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Marine Biodiversity

, Volume 48, Issue 4, pp 2237–2242 | Cite as

Evidence of a rapid colonization of the Atlantic European waters by the non-native weakfish Cynoscion regalis (Perciformes: Sciaenidae)

  • Rafael Bañón
  • David Barros-García
  • David Gómez
  • Maria Berta-Ríos
  • A. de Carlos
Short Communication

Abstract

The weakfish Cynoscion regalis is a sciaenid native to the northwest Atlantic, along the North American coast. It was reported for the first time outside its native distributional range in a Belgian estuary in 2009. Six specimens were captured in different locations of northwestern Spanish Atlantic waters in 2016. They were identified by examining morphological traits and DNA sequences within a taxonomic integrative context. A revision of the records of this non-native species in European coastal waters was also carried out. The fact that various specimens of weakfish have been captured in the last 7 years, along with a wide distribution range, could indicate rapid expansion and colonization processes along the northeastern Atlantic coasts.

Keywords

Biological invasion Marine introduction Weakfish Cynoscion regalis Atlantic European waters 

Introduction

The family Sciaenidae comprises about 67 genera with 283 species of demersal worldwide distributed fishes (McEachran and Fechhelm 2005; Nelson et al. 2016). Only five native species occur in the Iberian and Atlantic European waters: Argyrosomus regius (Asso, 1801), Sciaena umbra Linnaeus, 1758, Umbrina canariensis Valenciennes, 1843, Umbrina cirrosa (Linnaeus, 1758), and Umbrina ronchus Valenciennes, 1843 (Quéro et al. 2003; Lloris 2015).

The weakfish Cynoscion regalis (Sciaenidae) is native to the Atlantic coast of North America, from Nova Scotia to the southern and western coasts of Florida, where it is less common (McEachran and Fechhelm 2005). It is most abundant off the coast from North Carolina to New York (Lowerre-Barbieri et al. 1996). In recent years, this species has also been reported outside its native distributional range in the northeastern Atlantic, first in Belgium in 2009 (Agentschap voor Natuur en Bos 2011). It was introduced from 2011 in the Gulf of Cádiz, initially misidentified as Cynoscion nebulosus (Acosta et al. 2013) and later correctly identified (Bañón et al. 2017). Recently, the species has also been caught in diverse areas of south and central Portugal (Béarez et al. 2016; Morais and Teodósio 2016; Gomes et al. 2017).

The aim of this manuscript is to report new records of C. regalis in the northeastern Atlantic waters of Galicia, and to review and discuss its current status in the context of a rapid colonization of a non-native fish species in the Atlantic European waters.

Materials and methods

Six specimens of the weakfish Cynoscion regalis (Bloch & Schneider, 1801) were captured in Galician waters (northwest of Spain) by the artisanal fleet during 2016, but only the first four were preserved (Table 1). According to fishermen depositions, this species has been frequently caught in the Ría de Vigo during the summer season, indicating 2016 as the year of the introduction of this species in Galician waters.
Table 1

Main data of the weakfish records captured in Galician waters

Date

Zone

Latitude

Longitude

Depth (m)

TL (mm)

20th April 2016

Ría de O Barqueiro

43.7698 N

−7.6672 W

7

323

20th April 2016

Ría de O Barqueiro

43.7698 N

−7.6672 W

7

324

20th May 2016

Ría de Vigo

42.1831 N

−8.9009 W

12

264

25th October 2016

Ría de Vigo

42.1373 N

−8.8346′ W

4

304

27th October 2016

Ría de Sada

43.4065 N

−8.3349 W

3.5

28th October 2016

Ría de Vigo

42.1373 N

−8.8346′ W

4

Specimens were kept frozen at −20 °C and, once thawed, measurements and meristic characters were obtained to the nearest mm; finally, they were preserved in 80% ethanol in the laboratory. The identification was accomplished using descriptions and keys reported by Chao (2002a, b).

A sample of muscle from each specimen was taken for DNA isolation using a centrifuged column procedure (E.Z.N.A. Tissue DNA Kit). Polymerase chain reaction (PCR) amplification and sequencing of the standard 5′ barcoding region of the mitochondrial cytochrome c oxidase subunit I (COI) gene was performed following previous procedures (Bañón et al. 2013) and using the primer set named COI-3 (Ivanova et al. 2007). A 652-bp nucleotide sequence was obtained for each specimen and deposited in the GenBank repository with accession numbers KX369273, KX369274, and KX820248.

A sequence alignment was built using COI sequences from C. regalis and C. arenarius, employed as the outgroup, searched among the published and released data from the BOLD Systems repository, with a total of 651 positions in the final dataset. The differences among DNA sequences were inferred using p-distances (Nei and Kumar 2000) and represented as a neighbor-joining (NJ) tree (Saitou and Nei 1987), which was edited using the program TreeGraph (Stöver and Müller 2010). Confidence limits were established after 2000 bootstrap replicates (Felsenstein 1985). These procedures were conducted employing the computing package MEGA6 (Tamura et al. 2013).

