Changes in Fish Assemblages in Catchments In

Freshwater Biology (2010) 55, 1734–1746 doi:10.1111/j.1365-2427.2010.02407.x

Changes in ﬁsh assemblages in catchments in north-eastern Spain: biodiversity, conservation status and introduced species

ALBERTO MACEDA-VEIGA*, ANTONIO MONLEON-GETINO†, NUNO CAIOLA‡, § FREDERIC CASALS AND ADOLFO DE SOSTOA* *Department of Animal Biology (Vertebrates), University of Barcelona, Spain †Department of Statistics, University of Barcelona, Spain ‡IRTA Aquatic Ecosystems, Spain §Department of Animal Production, University of Lleida, Spain

SUMMARY 1. North-eastern Spain is a hot spot for the introduction of alien fish species, and its native fish fauna is one of the most endangered worldwide. We used an extensive data set from 2002 to 2003 and historical information from the area to characterize fish diversity and establish conservation priorities in river catchments. 2. Diversity indices were used to characterize fish diversity at the basin scale. An index of conservation status was applied for each species, which considers the occurrence, abundance and endemicity of each taxon. We used indirect ordination methods to test the relationship among basin features and to identify those variables most correlated with each other. To identify physical, biotic and environmental characteristics that seem to make a basin particularly susceptible to invasion, we performed a step-wise multiple regression to examine the relationship between the number of native, translocated and introduced fish species (including the original native species richness of each basin), and landscape variables. 3. Over a period of approximately 50 years, the mean range size of native fish species has decreased by 60%. The greatest decline occurred in Gasterosteus gymnurus, Anguilla anguilla and Salaria ﬂuviatilis, for which species over 75% of the original distribution area has been lost. The species with the highest conservation index were Gasterosteus gymnurus and Salaria ﬂuviatilis. 4. Basin area and the catchment type explained 70% of variation in native species richness, whereas the number of dams and basin area accounted for more than 80% of variation in the number of introduced species. 5. The original native species richness and the number of introduced species at basin scale were not related, and thus there was no evidence of ‘‘biotic resistance’’ to invasion. The restoration of natural hydrologic processes and the development of specific management tools to protect native species, such as the prioritization of areas for fish conservation and the eradication of local populations of exotic species, are required to restore native fish fauna in these catchments.

Keywords: conservation, damming, endangered species, ﬁsh diversity, non-indigenous species

Correspondence: Maceda-Veiga, Department of Animal Biology (Vertebrates), University of Barcelona, Spain. E-mail: [email protected]

1734 2010 Blackwell Publishing Ltd Changes in Iberian fish assemblages 1735 Vilizzi, 2005). In some respects, freshwaters can be Introduction considered as ‘‘islands’’ in a sea of land and fresh- Mediterranean streams are among the most endan- water fish are unable to disperse across land and sea gered of ecosystems (Magalha˜es, Ramalho & Collares- (Gido & Brown, 1999). Identifying the factors that Pereira, 2008). The decline of freshwater fish and the make systems more or less invasible has been one of spread of alien species is a complex phenomenon the most important issues in invasion ecology (March- emerging on global, regional and local scales (Apari- etti et al., 2004; Davies et al., 2007a; Fridley et al., 2007). cio et al., 2000; Clavero, Blanco-Garrido & Prenda, From the beginning of the study of ecological inva- 2004; Leprieur et al., 2008). Fish communities are sions (Elton, 1959), many factors have been used to determined by a wide range of physical and biotic predict invasibility in freshwater ecosystems, and the processes and their composition changes over time variables highlighted in most studies are related to and space (Magalha˜es, Batalha & Collares-Pereira, anthropogenic disturbances and the strength of any 2002; Blanchet et al., 2009). A greater understanding of biotic resistance of native communities to invasion the structure of fish communities and the distribution (Fridley et al., 2007; Leprieur et al., 2008; Olden, of species is necessary to establish the conservation Kennard & Pusey, 2008). status of native species, to develop management The decline of freshwater fish species in some strategies and to analyse the spread and introduction Iberian catchments up until 1996 has been assessed, of alien biota (Filipe et al., 2004; Marchetti et al., 2004; although the various hypotheses to explain the Clavero & Garcıá-Berthou, 2006; Magalha˜es et al., decline have not been tested (Aparicio et al., 2000). 2008). In addition, the conservation status of native species The native ichthyofauna of the Iberian Peninsula is in this region has probably declined further as a result dominated by the Cyprinidae and contains few of new alien species and ineffective management; piscivores (Sostoa et al., 1990; Doadrio, 2001). This indeed, aquatic species are usually not considered in fauna is highly adapted to the harsh climatic condi- protected areas (Aparicio et al., 2000; Filipe et al., tions of the region, in which droughts and floods are 2004). common cyclical phenomena (Magalha˜es et al., 2007). Here, we examined the distribution of freshwater Although such climatic features contribute strongly to fish to establish conservation priorities and to identify the structure of assemblages (Magalha˜es et al., 2002), the species that are most threatened. Our main goals habitat destruction and the introduction of alien were (i) to characterize fish diversity between basins; species are now strongly involved and considered (ii) to compare the spatial distribution of alien and the main threats to native biodiversity worldwide native fish; (iii) to analyse the changes in fish assem- (Aarts, Van Den Brink & Nienhuis, 2004; Marchetti blages over time, comparing the distribution in 2002– et al., 2004; Clavero & Garcıá-Berthou, 2005; Leprieur 2003 with the original range of native fish species and et al., 2008; Blanchet et al., 2009). (iv) to identify catchment features (land-use, native The introduction of alien species has social, economic fish diversity, hydrological disturbance, habitat pro- and ecological implications. For instance, biological tection, etc.) associated with the number of native and invasions may be the cause of species extinctions introduced fish species present in each basin. (Clavero & Garcıá-Berthou, 2005), and this phenomenon is particularly worrying in regions with high species richness (of which many are endemic), as is the Methods case in the Iberian Peninsula (Doadrio, 2001). More Study area than 50% of the species in catchments in Catalonia (NE Spain) have been classified as vulnerable, endangered This study was conducted in Catalonia, in the NE of or critically endangered (Doadrio, 2001). Moreover, the Iberian Peninsula, and involved all the rivers this region is considered a ‘‘hot spot’’ for the introduc- between the Muga and Riudecanyes basins (known as tion of alien fish in the Iberian Peninsula. ‘‘inland Catalonian catchments’’ in this region Freshwater fish communities provide excellent because both the source and mouth of these rivers is case-studies for assessing the patterns and conse- in Catalonia), plus parts of the Ebro (Noguera Palla- quences of biological invasions (Copp, Wesley & resa, Noguera Ribagorçana and Segre rivers) and

