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The transatlantic introduction of weakfish Cynoscion regalis (Sciaenidae, Pisces) into Europe

November 2016
BioInvasions Records 5(4)

DOI:10.3391/bir.2016.5.4.11

Authors:

Pedro Morais

Florida International University

Maria Alexandra Teodósio Chícharo

Universidade do Algarve

Weakfish Cynoscion regalis (Bloch & Schneider, 1801) is a sciaenid fish native to the east coast of North America and has been recently collected in three areas of the Iberian Peninsula (Europe). We aimed to i) provide the first report of the presence of weakfish in Europe, ii) hypothesize the most likely introduction vector, iii) discuss the potential for ecological overlap between weakfish and meagre Argyrosomus regius (Asso, 1801), the native Sciaenidae species, and iv) highlight the importance of citizen science in the detection of non-native species. Weakfish were captured in the Sado estuary (July 2014), Gulf of Cadiz (November 2015) and the adjacent Guadiana estuary (June 2016), and in two Galician Rías (June 2016). Anglers reported that weakfish was present in the Sado estuary for “some” years, while their presence was only noticed recently in the other two areas. We hypothesize that ballast water was the introduction vector, that weakfish established a reproducing population in the non-native range, and that it dispersed from the Sado estuary, a central region of its current distribution range. The Sado estuary might have been the introduction area for weakfish via ballast water because there is a busy transoceanic commercial port in the estuary. Moreover, they are not used in European aquaculture facilities, nor in the aquarium trade. The collected specimens were ≤50 cm, with average lengths of 30 cm, which corresponds to a median age of 2 years and to individuals capable of reproducing. As a result, the year of introduction must be before 2012. Weakfish have a similar ecological niche to meagre, but the outcome of potential interactions is uncertain. Citizen science, especially the initiative of local fishermen, was critical to detect this non-native species.

Map of the Iberian Peninsula indicating the Guadiana River basin (A) and location where the specimen of weakfish Cynoscion regalis was collected in the Guadiana estuary on 16 June 2016 (white star) (B).

…

Photograph of the weakfish Cynoscion regalis collected in the Guadiana estuary on 16 June 16th, 2016 (A), and detailed photos of the head and operculum (B) and of the pigmentation pattern in the dorsal area and second dorsal fin (C). Scale bars: 1 cm.

…

Figures - uploaded by Pedro Morais

Content may be subject to copyright.

Content uploaded by Pedro Morais

Content may be subject to copyright.

BioInvasions Records (2016) Volume 5 Article in press

Open Access

Rapid Communication CORRECTED PROOF

The transatlantic introduction of weakfish Cynoscion regalis

(Bloch & Schneider, 1801) (Sciaenidae, Pisces) into Europe

Pedro Morais

1,2

and Maria Alexandra Teodósio

CCMAR – Centre of Marine Sciences, Campus de Gambelas, University of Algarve, 8005-139 Faro, Portugal

CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de

Cruzeiros do Porto de Leixões, Avenida Norton de Matos, 4450-208 Matosinhos, Portugal

E-mail addresses: pmorais@ualg.pt (PM), mchichar@ualg.pt (MAT)

*Corresponding author

Received: 28 June 2016 / Accepted: 28 September 2016 / Published online: 7 October 2016

Handling editor: Charles W. Martin

Abstract

Weakfish Cynoscion regalis (Bloch and Schneider, 1801) is a sciaenid fish native to the east coast of North America and has been recently

collected in three areas of the Iberian Peninsula (Europe). We aimed to i) provide the first report of the presence of weakfish in Europe,

ii) hypothesize the most likely introduction vector, iii) discuss the potential for ecological overlap between weakfish and meagre

Argyrosomus regius (Asso, 1801), the native Sciaenidae species, and iv) highlight the importance of citizen science in the detection of non-

native species. Weakfish were captured in the Sado estuary (July 2014), Gulf of Cadiz (November 2015) and the adjacent Guadiana estuary

(June 2016), and in two Galician Rías (June 2016). Anglers reported that weakfish was present in the Sado estuary for “some” years, while

their presence was only noticed recently in the other two areas. We hypothesize that ballast water was the introduction vector, that weakfish

established a reproducing population in the non-native range, and that it dispersed from the Sado estuary, a central region of its current

distribution range. The Sado estuary might have been the introduction area for weakfish via ballast water because there is a busy transoceanic

commercial port in the estuary. Moreover, they are not used in European aquaculture facilities, nor in the aquarium trade. The collected

specimens were ≤50 cm, with average lengths of 30 cm, which corresponds to a median age of 2 years and to individuals capable of

reproducing. As a result, the year of introduction must be before 2012. Weakfish have a similar ecological niche to meagre, but the outcome

of potential interactions is uncertain. Citizen science, especially the initiative of local fishermen, was critical to detect this non-native species.

Key words: non-native, fish, ballast water, citizen science, Portugal, Spain, Iberian Peninsula

Introduction

Reports on transoceanic marine invasions are

becoming more common (Callaway et al. 2006), and

they consist primarily of introductions of

holoplanktonic (Berg et al. 2002) and meroplanktonic

invertebrate species via ballast water (Roman 2006).

In the case of vertebrates (i.e. fish), intentional

introductions (e.g., for recreational fishing), escapees

from aquaculture facilities (Bartley 2011 (Copp et

al. 2007), and aquarium release (Brice et al. 2004)

are the most common vectors of introduction rather

than via ballast water (Wonham et al. 2000;

Grigorovich et al. 2003; Copp et al. 2007).

