Journal of Fish Biology (2016) doi:10.1111/jfb.13014, available online at wileyonlinelibrary.com Invasion status of the common carp Cyprinus carpio in inland waters of Argentina T. Maiztegui*, C. R. M. Baigún†‡, J. R. Garcia de Souza*, P. Minotti‡ and D. C. Colautti*§ *Instituto de Limnología ‘Dr. Raúl A. Ringuelet’ (ILPLA) (UNLP-CONICET), Boulevard 120 y 62, CC 712, La Plata, Provincia de Buenos Aires, Argentina, †Instituto Tecnológico Chascomús IIB-(INTECH) (UNSAM-CONICET), Av. Intendente Marino, km 8,2, CC164, B7130IWA Chascomús, Provincia de Buenos Aires, Argentina and ‡Universidad Nacional de San Martín, Instituto de Ingeniería e Investigación Ambiental (3iA UNSAM), Laboratorio de Ecología, Teledetección y Ecoinformática, Campus Miguelete Edificio 3iA, Francia y 25 de Mayo s/n, 1650 Gral. San Martín, Buenos Aires, Argentina This study documents the presence of Cyprinus carpio in 119 natural environments and 49 artificial habitats in Argentina, showing an exponential increment of invaded locations over time since it was introduced in the nineteenth century. Geographic expansion patterns revealed that since its initial intro- duction, species records demonstrate an increment in the central portion of the country only after 1970 and subsequent expansion after 1990 to the north, west and south. Using an environmental similarity index it was determined that more than half the country offers good conditions for C. carpio establish- ment. Environmental factors and anthropogenic impacts are relevant drivers that can account for the current and future distribution of C. carpio in Argentina. © 2016 The Fisheries Society of the British Isles Key words: environmental similarity index; geographic expansion; invasive fish; lakes and reservoirs. INTRODUCTION Biological invasion is a process that involves the arrival of an organism into an environ- ment in which it did not previously exist (Williamson, 1996). The consequences of this process are reflected in the interactions between the invading life form and the native members of the ecosystem (Lodge, 1993; Williamson, 1996). The introduction of a non-native species to an ecosystem exhibits a potential ecological risk if the species is able to establish a self-sustaining population in the new habitat (Gozlan & Newton, 2009), resulting in possible detrimental interactions (Gozlan et al., 2010). Although some successful introductions have not caused negative impacts (Moyle & Light, 1996; Gozlan, 2008), introductions of alien species have often resulted in deleterious ecologi- cal effects on the ecosystem (Crivelli, 1983; Zambrano et al., 1999; Parkos et al., 2003; Kloskowski, 2011). A notable example of this sort of introduction is the global introduction of the common carp Cyprinus carpio L. 1758. This invasive species is considered to be one §Author to whom correspondence should be addressed. Tel.: +54 0221 422 2775; email: colautti@ilpla.edu.ar 1 © 2016 The Fisheries Society of the British Isles 2 T. M A I Z T E G U I E T A L. of the most ecologically harmful freshwater fish (Koehn, 2004; Britton et al., 2010; Kloskowski, 2011) and worldwide it accounts for most of the records of successful establishments (Casal, 2006; Kulhanek et al., 2011). Cyprinus carpio exhibits high physiological tolerance to environmental stress, allowing it to survive in a wide range of abiotic conditions (i.e. temperature, dissolved oxygen, pH and turbidity) (Crivelli, 1983; Koehn, 2004; Zambrano et al., 2006). In addition, C. carpio employs a generalist feeding strategy, capable of exploiting a wide range of food resources such as detritus, macroinvertebrates, zooplankton and plant material (Sibbing, 1988; García-Berthou, 2001). These adaptive life-history traits, together with rapid growth, early maturation and high fecundity (Colautti, 1997; Sivakumaran et al., 2003; Winker et al., 2011) make C. carpio not only a highly successful invader, but also a target species for commercial and aquaculture purposes. For these reasons, C. carpio is one of the most extensively translocated and domesticated species worldwide (Welcomme, 1988; Sivakumaran et al., 2003; Casal, 2006; FAO, 2010). The native distribution of C. carpio covers a wide area ranging from eastern Europe, eastward across Russia and China (Balon, 1995; Zambrano et al., 2006). Due to intro- ductions associated with human activities, however, the species is currently established on every continent, making it the most widely distributed freshwater fish (Sivakumaran et al., 2003; Kloskowski, 2011). Although the worldwide C. carpio distribution has been modelled and predicted by global climatic conditions (Zambrano et al., 2006), local factors based on environmental conditions, catchment morphology and anthro- pogenic effects can also be important and responsible for this species distribution at a local scale. According to Zambrano et al. (2006), the areas climatically suitable for C. carpio colonization in South America encompasses mainly Argentina, southern Brazil and southern Chile, but information about its current distribution and invasion status are still scarce. In Argentina, C. carpio was first introduced in the mid-nineteenth century for orna- mental and aquaculture purposes, and this represents the first recorded introduction of an alien fish in the country (Baigún & Quirós, 1985). In the early and middle 20th cen- tury, C. carpio was also stocked for commercial harvest and sport fishing into several reservoirs of central and northern Argentina (Baigún & Quirós, 1985). The first record of the species in the wild was in 1945 from the Río de la Plata estuary (Mac Donagh, 1945), and the second in 1967 from the same area (Candia et al., 1967). Baigún & Quirós (1985) developed the first C. carpio distribution map, identifying the Colorado River system as the southern boundary of the species distribution (39∘ S). Since then, the number of new reports in Argentina has increased (Liotta, 2005) probably not only as a result of the invasive traits of this species (Koehn, 2004), but also due to multiple direct stocking across the country. For this reason an update of the invasion status of C. carpio is urgently required. The aims of the current study were to update the inva- sion status of C. carpio in Argentina by describing the patterns of occupation over time and to discuss future expansion scenarios based on an assessment of environmental suitability. MATERIALS AND METHODS S T U DY A R E A Argentina is the second largest country in South America, and the eighth largest in the world, extending its American continental surface from subtropical (21∘ S) to subantarctic (55∘ S) © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 I N VA S I O N S TAT U S O F C . C A R P I O I N A R G E N T I NA 3 25° S 35° S 45° S 55° S 75° W 65° W 55° W 0 250 km 600 7 3 2 1 98 7 7 5 10 4 7 6 7 7 7 Fig. 1. Hydrographic regions of Argentina (Subsecretaría de Recursos Hídricos, 2010). , Atlantic drainage: 1, Uruguay River system; 2, Paraná River system; 3, Paraguay River system; 4, Río de la Plata River system; 5, Colorado River system; 6, Patagonic River system; , Endorheic catchments: 7, Independent systems; 8, Serrano systems; 9, Mar Chiquita systems; 10, Pampeano systems; , Pacific drainage. regions, encompassing wide ranges in both latitude and altitude. The Andes Mountains along the western border of the country are responsible for remarkable orographic effects over precipita- tion on a west to east gradient, particularly in the southern area (Patagonia). Climatic variability, in addition to topographic differences, has created a diverse mixture of ecoregions, ranging from regions of high to low rainfall (Burkart et al., 1999; Morello et al., 2012). This gradient promotes the existence of different natural and artificial aquatic systems portrayed by a wide array of lake types that differ according to their origin, size, shape, chemistry and edaphic characteristics (Drago & Quirós, 1996). Within this heterogeneous landscape, three main hydrographic drainages encompassing dif- ferent river systems can be identified (Subsecretaría de Recursos Hídricos, 2010) (Fig. 1): (1) The Atlantic Drainage, which at its upper portion encompasses the Uruguay River system, two large floodplain rivers, the Paraná and Paraguay River systems, and the Río de la Plata River sys- tem. Its southern portion contains extended rivers that drain the Andes Mountains, crossing the Patagonic plateau and flowing into the ocean, including the Colorado and the Patagonic River systems, (2) The endorheic catchments, comprising the Independent Systems, spread along the country, and the Serrano, the Mar Chiquita and the Pampeano systems in the central portion of Argentina and (3) The Pacific Drainage, including short rivers draining from Andean Mountain lakes located in the west Patagonic border (Fig. 1). © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 4 T. M A I Z T E G U I E T A L. DATA C O L L E C T I O N A N D H I S T O R I C A L A NA LY S I S A review of literature encompassing around 450 documents, including scientific publications, PhD theses, books, official reports and conference presentations was used to determine C. carpio occurrences across the country. Also, local fishery management authorities and stakeholders were consulted on the presence of C. carpio. In addition, to find more records of water bodies invaded by the species an internet search was made. Cyprinus carpio records were numbered and their location, geographic position, data source and year of publication were also identified. Environments with C. carpio records were classified as natural (lakes and rivers) or artificial (reservoirs and canals). In those environments with multiple records of C. carpio presence, only the oldest citation for each location was considered for the study. The cumulative number of invaded locations through decades was calculated and a regression model was fitted to the data-set to determine invasion rate. The cumulative records of C. carpio were mapped for the Argentine territory, considering hydrographic systems and natural or artificial environments for three different time periods since the first citation until present, to elucidate both temporal and geographical invasion patterns. Record mapping was accomplished using Mapinfo Professional 6.5 GIS software (www.mapinfo.com). E N V I RO N M E N TA L M O D E L L I N G A niche distribution model was developed based on the environmental conditions correspond- ing to species records in the natural habitats. This approach represents a scenopoetic and Grin- nellian niche (Soberón, 2007), as it only takes into account