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Fig. 1 The mainstems of rivers in Catalonia (NE of Iberian Peninsula, Spain) whose catchments were surveyed. Se`nia basins (Fig. 1). Together, the study area covered CPUE) for all freshwater fish species at the 325 nearly 155 000 km2. The Ebro is the second largest sampling sites surveyed between 2002 and 2003. Fish river in the Iberian Peninsula, and has the highest were caught with a portable electrofishing unit which discharge, followed in the case of Catalonia by the generated up to 400 V and 2 A pulsed D.C and the Llobregat and Ter basins. The other Catalonian basins same equipment was operated across sites. Fish sam- are smaller because they rise in a coastal range of pling was based on a single-pass electric fishing mountains and their valleys slope relatively steeply method, and sites were surveyed in the same season down to the sea. Although most of these rivers follow to provide similar hydrologic conditions (mainly low a typical Mediterranean hydrological regime, with flow) within sampling sites (CEN, 2003). The location of highly variable intra- and interannual discharge, there each sampling site within a reach was selected in the are slight differences between large and small basins. field based on accessibility and representativeness, and The former are characterized by main peak flow in attempts were made to include a variety of habitat spring, as a result of snow melt and rain, and a types (pools, riffles and runs). Sampling effort was secondary peak in autumn caused by rainfall. In uniform among sites, a reach length of approximately contrast, small basins have the highest flow in autumn 100 m being fished, and only relatively shallow reaches and very low flow in summer, often being reduced to (<1 m) were selected to allow for efficient electrofish- a series of isolated pools. In addition to natural ing. Our experience indicated that this methodology is fluctuations, starting in the 20th century, the flow of effective at recording common species but may miss a all these basins has been considerably modified as a few rarer species in reaches deeper than those we result of dams and abstractions. surveyed. After capture, fish were identified to species, counted and returned to the river. We derived a second presence ⁄absence data set Data collection based on the historical distribution of native species, We gathered presence ⁄absence data and made esti- using mainly unpublished records of other authors mates of the relative fish density (catch per unit effort, and ourselves. To build this data set, we consulted

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1734–1746 Changes in Iberian fish assemblages 1737 different sources covering the last 50 years (from information was obtained from the Catalonian Water 1960), when many fish assemblages were still pristine Agency database (available at: http://www.gencat. in this area: fish collections (especially from the cat/aca). For climatological and geomorphological University of Barcelona and the Natural History variables and protection status, several landscape Museum of Madrid), the Atlas and Redbook of layers from the ‘‘Department de Medi Ambient i Spanish Freshwater Fishes (Doadrio, 2001), the Ency- Habitatge (2009)’’ (‘‘Generalitat de Catalunya’’ clopedia of Natural History of Catalan Countries (Regional Government)) were combined with the layer (Sostoa, 1990) and a PhD dissertation (Doadrio, 1984), containing all our sampling points using the GIS (Geo- plus our own surveys carried out over the last graphical Information System) software ARCVIEW 30 years. Fish were mainly collected using the same V. 3.5. (Environmental Systems Institute Inc., USA). electrofishing method but many records consisted of Subsequently, we obtained a matrix with our sampling qualitative data on fish abundance or record only the points and the nearest value of each landscape attri- presence of species. Thus, this information could be bute. Moreover, we combined a human population used to establish the distribution of native species but census file provided by the ‘‘Generalitat de Catalu- not for any quantitative assessment of density. All fish nya’’ with our data matrix, to obtain the total number species were considered in the analysis, including of inhabitants of the nearest village (usually) upstream both strictly freshwater and amphidromous species. of each sampling site. An average was then calculated The number of native, exotic and translocated species of all the sampling sites within each basin. For the was recorded for each basin. ‘‘Exotic’’ species are other variables related to human land use, a frequency whose original range did not include any basin on the was calculated for each basin taking account of all its Iberian Peninsula. ‘‘Translocated’’ species are species sampling points. Land use was determined using a that have been introduced into a given catchment in binary variable at each sampling site by observing the which they were not originally found. Both exotic and land-use categories bordering the reach surveyed up translocated species are referred together here as to 500 m from the channel. ‘‘introduced’’ species. The status of species was assigned following the Atlas and Red Book of Spanish Data analysis Freshwater Fish (Doadrio, 2001). Amphidromous species, typical of coastal lagoons, such as Atherina In addition to inferring species richness from the boyeri Risso, 1810 or Aphanius iberus (Valenciennes, number of species in each basin, three indices of alpha

