerrae (Masi, 1905)

1986

NR


4

Tanycypris sp.

1988

NR

1990s

NR

Synidotea laticauda Benedict, 1897

1996

NR

Garcıá-Berthou et al. (2007) Garcıá-Berthou et al. (2007) Garcıá-Berthou et al. (2007)

3,4

Acartia tonsa Dana, 1849

I

U

U

AQ

I

FP

I

AO

U

U

Morelet (1845) 1999

Rolań et al. (1999)

Annelida

Crustacea

123

5 5


3481


First record

Reference

HB

IP

Galicia

Cherax destructor Clark, 1936

1983

NR


5

Eriocheir sinensis Milne Edwards, 1853

1988

NR


5

Pacifastacus leniusculus (Dana, 1852)

1974

Carral et al. (1993)

1

Palaemon macrodactylus MJ Rathbun, 1902

1999

Xunta de Galicia (2009) Garcıá-Berthou et al. (2007)

5

Procambarus clarkii (Girard, 1852)

1973


1,2,4,5

Rhithropanopeus harrisii (Gould, 1841)

1990

NR

Mariscal et al. (1991)

5

Aedes albopictus (Skuse, 1895)

2004

NR


3

Stenopelmus rufinasus Gyllenhal, 1835

2002

NR

Fernańdez-Carrillo et al. (2005)

1,2,4,5

Trichocorixa verticalis (Fieber, 1851)

1997

NR


3,5

Abramis bjoerkna (Linnaeus, 1758)

1995

NR

Elvira (1998)

1,2

Abramis brama (Linnaeus, 1758)

2004

NR


2

Acipenser baerii Brandt, 1869

1995

NR

Elvira and Almodo´var (1999)

Alburnus alburnus (Linnaeus, 1758)

1992

NR

Elvira (1995)

1,2

Ameirus melas (Rafinesque, 1820)

1910

NR

Elvira and Almodo´var (2001)

1,2

Aphanius fasciatus (Valenciennes, 1821)

1997

NR


3

Australoheros facetus (Jenyns, 1842)

1943

NR

Helling (1943)

1,2

Carassius auratus (Linnaeus, 1758)

17th cent.

17th cent.

Loboń-Cervia´ et al. (1989)

1,2,3

NR


1

Lozano-Rey (1935)

1,2

Gutie´rrez-Calderoń (1954)

1,2

2009 ** NR

1980s

ST P/V

U

U

I

IR

N

AT

N

AT

U

A

Insecta

Pisces

Cobitis bilineata Canestrini, 2002 1865 Cyprinus carpio Linnaeus, 1758

17th cent. 18th cent.

Esox lucius Linnaeus, 1758 1949 2007**

Press note (2008). C. H. MinõSil

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3482



First record

Reference

HB

IP

Galicia

Fundulus heteroclitus (Linnaeus, 1766)

1970

NR

Gambusia holbrooki (Girard, 1859)

1921

Gobio lozanoi Doadrio & Madeira, 2004

Authoct. 1998

Hervella and Caballero (1999) 1,2,3

Hucho hucho (Linnaeus, 1758)

1968

NR

Mondejar (1981)

1

Ictalurus punctatus (Rafinesque, 1818)

1995

NR


1,2,3

Lepomis gibbosus (Linnaeus, 1758)

1910


1,2


4

Na´jera (1944)

1,2,3,4

[1940

Misgurnus anguillicaudatus 2001 (Cantor, 1842)

N/I AT

2005

Comesanã and Ayres (2009)

NR

Franch et al. (2008)

3,4

Godinho and Ferreira (1994)

1,2

Micropterus salmoides (Lace´pe`de, 1802)

1952

Oncorhynchus mykiss (Walbaum, 1792)

1898

Oncorhynchus kisutch (Walbaum, 1792)

1983

Perca fluviatilis Linnaeus, 1758

1975

Phoxinus bigerri Kottelat, 2007

Authoct.

Poecilia reticulata Peters, 1859

2000

NR

Hervella and Caballero (1999) Garcıá-Berthou et al. (2007) 1,4

Pseudorasbora parva (Temminck & Schlegel 1846)

1999

NR

Caiola and de Sostoa (2002)

1

Rutilus rutilus (Linnaeus, 1758)

1910

NR


1,2

Salvelinus fontinalis (Mitchill, 1814)

19th cent.

NR

Lozano-Rey (1935)

1,2

Sander lucioperca (Linnaeus, 1758)

1975

NR


1,2

Scardinius erythrophthalmus (Linnaeus, 1758)

1910

NR

Sostoa et al. (1990)

1,2

Silurus glanis Linnaeus, 1758

1974

NR


1,2


2,3

1982

1,2

NR

Callejo et al. (1982) Garcıá-Berthou et al. (2007)

1

NR


1,2

123

N

AB

N

AT

N

A

NN AQ

Garcıá-Berthou et al. (2007) 1990s

Tinca tinca Linnaeus, 1758 12th cent.

Callejo et al. (1982) Welcomme (1988)

1982

ST P/V

N

AB


3483


First record IP

Reference

HB

ST P/V

Galicia \1991

Hervella and Caballero (1999)

NR


1

Tauxe et al. (1985)

1,2,3,4

N

A

I

AT

N

AT

Amphibia Discoglossus pictus (Otth, 1837)

1900

Reptilia Trachemys scripta (Schoepf, 1792)

1983

Mauremys leprosa (Schweigger, 1812)

Authoct.

1990s

Galań (1999) 1,3

1990s

Ayres and Garcıá (2006)

Mammalia Neovison vison (Schreber, 1777)

1958

Bravo and Bueno (1992)

1,2,3,4

1960

Vidal-Figueroa and Delibes (1987)

Myocastor coypus (Molina, 1970 782)

NR

Saint-Girons (1973)

1

Ondatra zibethicus (Linnaeus, 1766)

2004

NR

Elosegui (2003)

1

Azolla filiculoides Lam.

1920

Pereira et al. (2001) Romero-Bujań et al. (2004)

1,2,3

1995

Moreira et al. (2005)

1,2,3

Eichhornia crassipes (Mart.)

Egeria densa Planch.

1939

1990

Elodea canadensis Michx.

1910

I

2008**

Press note (2009). C.H. Minõ-Sil

\2005

Pulgar and Izco (2005)

NR

Domingues de Almeida and Freitas (2006)

1,2,3


1,2,3

1995

Pistia stratiotes L.

N/I FS

Cirujano et al. (1995)

2006

AT

N/I AT 1,2,3

Heteranthera limosa (SW.) 1995 Willd.

NR

Servia et al. (2006) Rodrı´guez et al. (1995)

3,4

Heteranthera reniformis Ruiz & Pav.

1993

NR

Zaragoza et al. (1993)

3,4

Heteranthera rotundifolia Griseb.

1996

NR


3,4

Myriophilllum aquaticum (Velloso) Verdc.

1936

Salvinia natans (L.) All.

1984

I

AT

N

AT

1971

Domingues de Almeida and Freitas (2006) Laıńz (1971)

AT

2005

Bolo´s and Vigo (1984) Go´mez Vigide et al. (2005)

U

123

3484


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