physical environmental factors in the landscape at regional scales and the choice of predictor variables is of particular impor- tance when developing niche models (Araujo & Guisan, 2006). The following variables Xi were selected for modelling: (1) temperature: annual mean X1, minimum of the coldest month X2 and maximum of the hottest month X3; (2) annual precipitation X4, which was used as proxy for freshwater availability and permanence in water bodies; (3) elevation X5; (4) slope X6. The last two variables were also included because they have been historically used to describe the distribution of freshwater fishes as they relate to river’s order, flow, water velocity and habitat availability (Huet, 1959; Illies & Botosaneanu, 1963; Lasne et al., 2007). Temperature (∘ C) and precipitation (mm) were obtained from WorldClim 1 km cell size cur- rent climate grid databases (Hijmans et al., 2005). Elevation (m a.s.l.; Shuttle Radar Topographic Mission (SRTM) grids 90 m cell size) was obtained from International Centre for Tropical Agri- culture (CIAT) (Jarvis et al., 2008). Slope (degrees× 104) was derived from the SRTM elevation grids, and median elevation and slope grids were calculated to match the 1 km cell size of climate grids. All geographic data were processed with ArcGIS Desktop 10.1 (www.esri.com). Taking into account the entire environmental data set from those locations already invaded by C. carpio, the distribution of values for each variable (X) was divided according to 20, 40, 60, 80 and 100th percentiles (Q(X) i for i= 1, 2, 3, 4, 5). Given that the number of locations within each Q(X) i is the same, but the range of values within each percentile is different as it depends on the distribution of the focal variable, the number of C. carpio locations at each quantile (N) were divided by the range of the corresponding quantile (R(X) i ) to obtain a score V (X) i : V (X) i = NR−1 i . The V (X) i scores where then expressed relative to the maximum S(X) i , ranging from 0 to 1. To assess the similarity of the different areas of the entire country with the ones invaded by C. carpio, the values of each environmental variable considered were obtained for the whole Argentina territory on a cell by cell basis, following the procedures described for the invaded locations. Each cell was qualified according to the S matrix or considering S(X) = 0 if the environmental variable for the cell fell out of the range of values where C. carpio is present in natural environments. Finally, an environmental similarity index (IES) was calculated for each cell (j) as the sum of all S(X) i on the corresponding cell and plotted for the whole country: IES j = n−1 ΣS(X). IES ranges from 0 to 1, with high values being indicative of zones with better environmental conditions for C. carpio establishment in Argentina, due to their similarity with natural areas already invaded by the species. © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 I N VA S I O N S TAT U S O F C . C A R P I O I N A R G E N T I NA 5 160 140 120 100 80 60 40 20 0 19 20 19 30 19 40 19 50 19 60 19 70 19 80 19 90 20 00 20 10 C um ul at iv e nu m be r of in va de d lo ca tio ns Decade Fig. 2. Cumulative number of locations invaded by Cyprinus carpio across decades ( ) and the exponential model fitted to dataset ( ; y= 0·383e0·6372x). RESULTS DATA C O L L E C T I O N A N D H I S T O R I C A L A NA LY S I S The total number of confirmed locations invaded by C. carpio was 168 (Table S1, Supporting Information), encompassing 119 natural environments (47·1% lakes and 52·9% rivers) and 49 artificial habitats (89·8% reservoirs and 10·2% canals). The C. carpio locality records, grouped by decade (D) since their first introduction grew exponentially according the following model: number of invaded records, NIR = 0·383 e 0·6372D (r2 = 0·96; Fig. 2). Geographic distribution of C. carpio records over time shows that until 1970 [Fig. 3(a)], the species records were scarce and restricted mainly to the central portion of the country. From 1970 to 1990 [Fig. 3(b)], a noticeable increment occurred in the number of invaded locations, reflecting a geographic expansion. Finally, between 1990 and present, the number of occupied sites almost doubled, expanding the distribution even more to the north, west and south of Argentina. The records of invaded natural environments were located mainly in the central-east portion of the country, whereas the ones corresponding to artificial environments were mainly distributed in the west, central and north-west portions where C. carpio is almost absent in natural environ- ments. Overall, these results indicated that C. carpio has occupied nearly all the river systems of Argentina with the exception of independent systems of the endorheic catchments and the Pacific drainage [Fig. 3(c)]. E N V I RO N M E N TA L M O D E L L I N G The range of each variable values in each percentile and the variable scores required to build the IES model map are shown in Table I. The map indicates that more than half of the continental area of the country has environmental conditions similar to those natural environments already invaded by C. carpio (Fig. 4). The highest values of IES are located in the central-east area of the country, surrounded by intermediate values in all directions. In the north