1846), were not included in this analysis. diversity were calculated (Margalef, DMg; Shannon, Information related to basin features was obtained H’; Berger–Parker, d) (Moreno, 2001) to obtain a more from a geographical information system and from complete characterization of the diversity. The Mar- field notes taken during surveys. Fourteen landscape galef index measures the relationship between the attributes characterized the fourteen catchments species richness and the total number of individuals included in the analysis. We examined variables captured. The higher the index, the greater the related to climatology (mean evapotranspiration, diversity. The Shannon index measures the average mm), hydrological alteration (the number of dams degree of uncertainty in predicting the species to and the area of reservoirs in m2), hydrology (flow in which an individual chosen at random from a sample ) m3 s 1 and catchment area in km2), human use (the of N individuals and S species will belong. It consid- proportion of land which is developed, used for ers the relative abundance of each species and is agriculture or well protected for conservation), strongly influenced by the occurrence of rare species. human population (density), geomorphology (mean The Berger–Parker index measures dominance by slope % and mean altitude, m) and type of basin calculating the ratio between the number of the most (‘‘inland Catalonian catchments’’, Ebro and Se`nia abundant species and the total number of individuals basins). In addition, the original native species rich- in the sample. In addition, we examined the contri- ness of each basin was also recorded. bution of native and introduced species separately to Each of these variables was measured directly at the total diversity index of each basin. each site, except for the number of dams, catchment The frequency of occurrence of each native species area and the surface area of reservoirs, for which was recorded in both our data sets (historical and

