First record of the North American black bullhead Ameiurus melas (Rafinesque, 1820) in the Guadalquivir Estuary (Southern Spain)

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1 Aquatic Invasions (2009) Volume 4, Issue 4: DOI /ai The Author(s) Journal compilation 2009 REABIC ( This is an Open Access article Short communication First record of the North American black bullhead Ameiurus melas (Rafinesque, 1820) in the Guadalquivir Estuary (Southern Spain) Juan Garcia-de-Lomas 1*, Elías D Dana 1, Javier López-Santiago 1, Rubén González 1, Guillermo Ceballos 2 and Fernando Ortega 2 1 Programa Andaluz para el Control de las Especies Exóticas Invasoras, Egmasa Consejería de Medio Ambiente, C/Américo Vespucio 5, Puerta 2, Bloque C, Local 5, Sevilla, Spain jgarciadelomas@egmasa.es (JGL); edana@egmasa.es (EDD); jlopezsa@egmasa.es (JLS); rgonzalezp@egmasa.es (RG) 2 Dirección General de Gestión del Medio Natural, Consejería de Medio Ambiente, Avda, Manuel Siurot 50, Sevilla, Spain guillermo.ceballos.ext@juntadeandalucia.es (GC); fernando.ortega@juntadeandalucia.es (FO) * Corresponding author Received 30 June 2009; accepted in revised form 20 August 2009; published online 29 September 2009 Abstract The North American black bullhead Ameiurus melas has been recorded for the first time in the Guadalquivir Estuary. The abundance of A. melas was monitored and quantified after first detection (February, 2007), with captures in two consecutive surveys (from October to December for 2007 and 2008) using nylon fyke nets. Catch per unit effort (CPUE) showed a rapid increase from 0.11 individuals per net in 2007 to 0.47 ind net -1 in Additionally, A. melas specimens collected in the 2008 survey (n = 1563), were measured (LT) and weighed to study the population structure and allometric growth relationship. The rapid increase in abundance of A. melas, together with the cohort analysis of individuals collected in the 2008 survey, suggest that incipient reproduction of black bullhead is already occurring. The invasion of A. melas constitutes a new threat to biodiversity in the Guadalquivir Estuary and connected natural parks and reserves (e.g., Doñana National Park). It also presents potential economic damage to fisheries and aquaculture fish-farms. Key words: Ictaluridae, catfish, non-native species, biological invasions The black bullhead Ameiurus melas (Rafinesque, 1820) (Ictaluridae, Siluriformes) is a freshwater fish native to North America from the Great Lakes to northern Mexico (Page and Burr 1991). This demersal species is found in low-flowing habitats with soft substrata in riverine and lacustrine environments, including artificial ponds and reservoirs. A. melas is considered an invasive species in some locations outside of its native range. High fecundity, parental care, voracious and versatile feeding habits, water quality flexibility and tolerance to pollution are among the ecological attributes that support its invasive potential (Vila-Gispert et al. 2005; Leunda et al. 2008; Ribeiro et al. 2008). A. melas was introduced to the Iberian Peninsula (Banyoles Lake) in the early 20th century, either for angling or improvement of fish communities (Elvira 1984; Elvira and Almodóvar 2001). Natural spread and indiscriminate introductions have increased rapidly the distribution of A. melas within the Iberian Peninsula. Currently, A. melas has been cited in the rivers Ebro (northern Spain), Guadarrama (Centre of Spain) (Leunda et al. 2008), Tagus and Guadiana (mid and southern Portugal, respectively) (Gante and Santos 2002; Ribeiro et al. 2009). This increasing distribution involves a new threat to native fish species and freshwater aquatic communities. The aim of the present paper is to make the first report of A. melas in the Guadalquivir Estuary, which occurred during the completion of control measures by the Regional Andalusian Government (Consejeria de Medio Ambiente) on non-native Chinese mitten crab Eriocheir sinensis (H. Milne Edwards, 1853). The Guadalquivir Estuary is a temperate, non stratified estuary with a gradual horizontal change of water salinity located in the southwest 719

2 J. Garcia-de-Lomas et al. Figure 1. Guadalquivir Estuary, indicating the location of first record (black circle) of Ameiurus melas, the main tributaries (blue lines) and protected areas (grey polygons) part of the Iberian Peninsula (Figure 1). The estuarine is subjected mixing-zone changes due to daily and seasonal tidal variations, with a mean sea water upstream incursion of 20 km (Drake et al. 1999). A dam located at 108 km upstream the river regulates the freshwater input to the estuary. Specimens of A. melas were collected in the upper stretch of the estuary, near the city of Seville (37º20'N; 06º01'W), where salinities were <5 (Baldó et al. 2005). Nylon fyke nets arranged parallel to the shore at water depths of 2 5 m were used to capture the specimens (Figure 2). Fyke net characteristics were: 6 m leads, three hoops per net (1, 0.95 and 0.85 m diameter), throat diameter of 15, 10 and 8 cm, respectively, and 7 mm square mesh. Nets were left in the river and emptied every 48 h during the months of March to December in 2005; January to April in 2006; January to June in 2007, with additional sampling October to December in 2007 and In the laboratory, identification to species was undertaken using descriptions in Scott and Crossmann (1973), with specific reference to the number of anal fin rays, colour of fin membranes and aspect of pectoral fin spine. Specimens collected in 2008 (n = 1563) were measured for total length (L T ) to the nearest mm and weighed (to the nearest 1 g), with cohorts provisionally identified using modal class progression analysis (length-frequency). Length (cm) and weight (g) data of A. melas were log-transformed and the resulting linear relationship fit to the least-square regression, using weight as the dependent variable: logw = loga + b logl T (Bagenal 1978). The catch-per-unit-effort (CPUE) were evaluated to assess population success. Specimens of A. melas collected in the Guadalquivir Estuary coincide with identification characters of A. melas reported by Elvira (1984) and Cucherousset et al. (2006): D I/6, P I/7, V 8, A and C A. melas was first 720