and central portions of these intermediate IES areas C. carpio © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 6 T. M A I Z T E G U I E T A L. (a ) (b ) (c ) 25 ° S 35 ° S 55 ° W 65 ° W 55 ° W 65 ° W 55 ° W 65 ° W Fi g. 3. C um ul at iv e nu m be r of lo ca tio ns in va de d by C yp ri nu s ca rp io :( a) be fo re 19 70 ,( b) un til 19 90 an d (c ) un til 20 14 . ,a rt ifi ci al w at er bo di es ; ,n at ur al w at er bo di es . © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 I N VA S I O N S TAT U S O F C . C A R P I O I N A R G E N T I NA 7 T ab le I. R an ge of va lu es fo r ea ch va ri ab le (X ) w he re C yp ri nu s ca rp io is pr es en ti n na tu ra le nv ir on m en ts ,b y pe rc en til e (R (X ) i ); sc or e of ea ch va ri ab le fo r ea ch pe rc en til e (V (X ) i ) an d th ei r re la tiv es va lu es to th e m ax im um va lu e (S (X ) i ) V ar ia bl e X R ,V an d S Q 1 Q 2 Q 3 Q 4 Q 5 X 1 :A nn ua lm ea n te m pe ra tu re (∘ C ) R 13 ·8 0 – 15 ·1 9 15 ·2 0 – 15 ·5 9 15 ·6 0 – 16 ·0 9 16 ·1 0 – 16 ·8 9 16 ·9 0 – 21 ·6 0 V 2· 40 8· 40 6· 72 4· 20 0· 71 S 0· 29 1· 00 0· 80 0· 50 0· 09 X 2 :M in im um of th e co ld es tm on th (∘ C ) R − 10 ·0 0 – 2· 09 2· 10 – 3· 79 3· 80 – 4· 39 4· 40 – 5· 73 5· 74 – 10 ·8 0 V 1· 08 1· 98 5· 60 2· 51 0· 66 S 0· 19 0· 35 1· 00 0· 45 0· 12 X 3 :M ax im um of th e ho tte st m on th (∘ C ) R 27 ·2 0 – 29 ·1 9 29 ·2 0 – 30 ·3 9 30 ·4 0 – 31 ·2 7 31 ·2 8 – 32 ·0 7 32 ·0 8 – 34 ·3 0 V 1· 68 2· 80 3· 81 4· 20 1· 51 S 0· 40 0· 67 0· 91 1· 00 0· 36 X 4 :A nn ua lp re ci pi ta tio n (m m ) R 17 6· 00 – 68 8· 50 68 8· 60 – 83 2· 30 83 2· 40 – 93 8· 70 93 8· 40 – 97 8· 30 97 8· 40 – 17 30 ·0 0 V 0· 07 0· 23 0· 32 0· 85 0· 04 S 0· 08 0· 28 0· 37 1· 00 0· 12 X 5 :E le va tio n (m a. s. l.) R − 9· 00 – 8· 50 8· 60 – 12 ·9 0 13 ·0 0 – 75 ·3 0 75 ·4 0 – 13 4· 50 13 4· 60 – 91 0· 00 V 1· 91 7· 64 0· 54 0· 57 0· 04 S 0· 25 1· 00 0· 07 0· 07 0· 01 X 6 :S lo pe (d eg re es × 10 4 ) R 0 – 11 ·5 0 11 ·6 0 – 19 ·9 0 20 ·0 0 – 31 ·7 0 31 ·8 0 – 80 ·9 0 81 ·0 0 – 55 4· 00 V 2· 90 4· 00 2· 85 0· 68 0· 07 S 0· 72 1· 00 0· 71 0· 17 0· 02 T he ra ng e of X i va lu es co rr es po nd in g to th e hi gh es ts co re s ar e in di ca te d in bo ld . © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 8 T. M A I Z T E G U I E T A L. 30°S 40°S 50°S 0 250 500 km 50°W60°W70°W I ES High: 1 Low: 0 Fig. 4. Environmental similarity index (IES) model map for Cyprinus carpio based on occurrences in natural water bodies. , artificial water bodies; , natural water bodies. has occupied mostly impoundments, meanwhile in the southern portion of this area the species has mainly invaded natural water bodies. On the other hand, the lowest or null IES scores, ergo the most environmentally dissimilar areas to those already invaded by C. carpio, cover an area that encompasses the north-west, the west (high mountainous landscape) and south (Patagonic River system) of Argentina. DISCUSSION This study is the first assessment of temporal and spatial expansion patterns of C. carpio in a South American country contributing to a better understanding of the factors explaining the successful colonization of the species in the south portion of this continent. Originally, after their first introduction, C. carpio exhibited a lag-phase in their spread, but since 1970 it has shown an exponential expansion which predicts an increase of up to 220 new locations by the end of the decade 2010–2020, as indicated © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 I N VA S I O N S TAT U S O F C . C A R P I O I N A R G E N T I NA 9 by simple extrapolation. This trend was related to multiple stocking events together with the self-spread to new areas with suitable conditions. In the last three decades, the spatial distribution of C. carpio has expanded sig- nificantly through Argentina, mainly to the west and south beyond the distribution boundaries described by Baigún & Quirós (1985). This remarkable expansion seems to be associated not only with a high dispersal capability (Jones & Stuart, 2009), but was probably also facilitated by human activities such as construction of impound- ments and by direct stocking. In particular, habitat alterations generated by the building of structures for water management have been identified as facilitators of C. carpio recruitment in other countries (Bice & Zampatti, 2011), providing recruit- ment hot spots for non-native species (Sheehy & Vik, 2010). This situation is in agreement with reservoir development in the Iberian Peninsula, where the species was introduced more than five centuries ago but its expansion and establishment has increased in the last century because of an increase in the construction of dams that have facilitated its spread (Clavero & Villero, 2014). A similar scenario has been found in southern Africa where C. carpio is usually found in most impoundments (Ellender et al., 2014) where they are often the dominant species (Ellender et al., 2010). Dams and reservoirs in south-east Australia have also been shown to favour C. carpio (Koehn, 2014), reinforcing the relevance of reservoirs as key habitats for the species. A possible driver for C. carpio invasions in impoundments may be the low biotic resistance in new impoundments, thereby making them particularly vulnerable to species invasions (Kolar & Lodge, 2000; Shea & Chesson, 2002; Havel & Med- ley, 2006). The conversion of free-flowing rivers to standing waters may therefore ultimately facilitate the development of invasive species populations (Fernando & Holcick, 1991; Johnson et al., 2008; Butler & David, 2010; Clavero & Villero, 2014). This is supported by Gehrke (1997) who found that C. carpio abundance was related to the degree of river regulation. In the case of Argentina, canalisation and weir construction in the Río de la Plata River system appears to have promoted C. carpio expansion, whereas stocking practices in reservoirs located in the Colorado, Serrano and Mar Chiquita systems could have been one of the main causes of C. carpio establishment in these areas. The high number of records in reservoirs in the central-west portion of Argentina reinforces their critical role in the expansion process, particularly in zones where slope and hydrological conditions could limit its self-propagation. Although this study is an update of C. carpio distribution based on the available information, the results could be biased due to unequal ichthyological study efforts across the country. Zambrano et al. (2006) predicted the potential invasive range of C. carpio in South America based on large scale climatic variables and using ecological niche modelling based on the GARP algorithm. According to their model, practically all of Argentina was considered climatically suitable for C. carpio establishment, with the exception of the north-western area of the Paraguay and the central Patagonic River systems. The results obtained in this study, in terms of C. carpio occurrences, indicate that there are areas where the species has not been recorded despite being predicted as environmen- tally suitable by Zambrano et al. (2006). Such mismatch was particularly evident on the western fringe of the country and in the middle and south Patagonic River system, where the species has not been recorded. © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 10 T. M A I Z T E G U I E T A L. When the IES map obtained in this study (IES model, Fig. 4) is compared to that of Zambrano et al. (2006), the results obtained are partially in agreement. The two mod- els indicate that Paraguay River system and the northern portion of both Paraná and Uruguay River systems are suitable zones for C. carpio establishment, but the pres- ence of the species is scarce. These basins have permanent connections with already invaded river systems of Argentina. Therefore, the limited establishment success of C. carpio suggests other environmental variables that have not been considered, could be affecting the species distribution in Argentina. Furthermore, biological variables such as species richness could also be playing an important role and should be incor- porated in the IES model, but currently, such information is not available for most of the locations considered in the analysis. The vulnerability of non-saturated commu- nities to C. carpio invasion was indicated by Hugueny & Paugy (1995). Therefore, the high species richness in the Paraguay, Paraná and Uruguay River systems (López et al., 2002) may be an important factor limiting C. carpio presence when compared to the large number of C. carpio records in the central portion of the country (i.e. Río de la Plata and Pampeano River systems) where species richness is low. Such patterns were also found in Australia where C. carpio dispersion was slower in those rivers containing higher richness and particularly piscivorous species (Koehn, 2004). The IES model identified the central-east region of Argentina, characterized by the presence of numerous shallow lakes, as the most suitable for C. carpio establishment. The expansion of C. carpio in these environments represents an example of natu- ral propagation of the species, a situation that has been taking place since the 1980s (Barla & Iriart, 1987), with this fish currently inhabiting almost all of them. These lakes provide ideal habitats for C. carpio because of optimal climatic and topographic con- ditions, and also because of their eutrophic condition which, according to Kulhanek et al. (2011), represents the most suitable trophic state for C. carpio population devel- opment. Furthermore, the existence of extraordinary rains and floods, together with canalisation for alleviating inundation problems, has led to the connection of most of the sub-basins within the Río de la Plata River system, representing another fea- ture which facilitates fish movement among water bodies in this area (Colautti et al., 2015). In addition, extraordinary flooding events, particularly in 1982 and 1997, could have improved C. carpio reproductive success by generating adequate environments for spawning activity. This assumption is in agreement with the results reported by Bajer & Sorensen (2010) who demonstrated that the success of this species in intercon- nected shallow freshwater environments is attributable, among other features, to their propensity to exploit peripheral unstable shallow areas as spawning/nursery habitats. The Patagonic River system appears to be almost uncolonized by C. carpio with the exception of its northern portion, where the species was introduced in the mid 1980s and currently is a common component of the fish assemblage in main rivers (Colautti, 1997; Sidorkewicj et al., 1998; López et al., 2002; Pascual et al., 2002; Alvear et al., 2007). Several large dams lacking fishways, however, represent major barriers to the dispersal of this fish to western Patagonia. Moreover, the absence of C. carpio in the middle and southern catchments could be linked to the isolation of basins and, probably, to the lack of stocking events in the area. In addition, low lake temperatures (Baigún & Marinone, 1995) could be unsuitable for C. carpio spawning (Sivakumaran et al., 2003). Despite the species never having been recorded in middle and south Patago- nia (Baigún & Ferriz, 2003; Aigo et al., 2008), it is documented that the species has been able to colonize cold-temperate lakes of Canada (McCrimmon, 1968; Scott & © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 I N VA S I O N S TAT U S O F C . C A R P I O I N A R G E N T I NA 11 Crossman, 1973; Chow-Fraser, 1998), located in a similar latitudinal range, but in the northern hemisphere. Natural environments of the Serrano system, north of both the Mar Chiquita system and Colorado River system are almost unoccupied by C. carpio which, however, are present in impoundments mostly because of direct stocking (Baigún & Quirós, 1985; Colautti, 1997). Taking into account these observations, the natural environments of these river systems may not be suitable for C. carpio supported by low values of the IES model. Nevertheless, this condition can drastically change if any river in these regions is impounded, and may favour invasion by C. carpio. In conclusion, the findings of this study support the idea that general climatic, topo- graphic and hydrological factors, together with such anthropogenic impacts as habitat modification and stocking practices, were relevant drivers that can account for the current and future distribution of C. carpio in Argentina. Biological and ecological variables related to fish assemblage composition and trophic state of water bodies could also play an important role, and they need to be better understood for more accurate modelling of inland water vulnerability to C. carpio invasion. Since C. carpio has been identified as one of the world’s worst invasive fish species (Lowe et al., 2000) and its effects on natural environments have been reported in several parts of the world (Zam- brano et al., 1999; Koehn, 2004; Haas et al., 2007; Weber & Brown, 2009; Kloskowski, 2011) further studies are needed to assess its economic and environmental impact in Argentina. The authors would like to thank all of the people and government agencies that provided information and helped with data collection, also to P. Bajer and J. M. Morales for critically reading the manuscript. Scientific Contribution N∘ 985 (ILPLA). Supporting Information Supporting Information may be found in the online version of this paper: Table S1. Records of Cyprinus carpio gathered in this study. References Aigo, J. E., Cussac, V., Peris, S., Ortubay, S., Gómez, S., López, H., Gross, M., Barriga, J. & Battini, M. (2008). Distribution of introduced and native fish in Patagonia (Argentina): patterns and changes in fish assemblages. Reviews in Fish Biology and Fisheries 18, 387–408. Alvear, P. A., Rechencq, M., Macchi, P. J., Alonso, M. F., Lippolt, G. E., Denegri, M. A., Navone, G., Zattara, E. E., García Asorey, M. I. & Vigliano, P. H. (2007). Composición, distribu- ción y relaciones tróficas de la ictiofauna del río Negro, Patagonia Argentina. Ecología Austral 17, 231–246. Araujo, M. B. & Guisan, A. (2006). Five (or so) challenges for species distribution modeling. Journal of Biogeography 33, 1677–1688. Baigún, C. R. M. & Ferriz, R. (2003). Distribution patterns of freshwater fish in Patagonia (Argentina). Organisms Diversity & Evolution 19, 151–159. Baigún, C. R. M. & Marinone, C. (1995). Cold-temperate lakes of South America: do they fit northern hemisphere models? Archive für Hydrobiologie 135, 23–51. Bajer, P. G. & Sorensen, P. W. (2010). Recruitment and abundance of an invasive fish, the com- mon carp, is driven by its propensity to invade and reproduce in basins that experience winter-time hypoxia in interconnected lakes. Biological Invasion 12, 1101–1112. © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 12 T. M A I Z T E G U I E T A L. Balon, E. K. (1995). Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129, 3–48. Barla, M. J. & Iriart, R. (1987). La presencia de la carpa (C. carpio) en la laguna de Chascomús y su significado. Limnobios 2, 685–686. Bice, C. M. & Zampatti, B. P. (2011). Engineered water level management facilitates recruitment of non-native common carp, Cyprinus carpio, in a regulated lowland river. Ecological Engineering 37, 1901–1904. Britton, J. R., Cucherousset, J., Godard, M. J. & Copp, H. (2010). Non-native fishes and climate change: predicting species responses to warming temperatures in a temperate region. Freshwater Biology 55, 1130–1141. Burkart, R., Bárbaro, N. O., Sánchez, R. O. & Gómez, D. A. (1999). Ecoregions of Argentina. Buenos Aires: Administración de Parques Nacionales. Butler, S. E. & David, H. W. (2010). Common carp distribution, movements, and habitat use in a river impounded by multiple low-head dams. Transactions of the American Fisheries Society 139, 1121–1135. Candia, C., Baiz, M. & Cabrera, S. (1967). Sobre