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1734–1746 1738 A. Maceda-Veiga et al. 2002–2003) and, thus, both frequencies were (Achondrostoma arcasii Steindachner, 1866), stone compared with a binomial test. We also expressed loach (Barbatula barbatula Linnaeus, 1758), Ebro the change in frequency of occurrence as a percentage barbel (Barbus graellsii Steindachner, 1866), Redtail for each native species during the period studied. An barbel (B. haasi Mertens, 1925), Mediterranean barbel ‘‘index of conservation’’ was calculated, to establish (B. meridionalis Risso, 1827), Ebro nase (Parachondros- the conservation value of each taxon. Following Filipe toma miegii Steindachner, 1866), colmilleja (Cobitis et al. (2004), to calculate the relative conservation paludica de Buen, 1930), Western threespined stickle- value of each species, we used data on the frequency back (Gasterosteus gymnurus Cuvier, 1829), Iberian of occurrence and the total number of captured gudgeon (Gobio lozanoi Doadrio and Madeira, 2004), individuals based on surveys carried out in 2002– European minnow (Phoxinus phoxinus Linnaeus, 1758), 2003. We also evaluated the degree of endemism of river blenny (Salaria fluviatilis Asso, 1801), brown trout the species captured, assuming that the aggregation of (Salmo trutta Linnaeus, 1758) and Catalan chub (Squa- these three criteria is a better measure of the conser- lius laietanus Doadrio, Kottelat and de Sostoa, 2007). vation value of a species than its occurrence alone. There were six amphidromous species: Atlantic stur- Finally, we used indirect ordination methods (PCA) geon (Acipenser sturio Linnaeus, 1758), allis shad (Alosa to describe the main sources of variation and relation- alosa Linnaeus, 1758), twaite shad (A. fallax Lace´pe`pe, ships among the basin features. The most intercorre- 1803), thinlip mullet (Liza ramada Risso, 1827), striped lated (r > 0.7) variables relating to basin features were mullet (Mugil cephalus Linnaeus, 1758) and European omitted from further analysis (using Pearson’s or eel (Anguilla anguilla Linnaeus, 1758). All these 19 Spearman’s tests according to data normality). All species were found in the 2002–2003 surveys, except variables followed a normal distribution, according to the two species of Alosa, A. sturio and the freshwater Kolmogorov–Smirnov test, with the exception of the species A. arcasii and C. paludica. Fourteen alien spe- number of dams, mean evapotranspiration and the cies were found: bleak (Alburnus alburnus Linnaeus, categorical variable type of catchment. To improve 1758), black bullhead (Ameiurus melas Rafinesque, normality, we applied log-transformation to reservoir 1820), goldfish (Carassius auratus Linnaeus, 1758), carp area, water flow, catchment area and mean evapotrans- (Cyprinus carpio Linnaeus, 1758), pike (Esox lucius piration, and square root transformation to the number Linnaeus, 1758), Eastern mosquitofish (Gambusia hol- of dams. We then performed a multiple regression brooki Girard, 1859), pumpkinseed (Lepomis gibbosus analysis to examine the relationship between basin Linnaeus, 1758), largemouth bass (Micropterus salmo- featuresselectedinpreviousanalysesandthenumberof ides Lacepe`de, 1802), rainbow trout (Oncorhynchus native and introduced species, including translocated mykiss Walbaum, 1792), pseudorasbora (Pseudorasbora species or not. To carry out the multiple linear regres- parva Temminck & Schlegel, 1846), roach (Rutilus sion, we chose the best combination of predictor rutilus Linnaeus, 1758), pikeperch (Sander lucioperca variables with step-wise selection, with a probability Linnaeus, 1758), rudd (Scardinius erythrophthalmus of entry of 0.05 and a probability of removal of 0.10. To Linnaeus, 1758) and European catfish (Silurus evaluate the models, the variables introduced were glanis Linnaeus, 1758). checked for colinearity by means of a Durbin-Watson The Shannon and Margalef indices showed that the test and the distribution of residuals was tested for highest diversity of native species was in the Ebro normality. All analyses were performed with SPSS for (Table 1). The opposite was true of the smaller basins Windows V.15., except for diversity analysis, for which (Riudecanyes, Riudaura and Foix), which had the the PAST was used (Hammer, Harper & Ryan, 2001). lowest indices of richness and evenness and where Significance was accepted at P < 0.05 in all analyses. only one native species was recorded. We also found that, after the Ebro, the most northerly and the largest basins (Muga, Tordera and Fluvia`) had the highest Results Shannon and Margalef indices, thus indicating the high abundance and species richness of fish, partic- Diversity and species richness ularly in the Muga and Fluvia`. Nineteen species of native fish were recorded, The highest species richness and Margalef index of including 13 strictly freshwater species: bermejuela introduced (including translocated) species was also

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1734–1746 Changes in Iberian ﬁsh assemblages 1739 )

Table 1 Species richness and of Margalef (DMg), Shannon (H’) Z and Berger-Parker (d) diversity indices, including native and introduced species in each basin ranked according its surface

area < 0.05) are P 2.54** 2.73** 1.23

Introduced 02–2003 surveys ) ) ) Native species species ) Binomial test (

Surface % 2 differences ( Basin (km )SDMg H’ dSDMg H’ d

Riudecanyes 31 1 0.00 0.00 1.00 1 0.00 0.00 1.00 52.0575.0063.51 3.96** 4.86** 12.21** 89.58 6.35** 53.7338.97 6.34** 4.47** 23.08 0.92 Ridaura 42 1 0.00 0.00 1.00 0 0.00 0.00 0.00 77.36 20.56** ) ) ) ) ) ) Changes in the frequency of occurrence ( ) ) Se`nia 198 3 0.28 0.81 0.57 1 0.00 0.00 1.00 Foix 312 1 0.00 0.00 1.00 1 0.00 0.00 1.00 Daro´ 320 3 0.24 0.84 0.67 0 0.00 0.00 0.00 Gaia` 424 2 0.11 0.69 0.52 0 0.00 0.00 0.00 Francolı´ 838 3 0.21 0.75 0.72 3 0.25 0.79 0.63 Muga 854 5 0.33 1.20 0.39 9 0.78 1.61 0.44 Tordera 894 4 0.32 0.96 0.64 4 0.35 0.71 0.71 Fluvia` 974 6 0.43 0.84 0.74 6 0.46 0.30 0.94 Frequency of occurrence in 2002–2003 surveys Beso`s 1039 2 0.09 0.36 0.88 6 0.48 1.17 0.57 Ter 2690 4 0.24 0.49 0.86 8 0.57 1.48 0.45 Llobregat 4948 3 0.19 0.52 0.83 10 0.81 1.75 0.36 Ebro 85550 11 0.77 2.12 0.20 12 1.03 1.22 0.62 Number of basins present in 2002–2003 found in the Ebro basin. However, the Llobregat, Muga and Ter basins had the highest values for the Shannon index. Although the Ebro had the largest number of introduced species, some were scarce and Original frequency of occurrence this downweighted the Shannon index. Note that all species classiﬁed as ‘‘translocated’’ are actually native to the Ebro, and most exotic species were also found in this basin. In general terms, however, the diversity analysis showed that richness and evenness indices Original number of basins present for introduced species were higher in basins with lower Margalef and Shannon indices. Thus, though extinctions have not yet been reported, ﬁsh assemblages tended to be dominated by introduced species 23.62 5 0.15 3 0.02 in some catchments (Table 1). Conservation value