3 Ameiurus melas in the Guadalquivir Estuary collected in February, Accompanying fish species found included the native species Barbus spp. (Cuvier, 1816), Liza spp. (Jordan and Swain, 1884), European eel Anguilla anguilla (Linnaeus, 1758) and sea bass Dicentrarchus labrax (Linnaeus, 1758), and the introduced species pumpkinseed Lepomis gibbosus (Linnaeus, 1758), common carp Cyprinus carpio (Linnaeus, 1758), largemouth bass Micropterus salmoides (Lacepede, 1802) and chameleon fish Australoheros Cichlasoma facetus (Jenyns, 1842). Capture abundance and effort data revealed that CPUE of A. melas increased fourfold after one year following the first detection (from 0.11 ind net -1 in 2007 to 0.47 ind net -1 in 2008). Figure 2. Ameiurus melas specimens collected in the Guadalquivir Estuary. Detail of an adult specimen (LT = 304 mm) (a); detail of specimens of different size (b); details of the mouth and barbles (c), first dorsal fin rays (d), pectoral fin rays (e) and caudal fin rays (f) (Photograph by J. Garcia-de-Lomas) 721

4 J. Garcia-de-Lomas et al. The analysis of the population size-structure and environmental versatility give additional support to the invasion potential of A. melas in the Guadalquivir Estuary. The absence of A. melas before 2007 suggest a recent introduction in the Guadalquivir Estuary A. melas specimens collected in the 2008 survey revealed the presence of two clear cohorts (Figure 3), likely to be those spawned in 2007 (> 150 mm L T ) and in 2008 (100 mm < L T <150 mm), respectively. The size ranges of these provisional cohorts are similar to those reported by Hanchin et al. (2002) for native A. melas. The presence of two well-differentiated cohorts suggest that active reproduction had already occurred in Spring, The presence of small specimens (<100 mm L T ; Figure 3) provides evidence of reproduction in the Guadalquivir Estuary, the small number of specimens probably being due to the type of sampling gear used (young-of-theyear specimens are pelagic; Cucherousset et al. 2006) and the dates sampled (young A. melas move about in tighty-packed shoals, following the mother, until early Autumn). These results suggest two possible scenarios for the introduction of A. melas in the Guadalquivir Estuary: (a) illegal introduction of young specimens for angling; or (b) accidental introduction of some breeding adults from neighbouring areas. The allometric growth equation here calculated for A. melas (logw = logl T ; r 2 = 0.97, P < 0.001, n = 1563), was very similar to that reported by Pedicillo et al. (2008) (intercept = , slope = 3.071). Concerning the environmental versatility, the salinity tolerance limits of A. melas (median lethal concentration) is (Bringolf et al. 2005), therefore this species could spread out through most of the Guadalquivir Estuary, excepting the lower 20 km (Baldó et al. 2001). The Guadalquivir Estuary is a highly productive ecosystem that provides permanent habitats for estuarine species as well as playing an important role as breeding and adult-feeding grounds for marine species (Baldó and Drake 2002; González-Gordillo and Rodríguez 2003). Considering the current increase of the A. melas population and its ability to feed voraciously on a variety of prey from small aquatic macroinvertebrates to fish (Leunda et al. 2008), further impacts on estuarine ecosystem function and services may occur but this requires further study. Acknowledgements This work was funded by the Environmental Council of the Regional Government (Consejeria de Medio Ambiente, Junta de Andalucía), through the Andalusian Programme for the Control of Invasive Alien Species. The authors sincerely thank P. Leon for support during catfish measurements, M. Montijano for storage of samples, and A. Ruiz for helpful comments on the cohort analysis. We are grateful to the port authorities for the facilities and permissions to carry out the work, and to three anonymous reviewers for their comments and suggestions on an earlier version of the manuscript. References Figure 3. Total length (L T, mm) of Ameiurus melas in the 2008 survey. Sample size (n) of each month is indicated Baldó F, Arias AM, Drake P (2001) Macrobentos en el estuario del Guadalquivir. Boletin del Instituto Español de Oceanografía 17: Baldó F, Drake P (2002) A multivariate approach to the feeding habits of small fishes in the Guadalquivir Estuary. Journal of Fish Biology 61: 21-32, doi: / j tb01758.x Baldó F, Cuesta JA, Fernández-Delgado C, Drake P (2005) Efecto de la regulación del caudal del Río Guadalquivir sobre las características físico-químicas del agua y la macrofauna acuática de su estuario. Ciencias Marinas 31:

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