la presencia de dos ejemplares de carpa Cypri- nus carpio en la zona de Punta Lara (Río de la Plata). Boletín del Servicio de Hidrografía Naval 4, 341–342. Casal, C. M. V. (2006). Global documentation of fish introductions: the growing crisis and rec- ommendations for action. Biological Invasion 8, 3–11. Clavero, M. & Villero, D. (2014). Historical ecology and invasion biology: long-term distribu- tion changes of introduced freshwater species. BioScience 64, 145–153. Chow-Fraser, P. (1998). A conceptual ecological model to aid restoration of Cootes Paradise Marsh, a degraded coastal wetland of Lake Ontario, Canada. Wetlands Ecology and Man- agement 6, 43–57. Colautti, D. C. (1997). Ecología de la carpa Cyprinus carpio en la cuenca del río Salado Provin- cia de Buenos Aires. PhD Thesis, Universidad Nacional de La Plata, Argentina. Colautti, D. C., Baigún, C. R. M., Llompart, F., Maiztegui, T., Garcia de Souza, J. R., Solimano, P., Balboni, L. & Berasain, G. E. (2015). Fish assemblage of a Pampean shallow lake, a story of instability. Hydrobiologia 752, 175–186. doi: 10.1007/s10750-014-2062-7 Crivelli, A. J. (1983). The destruction of aquatic vegetation by carp. Hydrobiologia 106, 37–41. Drago, E. & Quirós, R. (1996). The hydrochemistry of the inland waters of Argentina: a review. International Journal of Salt Lake Research 4, 315–325. Ellender, B. R., Weyl, O. L. F., Winker, H. & Booth, A. J. (2010). Quantifying annual harvests from South Africa’s largest impoundment. Water SA 36, 45–52. Ellender, B. R., Woodford, D. J., Weyl, O. L. F. & Cowx, I. G. (2014). Managing conflicts arising from fisheries enhancements based on non-native fishes in southern Africa. Journal of Fish Biology 85, 1890–1906. Fernando, C. H. & Holcick, J. (1991). Fish in reservoirs. Internationale Revue der gesamten Hydrobiologie und Hydrographie 76, 149–167. García-Berthou, E. (2001). Size- and depth dependent variation in habitat and diet of the com- mon carp (Cyprinus carpio). Aquatic Sciences 63, 466–476. Gehrke, P. C. (1997). Differences in composition and structure of fish communities associated with flow regulation in New South Wales. In Fish and Rivers in Stress: The NSW Rivers Survey (Harris, J. H. & Gehrke, P. C., eds), pp. 169–200. Cronulla, NSW: NSW Fisheries Office of Conservation & Cooperative Research Centre for Freshwater Ecology. Gozlan, R. E. (2008). Introduction of non native freshwater fish: is it all bad? Fish and Fisheries 9, 106–115. Gozlan, R. E., Britton, J. R., Cowx, I. & Copp, G. H. (2010). Current knowledge on non-native freshwater fish introductions. Journal of Fish Biology 76, 751–786. Gozlan, R. E. & Newton, A. C. (2009). Biological invasions: benefits versus risks. Science 324, 1015–1016. Haas, K., Kohler, U., Diehl, S., Köhler, P., Dietrich, S., Holler, S., Jaensch, A., Niedermaier, M. & Vilsmeier, J. (2007). Influence of fish on habitat choice of water birds: a whole system experiment. Ecology 88, 2915–2925. Havel, J. E. & Medley, K. A. (2006). Biological invasions across spatial scales: intercontinental, regional and local dispersal of cladoceran zooplankton. Biological Invasions 8, 59–73. © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 I N VA S I O N S TAT U S O F C . C A R P I O I N A R G E N T I NA 13 Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978. Huet, M. (1959). Profiles and biology of western European streams as related to fisheries man- agement. Transactions of the American Fisheries Society 88, 155–163. Hugueny, B. & Paugy, D. (1995). Unsaturated fish communities in African rivers. American Naturalist 146, 162–169. Illies, J. & Botosaneanu, L. (1963). Problèmes et méthodes de la classification et de la zona- tion écologique des eaux courantes, considérées surtout du point de vue faunistique. Mitteilung Internationale Vereinigung für Theoretische und Angewandte Limnologie 12, l–157. Jones, M. J. & Stuart, I. G. (2009). Lateral movement of common carp (Cyprinus carpio L.) in a large lowland river and floodplain. Ecology of Freshwater Fish 18, 72–82. Johnson, P. T. J., Olden, J. D. & Vander Zanden, M. J. (2008). Dam invaders: impoundments facilitate biological invasions into freshwaters. Frontiers in Ecology and the Environment 6, 357–363. Kloskowski, J. (2011). Impact of common carp Cyprinus carpio on aquatic communities: direct trophic effects versus habitat deterioration. Fundamental and Applied Limnology 178, 245–255. Koehn, J. D. (2004). Carp (C. carpio) as a powerful invader in Australian waterways. Freshwater Biology 49, 882–894. Koehn, J. D. (2014). The biology, ecology and vulnerability of carp. In Forum Proceedings: Carp Management in Australia – State of Knowledge (Fulton, W. & Hall, K., eds), pp. 10–16. Canberra: Pestsmart Toolkit Publication, Invasive Animals Cooperative Research Centre. Kolar, C. S. & Lodge, D. M. (2000). Freshwater nonindigenous species: interactions with other global changes. In Invasive Species in a Changing World (Mooney, H. A. & Hobbs, R. J., eds), pp. 3–30. Washington, DC: Island Press. Kulhanek, S. A., Leung, B. & Ricciardi, A. (2011). Using ecological niche models to predict the abundance and impact of invasive species: application to the common carp. Ecological Applications 21, 203–213. Lasne, E., Bergerot, B., Lek, S. & Laffaille, P. (2007). Fish zonation and indicator species for the evaluation of the ecological status of rivers: example of the Loire basin (France). River Research and Applications 23, 877–890. Liotta, J. (2005). Distribución geográfica de los peces de aguas continentales de la República Argentina. La Plata: Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata. Lodge, D. M. (1993). Biological invasions: lessons for ecology. Trends in Ecology & Evolution 8, 133–137. López, H. L., Morgan, C. C. & Montenegro, M. J. (2002). Ichthyological ecoregions of Argentina. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata (UNLP). ProBiota, Serie Documentos 1, 1–68. Lowe, S., Browne, M., Boudjelas, S. & Depoorter, M. (2000). 100 of the World’s Worst Inva- sive Alien Species. A Selection from the Global Invasive Species Database. Auckland: The Invasive Species Specialist Group (ISSG), a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN). Mac Donagh, E. J. (1945). Pesca de una "Carpa de espejuelos" en el Río de la Plata. Notas del Museo de la Plata T. X Zoologia 69, 315–324. McCrimmon, H. (1968). Carp in Canada. Bulletin of the Fisheries Research Board of Canada 165. Morello, J., Matteucci, S. D., Rodriguez, A. F. & Silva, M. E. (2012). Ecorregiones y Complejos Ecosistémicos Argentinos. Buenos Aires: Editorial Orientación Gráfica Argentina. Moyle, P. B. & Light, T. (1996). Biological invasions of fresh water: empirical rules and assem- bly theory. Biological Conservation 78, 149–161. Parkos, J. J., Santucci, V. J. & Wahl, D. H. (2003). Effects of adult common carp (Cyprinus carpio) on multiple trophic levels in shallow mesocosms. Canadian Journal of Fisheries and Aquatic Sciences 60, 182–192. © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014 14 T. M A I Z T E G U I E T A L. Pascual, M. A., Macchi, P., Urbanski, J., Marcos, F., Riva Rossi, C., Novara, M. & Dell’Archiprete, P. (2002). Evaluating potential effects of incomplete fish presence- absence data. Biological Invasions 4, 101–113. Scott, W. B. & Crossman, E. J. (1973). Freshwater fishes of Canada. Bulletin of the Fisheries Research Board of Canada 184. Shea, K. & Chesson, P. (2002). Community ecology theory as a framework for biological inva- sions. Trends of Ecology & Evolution 17, 170–176. Sheehy, D. J. & Vik, S. F. (2010). The role of constructed reefs in non-indigenous species intro- ductions and range expansions. Ecological Engineering 36, 1–11. Sibbing, F. A. (1988). Specializations and limitations in the utilization of food resources by the carp, Cyprinus carpio: a study of oral food processing. Environmental Biology of Fishes 22, 161–178. Sidorkewicj, N. S., López Cazorla, A. C., Murphy, K. J., Sabbatini, M. R., Fernandez, O. A. & Domaniewski, J. C. J. (1998). Interaction of common carp with aquatic weeds in Argen- tine drainage channels. Journal of Aquatic Plant Management 36, 5–10. Sivakumaran, K. P., Brown, P., Stoessel, D. & Giles, A. (2003). Maturation and reproductive biology of female wild carp, Cyprinus carpio, in Victoria, Australia. Environmental Biol- ogy of Fishes 68, 321–332. Soberón, J. (2007). Grinnellian and Eltonian niches and geographic distributions of species. Ecology Letters 10, 1115–1123. Weber, M. J. & Brown, M. L. (2009). Effects of common carp on aquatic ecosystems 80 years after “Carp as a dominant”: ecological insights for fisheries management. Reviews in Fisheries Science 17, 524–537. Welcomme, R. L. (1988). International introductions of inland aquatic species. FAO Technical Paper 294, 1–318. Williamson, M. (1996). Biological Invasions. London: Chapman & Hall. Winker, H., Weyl, O. L. F., Booth, A. J. & Ellender, B. R. (2011). Life history and popula- tion dynamics of invasive common carp, Cyprinus carpio, within a large turbid African impoundment. Marine and Freshwater Research 62, 1270. doi: 10.1071/MF11054 Zambrano, L., Perrow, M. R., Macias-Garcia, C. & Aguirre-Hidalgo, V. (1999). Impact of intro- duced carp (Cyprinus carpio) in subtropical shallow ponds in central Mexico. Journal of Aquatic Ecosystem Stress and Recovery 6, 281–288. Zambrano, L., Martínez-Meyer, E., Menezes, N. & Townsend Peterson, A. (2006). Invasive potential of common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American freshwater systems. Canadian Journal of Fisheries and Aquatic Sciences 63, 1903–1910. Electronic References Baigún, C. R. M. & Quirós, R. (1985). Introducción de peces exóticos en la República Argentina. Informe técnico del Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP). Available at http://aquaticcommons.org/1705/1/Inf.Tec.AC2.pdf/ (last accessed 25 April 2013). FAO, (2010). The State of World Fisheries and Aquaculture. Rome: FAO. Available at http://www.fao.org/docrep/013/i1820e/i1820e.pdf/ (last accessed 26 February 2015). Jarvis, A., Reuter, H. I., Nelson, A. & Guevara, E. (2008). Hole-filled Seamless SRTM data V4. International Centre for Tropical Agriculture (CIAT). Available at http://srtm.csi.cgiar. org/ (last accessed 25 April 2014). Subsecretaría de Recursos Hídricos (2010). Atlas de cuencas y regiones hídricas superficiales de la república Argentina versión 2010. Buenos Aires: Ministerio de planificación federal. Available at http://www.hidricosargentina.gov.ar/info_mapas.php?seccion=info&link= mapas&mapa=i8/ (last accessed 26 February 2015). © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13014