Fish distribution and conservation status

All native species have declined greatly in these catchments, with the exception of these which have been translocated: B. graellsii, G. lozanoi, P. phoxinus stickleback River blennyCatalan chubBrown trout 10.89 5.83 4.78 4 11 2 0.14 0.68 0.21 2 9 9 0.04 0.25 0.30 52.94 Ebro nase 8.94 2 0.22 4 0.11 Iberian gudgeonEuropean minnow 8.22 6.65 1 2 0.00 0.08 4 6 0.09 0.15 84.62 – – Mediterranean barbelWestern threespined 5.46 7 0.42 6 0.26 Redtail barbel 8.05 7 0.41 7 0.19 Ebro barbel 7.56 1 0.16 4 0.20 20.75 Stone loach 9.02 1 0.08 2 0.06 and S. trutta (Table 2). Note that P. miegii, despite European eel 5.49 14 0.81 8 0.18 have been introduced into two other basins, showed a decrease in frequency of occurrence. Gasterosteus gymnurus was the native species in the most precar- ious situation, with a decline of almost 90% in its frequency of occurrence. Of particular concern is The proportion of sites at which native freshwater species were found in catchments in Catalonia on the basis of historical distribution and IBICAT 20 another small species S. ﬂuviatilis, which is locally = 325 sampling sites). The change in the frequency of occurrence is expressed as a percentage, and their conservation value is also shown. Statistical n Salaria ﬂuviatilis Squalius laietanus Salmo trutta Parachondrostoma miegii Phoxinus phoxinus Gobio lozanoi Barbus meridionalis Gasterosteus gymnurus Barbus haasi ( Table 2 Barbus graellsii Barbatula barbatula Anguilla anguilla abundant in a few basins. Consequently, these two marked** Species Common names

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Table 3 Frequency of occurrence for non-native ﬁsh species in catchments in Catalonia according to IBICAT surveys (2002–2003)

Number of Frequency of Date of basins present occurrence Species Common name Family introduction in 2002–2003 in 2002–2003

Alburnus alburnus Bleak Cyprinidae 1992 4 0.07 Ameiurus melas Black bullhead Ictaluridae 1910 1 <0.01 Carassius auratus Goldfish Cyprinidae 17th century 3 0.02 Cyprinus carpio Carp Cyprinidae 17th century 8 0.19 Esox lucius Pike Esocidae 1949 1 <0.01 Gambusia holbrooki Eastern mosquitofish Poeciliidae 1920 5 0.03 Lepomis gibbosus Pumpkinseed Centrarchidae 1910 6 0.05 Micropterus salmoides Largemouth bass Centrarchidae 1955 2 0.02 Oncorhynchus mykiss Rainbow trout Salmonidae 19th century 5 0.02 Pseudorasbora parva Pseudorasbora Cyprinidae 2001 1 <0.01 Rutilus rutilus Roach Cyprinidae 1910 1 0.01 Sander lucioperca Pikeperch Percidae 1975 1 0.01 Scardinius erythophthalmus Rudd Cyprinidae 1910 3 0.06 Silurus glanis European catfish Siluridae 1974 1 0.02

species had the highest conservation value. Amphidr- suffered other stresses, such as a high degree of omous species were also found to be endangered, and development or agriculture. The second PCA axis the range of A. anguilla has decreased by more than distinguished between basins with a high ratio of 75%. Mugillid species were not included in this surface area of reservoirs per catchment area and analysis because they have natural restricted ranges basins with high evapotranspiration. The PCA results and the conservation value could be overestimated summarized the correlation between variables. The and misinterpreted. Hence, the conservation value of strongest correlations (r > 0.70) were between vari- translocated species must be interpreted with care ables highlighted in the two PCA axes: Altitude – because their native distribution area did not include Water flow, r = 0.71; Altitude – Catchment area, wide areas of Catalonian catchments. r = 0.74; Water flow – Catchment area, r = 0.79; Water In the 2002–2003 surveys, the most widespread flow – Original native richness, r = 0.94; Catchment exotic species was C. carpio followed by another area – Original native richness, r = 0.77; Number of cyprinid (A. alburnus) and two centrarchids (L. gibbo- dams – Altitude, r = 0.72 and Number of dams – sus and M. salmoides) (Table 3). However, other spe- Surface area of reservoirs, r = 0.94. cies were located in only one basin or were restricted in area (A. melas, E. lucius, P. parva, R. rutilus, S. lu- General linear model (GLM) cioperca and S. glanis). Step-wise multiple regression was used to estimate the combination of variables that best predicted the Indirect analysis number of native and introduced species in each The PCA of the combined data set of basin features basin. A GLM was performed with introduced species and species presence explained 39.3 and 20.2% of the (both exotic and translocated) and considering only total variation for the first two axes, respectively exotic species as non-native. Before performing the (Fig. 2). The first PCA axis loaded positively on the analysis, intercorrelated basin attributes were number of dams, total surface area of reservoirs, excluded (r > 0.70). catchment area, flow and the historical number of The linear multiple regression, using the number of native species recorded in each catchment, displaying native species as dependent variable, accounted for mainly a gradient based on catchment area, from the 70% of variation (R2 = 0.70), and the variables largest with the highest discharge (Ebro) to the selected by the model were catchment size and type smallest with intermittent flow (‘‘inland Catalonian of catchment (B, slope = 2.27, P < 0.05; B = 2.81, catchments’’ and Se`nia basin). These basins also P < 0.05; respectively). As for native species, the