The preserved specimens were deposited in the fish collection of the “Museo Luis Iglesias de Ciencias Ciencias Naturais”, Santiago de Compostela (Galicia, Spain) with the reference numbers MHNUSC 25048-1 to MHNUSC 25048-3.

Results

The main morphometric and meristic characters are presented in Table 2. These data are in agreement with measurements and counts reported by other authors describing this species in both the western and eastern Atlantic coasts (McEachran and Fechhelm 2005; Bañón et al. 2017). The presence of scales at the base of the soft dorsal and anal fins, the size and disposition pattern of the spots, and the biometrics and meristic counts distinguish this species from other sciaenid species.
Table 2

Comparison of morphometric, meristic, and respective body proportion data for specimens of Cynoscion regalis from the eastern Atlantic (MHNUSC, Galicia and CFM-IEOMA, Gulf of Cádiz) and western Atlantic (McEachran and Fechhelm 2005)

Cynoscion regalis

MHNUSC 25048 1–4

CFM-IEOMA-6020-6032

McEachran and Fechhelm (2005)

Total length (mm)

264–324

276–330

Standard length (mm)

225–276

234–285

As % Ls

 Head length

26.6–29.8

27.1–29.4

29–32

 Eye diameter

5.1–5.8

5–6

6–7

 Preorbital length

5.9–7.6

5.9–7.4

7–8

 Postorbital length

15.2–16.4

15.8–16.5

 Interorbital length

5.9–6.7

6.1–7.3

5–6

 Maxillar length

11.2–11.8

10.7–12.2

13–14

 Predorsal length

32.6–33.8

30.8–34.5

 Dorsal base length

50–52

50.2–56.0

 Preanal length

70.1–72.4

68.4–73.3

 Anal base length

10.6–12.2

9.7–11.8

 Pectoral length

15.9–16.5

15.4–16.9

13–15

 Pelvic length

14.4–15.6

14.3–16.5

 Prepelvic length

29.5–32.9

27.1–31.3

 Prepectoral length

25.8–28

24.2–27.6

 Body depth

24.6–26.6

24.2–28.3

24–25

Meristic features

 Dorsal fin rays

X + I + 25–27

X + I + 26–29

X + I + 24–29

 Anal fin rays

II + 10–11

II + 11–12

II + 10–13

 Ventral fin rays

I + 5

I + 5

 Pectoral fin rays

19

18–20

18–19

 Pored scales lateral line

53–58

53–59

 Branchiostegal rays

7

7

 Gill rakers

5–7 + 1 + 11

5–6 + 1 + 10–11

14–20

The resulting NJ tree grouped together in a strongly supported clade all the C. regalis specimens, independently from their native or introduced origin. The C. regalis clade is constituted by 15 individuals who shared the same haplotype among them. This cluster also appeared separated from the clade formed by the closely related species C. arenarius (Fig. 1). A map showing the native distribution area and the locations of records over the time in the European areas is shown (Fig. 2).
Fig. 1

Neighbor-joining (NJ) tree based on an alignment of 651 nucleotides of the cytochrome c oxidase subunit I (COI) gene. The numbers at nodes show bootstrap support values (only above 70%) after 2000 replicates. GenBank accession numbers and geographical locations are shown after the species names. Specimens from this study are highlighted in bold

Fig. 2

Map representing the native distribution of Cynoscion regalis in the northwestern Atlantic (blue area) and non-native records in the northeastern Atlantic (red stars) as follows: Belgian waters (1); Guadalquivir estuary (2); Guadiana river (3); Sado estuary (4); Tagus estuary and central-west coast of Portugal (5); and Galician waters (This study). See the text for a more comprehensive explanation

Discussion

The morphological measurements and meristic counts of the examined specimens allowed their taxonomic identification as C. regalis, a fact also strongly supported by the DNA barcoding results. These are the first records of this species in Galician waters and the northernmost report from the Iberian Peninsula. Previous occurrences of alien marine fishes in this area are mainly due to the arrival of southern warm affinity species by natural displacement, due to global warming and changes in the oceanic conditions (Bañón and Santás 2011; Bañón et al. 2014). This is also the first documented case of a native western Atlantic fish species in the area, although the occurrence of a specimen of the striped bass Morone saxatilis was also recorded on 8th February 2015, at 43° 17′ 50″ °N 8° 41′ 09″ W, in the north of Galicia (http://santinitas.blogspot.com.es), although the morphological examination and confirmation of this record was not possible.

Although the introduction vector of C. regalis is unknown, it is very unlikely that this species would have crossed the Atlantic Ocean by itself (Béarez et al. 2016), and anthropogenic causes seem to be the most probable pathway. As this species is not cultured in Spain, introduction by shipping seems to be the most plausible vector. Actually, ship transport was reported as the most probable method of entry into other European areas where this species has been detected (Béarez et al. 2016; Morais and Teodósio 2016; Bañón et al. 2017), whereas Gomes et al. (2017) only mentioned the anthropogenic factor as the most probable cause. The fact that the majority of the reported Galician specimens were detected in the proximities of international trading ports such as Celeiro, San Cibrao, and Vigo would support this hypothesis.