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1734–1746 Changes in Iberian ﬁsh assemblages 1741

Fig. 2 Principal component analysis of basin features. Top, factor loadings of the variables: ELE (average elevation), GLS (average gradient slope), AGR (agriculture), FOR (proportion of forest land), DEV (proportion of developed land), POP (number of inhabitants in the nearest village), PRO (proportion of protected land), BSH (catchment type), DAM (number of dams per catchment), RES (reservoir area), FLO (average water flow), BAS (catchment area), RAT (ratio between reservoir and catchment area), DIV (original native fish diversity) and EVA (average annual evapotranspiration). Bottom, basin scores for the first two principal components.

model showed a strong relationship between the (being close to 2 in the first two models). Thus, there number of exotic species and the catchment area was no evidence of positive serial correlation, and (B = 1.57; P < 0.05); however, in this case, the number residuals fitted a normal distribution (Kolmogorov- of dams was also significant, accounting for 81% of Smirnov test P > 0.05). variation (R2 = 0.81; B = 2.22; P < 0.05). However, Although the original number of native fish in each when introduced species were considered, 73% of basin was not included in the model (since it was the variation was accounted for and only catchment highly correlated with basin surface area), a univar- area was selected by the model (B = 4.78; P < 0.05). iate regression analysis was performed between the The Durbin–Watson test was over 1.5 in all cases number of introduced fish species and the original

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14 islands, should harbour a greater number of species

12 than smaller ones (Elton, 1959; McArthur & Wilson, 2001). 10 The positive relationship found between the histor-

8 ical native species richness in each basin and the present non-native ﬁsh richness suggested that all 6 communities are susceptible to invasion by intro- 4 duced species, regardless of the original native species

Introduced fish richness 2 diversity (Marchetti et al., 2004; Harrison et al., 2006). Our finding is consistent with other macroecological 0 studies and recent theoretical and empirical studies –2 (Davies et al., 2007a; Leprieur et al., 2008; Blanchet 02468 1012141618 et al., 2009). However, studies carried out at finer Original native fish richness scales tended to document negative relationships Fig. 3. Linear regression between the original native species between the original number of native present and richness of each basin and the number of exotic species (filled the number of exotic species that the system has now 2 circles, R = 0.75; Slope = 0.85; P < 0.001). The regression for (Knops et al., 1999; Fridley et al., 2007). translocated species (open circles) was not significant (R2 = 0.03; Slope = 0.08; P = 0.55). It may be that ecological communities are rarely saturated with species and therefore that there are key factors other than species richness that determine native species richness in the basin (Fig. 3). A signif- susceptibility to invasion. These include the number icant positive relationship was found between the of attempts at colonization, the characteristics of the number of exotic species and the original number of invasive species and aspects of the environment (Gido native species. In contrast, when only translocated & Brown, 1999; Davies et al., 2005; Duggan, Rixon & species were considered in the analysis, a non-signif- MacIsaac, 2006; Belote et al., 2008). Species rich com- icant relationship was found between the original munities occur where habitat heterogeneity is high. number of native fish in each basin and the number of Thus, alien species are more likely to find suitable translocated species. In addition, univariate regres- habitats in more heterogeneous areas (Davies et al., sion analyses revealed that there was a weak signif- 2005; Richardson & Pysek, 2006). These factors can icant positive relationship among the number of covary among themselves and they may mask the basins colonized by exotic species (R2 = 0.26; effect of native species richness on susceptibility to B = 0.01; P < 0.05) or their frequencies of occurrence invasion (Gilbert & Lechowicz, 2005; Fridley et al., (R2 = 0.25; B = 0.00; P < 0.05) and the time spent since 2007). Thus, the question is not whether diversity is their introduction. important, but how important it is relative to the other factors (Stachowicz et al., 2002a). It is clear that the same conditions that promote high diversity of native Discussion species also support diverse of alien species (Stohl- The native fish assemblages of the Iberian Peninsula gren et al., 2006). have only a low to moderate species richness when The native fish fauna of catchments in Catalonia, as compared, for instance, to the tropics. Our study in freshwater ecosystems throughout the world, has confirms that the largest basins of the Iberian Penin- decreased a mean of 60% in recent decades, and the sula harbour the greatest native biodiversity of fish situation of certain species is seriously compromised (Clavero et al., 2004). However, these basins also have (Elvira, 1995; Aparicio et al., 2000; Doadrio, 2001; the largest number of introduced species, while the Leonardos et al., 2008). Nevertheless, extinctions have smallest basins have largely maintained pristine fish not yet been reported. The ichthyofauna of most communities (Aparicio et al., 2000; Clavero et al., northern basins in Catalonia and the Ebro have a good 2004). This agrees with the postulates of invasion conservation status (high native species richness and ecology and the theory of island biogeography, which abundance) but there are also hot spots of introduced would predict that larger basins, as with true oceanic species. Among all native freshwater fish in Catalonia,

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1734–1746 Changes in Iberian fish assemblages 1743 G. gymnurus and S. fluviatilis are the species with the Exotic species have increased their range since highest conservation value. Special attention should 2002–2003 (Aparicio et al., 2000). Non-native fish make also be paid to amphidromous species (A. sturio, up 54% of the ichthyofauna of Catalonia, higher than A. anguilla and Alosa spp., for example) and the other European countries such as Italy (48%), France freshwater species A. arcasii, which have suffered (44%) and Flanders (35%) (Copp et al., 2005). Unfor- local extinctions despite having a wide overall distri- tunately, this percentage is expected to increase bution (Aparicio et al., 2000; Doadrio, 2001). Note that further since new introductions have been reported the range of A. anguilla has declined by over 75% in in Spain but also throughout of Europe since 2003 Catalonia but is also in decline throughout Europe (Gisbert & Lo´pez, 2007; Benejam et al., 2008; Franch (Helfman, 2007; Leonardos et al., 2008). Therefore, we et al., 2008; Maceda-Veiga et al., 2009; Tockner, recommend that the legal conservation status of Robinson & Uehlinger, 2009). In general, southern native fish in the Iberian Peninsula be reviewed. Europe and the Mediterranean harbour a greater Furthermore, aquatic habitats need to be restored and proportion of introduced fishes (Verreycken et al., protected to enhance the survival of native fish fauna 2007). and other less studied aquatic organisms (Moyle, The first species to be introduced do not always 1995; Aparicio et al., 2000; Filipe et al., 2004; Maceda- have the widest distribution range (Clavero & Garcia- Veiga et al., 2009). Berthou, 2006). For instance, C. carpio and L. gibbosus Habitat restoration practices should also guarantee were introduced in the 17th century and in 1910 river connectivity. As physical barriers to fish move- (Elvira, 1995), respectively, and these species do have ment, dams are the major cause of the decline of the widest range in Catalonia. However, other species migratory species (Aarts et al., 2004; Humphries et al., introduced around the same time, such as A. melas, 2008). River connectivity should be enhanced through C. auratus and S. erythrophthalmus, have a more the construction of fish passes around or through restricted distribution. As stated previously, patterns physical barriers such as dams or weirs (Lo´pez et al., of species invasions may vary over time in response to 2007). However, if this measure cannot be imple- natural and human-related factors of introduction, mented, periodic moderate-to-high flows should be establishment and dispersal across landscape (Gido & guaranteed (Humphries et al., 2008). More efficient use Brown, 1999; Olden & Rooney, 2006). of water is also required in the Mediterranean area to Besides exotic species, the translocation of native reduce the need for more dams, or new connections species has profound effects on recipient ecosystems among basins, and also to maintain natural flows. (Gregersen et al., 2006; Museth et al., 2007). This Dams are also linked to the introduction of alien practice has been unusual in Spain (Elvira & species, providing extensive areas of lenthic habitat Almodo´var, 2001). Nevertheless it is increasing, at (otherwise scarce in the Mediterranean) (Ruiz, 1998; least in Catalonia, where native fish translocations Clavero et al., 2004). In particular, the fish introduced accounted for up to 50% of fish introductions in the to Spain are mainly limnophilic species (S. glanis, Fluvia` and Llobregat basins. The usual pathway for S. lucioperca and A. alburnus, among others) (Elvira, the translocation of native species (artificial connec- 1995; Elvira & Almodo´var, 2001). Habitat alteration tions among river basins) does not yet exist in our tends to begin long before exotic species are intro- catchments (Elvira & Almodo´var, 2001). Angling is duced (Light & Marchetti, 2007). Small rivers which considered the main pathway of fish introductions in still have typical Mediterranean characteristics (high Spain. The exceptions are G. holbrooki, introduced to evapotranspiration and cyclical periods of drought control mosquitoes, and P. parva, that escaped from and floods) usually have the most pristine fish an ornamental aquaculture facility (Elvira & communities. Native species may be more competi- Almodo´var, 2001; Caiola & Sostoa, 2002). Therefore, tive in rivers with an undisturbed hydrological regime we expected that, as for exotic species, native (Oliva-Paterna, Minãno & Torralva, 2004). Natural translocations are mainly to satisfy the demand from flow regimes can hinder the establishment of non- anglers for bait or as forage species for predatory native fish, and the success of non-native species may sport fishes, such as M. salmoides, S. lucioperca and be reversed if such regimes are restored (Marchetti & E. lucius (Elvira & Almodo´var, 2001; Hesthagen & Moyle, 2000). Sandlund, 2007).