Secondary introduction from already reported areas is also possible. The first documented record in the eastern Atlantic occurred in Belgian waters in 2009 and happened to be a juvenile of 98 mm TL captured as a solitary specimen (Stevens pers. comm.), which makes it unlikely to be the origin of posterior European records. All other records have been reported from the waters surrounding the Iberian Peninsula, first in 2011, in the Guadalquivir estuary, in the Gulf of Cádiz, where C. regalis now constitutes a well-established and commercially exploited population of mature specimens (Bañón et al. 2017). Posterior records northwards of this site, in the Guadiana, Sado, and Tagus estuaries, the central-west coast of Portugal, and in Galician waters (Spain) in 2015 and 2016 could represent expansions of the introduced Guadalquivir estuary population, either due to natural migration and/or to displacement by northward currents. Since, in its native area, seasonal migration during the spring leads the weakfish in a northern movement along the coast (Wilk 1979), a similar behavior could have happened in the eastern Atlantic. The existence of a northward flow off western Iberia could help in explaining the apparent northern expansion of C. regalis. Part of this flow originates from the south, possibly as a recirculation of the Azores Current from the Gulf of Cádiz (Peliz et al. 2005). Also to be considered is the winter Iberian Poleward Current, which flows over the shelf on the Atlantic side of Iberia, transporting warm and salty surface waters northward and reaching the northwestern Iberian margin (Teles-Machado et al. 2015). As successive introductions in ballast water are unlikely, we hypothesize that both the Portuguese and the Galician records are due to expansions of the first introduction in the Iberian Peninsula, in the Guadalquivir estuary. This is also supported by the homing of spawning weakfish to natal estuaries, ranging from 60 to 81% in its native area, similar to the estimates of natal homing in birds and anadromous fishes (Thorrold et al. 2001).

Morais and Teodósio (2016) report one specimen of weakfish from the Guadiana estuary. However, their manuscript is poorly documented and includes some erroneous conclusions. It is pointed out that it is the first report of the presence of weakfish in Europe, but the first report corresponds to a Belgian specimen caught in 2009 (Agentschap voor Natuur en Bos 2011). These authors are neither ignoring the misidentification of C. regalis as C. nebulosus (Acosta et al. 2013) in the nearby Guadalquivir estuary (Béarez et al. 2016; Bañón et al. 2017), but also that this species is already well established in this estuary (Bañón et al. 2017). Accordingly, they also erroneously conclude that the Sado river estuary was the first site of introduction of C. regalis in the Iberian Peninsula waters.

The occurrence of several specimens along a wide distributional range, including an already established population in the Gulf of Cádiz, seems to be indicative of rapid colonization and expansion processes of C. regalis in the Atlantic European waters. Marine fish introductions are thought to have limited effects on ecosystems, which is in sharp contrast with the behavior of exotic fishes in estuaries and inland seas, generally having devastating effects on fish communities and fisheries (Baltz 1991). Weakfish are facultative estuarine-dependent organisms that use estuarine and coastal areas as feeding and nursery grounds (Turnure et al. 2015). Adult specimens are piscivorous and their presence could account as a factor influencing the estuarine food web and/or the populations of some native species with time.

The impact of C. regalis in the European coastal ecosystems, mainly in estuarine areas, should be the focus of future investigations. A first approach has been carried out by Morais and Teodósio (2016), comparing some reproductive aspects of the exotic weakfish with the native meager Argyrosomus regius, recommending the establishment of a monitoring program for these two sciaenid species in the Gulf of Cádiz and adjacent estuarine nursery areas. This area, due to the spawning site fidelity, should also be the first focus of future reproductive and recruitment studies of C. regalis in European waters, which may help in developing proper management regimes.

Notes

Acknowledgments

We are grateful to Jose Carlos García Lemos (vessel “O Vilela”) and “Confraría de Cangas” staff for providing the specimen and data of C. regalis from the Ría de Vigo and to Manuel and Bernardo Riveira Vale (vessel “Hermanos Riveira”) and “Confrarías de O Vicedo and Celeiro” staff for providing the specimen and data of C. regalis from the Ría de O Barqueiro. Thanks also go to Alberto Arias, Diego Arana, and José Antonio Cuesta for providing sequences and information of this species from the Gulf of Cádiz. This study was partially financed by the Agreement between CSIC and Xunta de Galicia to analyze fisheries-dependent data from the monitoring program of small-scale fisheries in Galicia (Agreement no. 070401150009).

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Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Instituto de Investigaciones Marinas, Consejo Superior de Investigaciones Científicas, IIM-CSICVigoSpain
  2. 2.Grupo de Estudos do Medio Mariño (GEMM)RibeiraSpain
  3. 3.Centro de Apoyo Científico y Tecnológico a la InvestigaciónUniversidad de VigoVigoSpain
  4. 4.Programa de Doctorado en Metodología y Aplicaciones en Ciencias de la Vida, Facultad de BiologíaUniversidad de VigoVigoSpain
  5. 5.BaioSpain
  6. 6.Cofradía de Pescadores San JoséCangas do MorrazoSpain
  7. 7.Departamento de Bioquímica, Genética e InmunologíaUniversidad de VigoVigoSpain

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