2010 Blackwell Publishing Ltd, Freshwater Biology, 55, 1734–1746 1744 A. Maceda-Veiga et al. The study of invasion biology is complex and it is uncertain native status of fish. Hydrobiologia, 603, 197– difficult to find a common pattern that explains the 210. reason of all invasions. Further research is needed at Blanchet S., Leprieur F., Beauchard O., Staes J., Oberdorff global, regional and local scales to elucidate the T. & Brosse S. (2009) Broad-scale determinants of non- invasion patterns. Our study has limitations that native fish species richness are context-dependent. Proceedings of the Royal Society B: Biological Sciences, 276, must be considerated. For instance, failed introduc- 2385–2394. tions were not usually recorded and, thus, the Caiola N. & Sostoa A.d. (2002) First record of the Asiatic number of introduced species may be biased. In cyprinid Pseudorasbora parva in the Iberian Peninsula. addition, the trend towards richer native communi- Journal of Fish biology, 61, 1058–1060. ties receiving more introduced species could be CEN (2003) Water Quality – Sampling of Fish with misinterpreted. After invasion, species richness goes Electricity. European standard – EN 14011:2003. Euro- up temporarily and may decrease when the dis- pean Committee for Standardization, Brussels, 18 pp. placement of native species is complete. This dis- Clavero M. & Garcia-Berthou E. (2006) Homogenization placement does not affect all native species equally. dynamics and introduction routes of invasive fresh- The species with the most restricted distribution area water fish in the Iberian Peninsula. Ecological Applica- will be the most endangered but exotic species may tions, 16, 2313–2324. not necessarily lead to the extinction of many native Clavero M. & Garcıá-Berthou E. (2005) Invasive species are a leading cause of animal extinction. Trends in Ecology and species. Nevertheless, although extinctions have not Evolution, 20, 110. yet been reported in some regions, they could Clavero M., Blanco-Garrido F. & Prenda J. (2004) Fish become evident in the near future because faunal fauna in Iberian Mediterranean river basins: biodiver- replacement is a slow process. sity, introduced species and damming impacts. Aquatic Conservation: Marine and Freshwater Ecosystems, 14, 575– Acknowledgments 585. Copp G.H., Wesley K.J. & Vilizzi L. (2005) Pathways of We thank D. Vinyoles, C. Franch, P. Riera and ornamental and aquarium fish introductions into S. Sanchez for their assistance in field work and urban ponds of Epping Forest (London, England): database management. We also thank two anony- the human vector. Journal of Applied Ichthyology, 21, mous referees and Professor Dr. Alan Hildrew for 263–274. their effort to improve the original manuscript. We Davies K.F., Chesson P., Harrison S., Inouye B.D., Melbourne B.A. & Rice K.J. (2005) Spatial heterogene- dedicate this work to Sergio who, unfortunately, is not ity explains the scale dependence of the native-exotic with us anymore. diversity relationship. Ecology, 86, 1602–1610. Davies K.F., Harrison S., Safford H.D. & Viers J.H. (2007a) References Productivity alters the scale dependence of the diversity-invasibility relationship. Ecology, 88, 1940– Aarts B.G.W., Van Den Brink F.W.B. & Nienhuis P.H. 1947. (2004) Habitat loss as the main cause of the slow Departament de Medi Ambient i Habitatge (2009) Gen- recovery of fish faunas of regulated large rivers in eralitat de Catalunya. Servei de mapes. Available at: Europe: the transversal floodplain gradient. River http://mediambient.gencat.cat/cat/el_departament/ Research and Applications, 20, 3–23. cartografia/inici.jsp Aparicio E., Vargas M.J., Ruiz-Olmo J. & De Sostoa A. Doadrio I.. (1984) Relaciones filogene´ticas y biogeogra´f- (2000) Decline of native freshwater fihes in a mediter- icas de los barbos (Barbus, Cyprinidae) de la Penıńsula ranean watershed on the Iberian Peninsula. Environ- Ibe´rica y aportes corolo´gicos y biogeogra´ficos a su mental Biology of Fishes, 59, 11–19. ictiofauna continental. Ph. D. Dissertation, Universi- Belote R.T., Jones R.H., Hood S.M. & Wender B.W. (2008) dad Complutense de Madrid, Madrid, Spain. Diversity-invasibility across an experimental distur- Doadrio I. (2001) Atlas y libro rojo de los peces continentales bance gradient in Appalachian forests. Ecology, 89, de Espanã. Direccioń General de Conservaciońdela 183–192. Naturaleza. Ministerio de Medio Ambiente, Madrid. Benejam L., Aparicio E., Vargas M., Vila-Gispert A. & 364 pp. Garcıá-Berthou E. (2008) Assessing fish metrics and Duggan I.C., Rixon C.A.M. & MacIsaac H.J. (2006) biotic indices in a Mediterranean stream: effects of Popularity and propagule pressure: determinants of

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