The presence of weakfish Cynoscion regalis

(Bloch and Schneider, 1801) (Sciaenidae, Pisces) in

the Iberian Peninsula (western Europe) is a recent

example of a transoceanic marine fish introduction.

This species is native to the east coast of North

America (Froese and Pauly 2016), was detected by

fishermen in several regions of the Iberian Peninsula

and subsequently announced in specialized magazines

(Mundo da Pesca 2016), personal blogs (OsPescas

2015), and regional online media (e.g., A Voz do

Algarve 2016; Europapress 2016; Vigoe 2016). The

native distribution of weakfish is from Florida’s

Atlantic coast (USA) to Nova Scotia (Canada), where

it is exploited in commercial and sport fisheries

(Froese and Pauly 2016; NMFS 2016). In Europe,

the meagre Argyrosomus regius (Asso, 1801) is the

most abundant Sciaenidae species. The meagre is a

valuable species for local and artisanal fisheries and

sport fishing, and it is also reared in aquaculture

(Mañanós et al. 2009; Duncan et al. 2013).

P. Morais and M.A. Teodósio

Weakfish and meagre share several ecological

traits (e.g. habitat use, reproduction period, diet)

(Froese and Pauly 2016) so their fundamental niche

might overlap where they now co-occur in the

Iberian Peninsula. In this paper we: i) provided the

first scientific report of weakfish in Europe;

ii) described the putative introduction vectors;

iii) discussed the potential ecological overlap

between weakfish and meagre; and iv) highlighted

the importance of citizen science in the detection of

non-native species.

Material and methods

Study area

The Guadiana River estuary is a mesotidal estuary

with an average depth of 6.5 m, occupying an area

of 22 km2, and the tidal amplitudes range from 1.3 to

3.5 m. The estuary drains into the Gulf of Cadiz

(Atlantic Ocean), extends inland for 70 km, and the

last 50 km serve as the southern border of Portugal

and Spain (Iberian Peninsula, Europe) (Figure 1).

The Guadiana River flow varies substantially within

and among years because of variations in rainfall.

However, after the completion of the Alqueva dam

in February 2002, the river discharge is usually lower

than 20 m3 s

-1 (Garel and Ferreira 2011), despite

episodic flooding events (e.g. March–April 2013).

Capture, identification, and distribution of weakfish

in Europe

One adult weakfish was collected in the Guadiana

estuary (SW-Iberian Peninsula) (Figure 1) using

longline fishing gear as part of a routine commercial

fishing operation. The longline was set in the estuary

11 km upstream from the river mouth (37º15′33″N;

7º25′55″W) during the night of 15 June 2016 and

retrieved 12 hours later. The identification of the

specimen was made according to Bigelow and

Schroeder (1953). The total length (TL, ±0.1 cm)

and total fresh weight (TFW, ±1 g) were determined,

and the meristic characteristics recorded: fin rays,

gill rakers, and lateral line scales.

After the identification of the specimen, we

established several contacts with fishermen and scien-

tists and also did online searches (in Portuguese,

Spanish, French, and English) to verify the existence

of previous records of this species in Europe. Then,

we made a press release (in Portuguese) announcing

the collection of weakfish in the Guadiana estuary to

reach a broad audience and get feedback from the

general public about the presence of this species in

Portugal.

Figure 1. Map of the Iberian Peninsula indicating the Guadiana

River basin (A) and location where the specimen of weakfish

Cynoscion regalis was collected in the Guadiana estuary on 16

June 2016 (white star) (B).

Results

The morphological characteristics of the specimen

we obtained from the Guadiana estuary, based dorsal

pigmentation and dorsal fin pigmentation (Figure 2),

allowed its identification as weakfish Cynoscion

regalis. This specimen measured 32.6 cm TL and

Transatlantic fish introduction into Europe

Figure 2. The specimen of weakfish Cynoscion regalis collected in the Guadiana estuary on 16 June 2016 (A), and detailed photos of the

head and operculum (B) and of the pigmentation pattern in the dorsal area and second dorsal fin (C). Scale bars: 1 cm. Photographs by Pedro

Morais.

Table 1. Meristic characteristics of the weakfish specimen collected in the Guadiana estuary, on 16

June 2016, of weakfish from its native

area on the east coast of North America and of meagre. Meristic data for North American weakfish is from Tagatz (1967) and Froese and

Pauly (2016), while meagre meristic data is from Chao (1986) and Dulčić et al. (2009).

Guadiana weakfish North America weakfish Meagre

Dorsal fins rays D

X, D

I+27 D

X, D

I+24–29 D

IX–X, D

I+26–29

Pectoral fin rays 18 – 16

Pelvic fin rays 5 – I–5

Anal fin rays II+11 II+10–13 II+7–8

Caudal fin rays 17 – –

Gill rakers 5+12 4–5+10–12 –

Lateral line scales 78 76–86 53

weighed 381 g TFW. The meristic characteristics of

the specimen fell within the range described for the

species in its native North American range (Table 1).

As of 24 June 2016, there were three online media

reports of weakfish in Europe. Weakfish were

reported for the first time in regional online media in

February 2016 when mention was made of their

capture in the Gulf of Cadiz (SW-Iberian Peninsula)

in November 2015 (Europapress 2016). These speci-

mens were collected by fishermen and identified by

A Arias, J Cuesta, and R Bañón (R. Bañón, Grupo

de Estudo do Medio Mariño, Spain, pers. comm.).

The fish from the Gulf of Cadiz ranged between 28 cm

and 33 cm TL although there were unsubstantiated

accounts of fish of almost 50 cm TL (Vigoe 2016).

The capture of weakfish in two Galician Rías (Ría de

Vigo and Ría O Barqueiro) was reported on 20 June

2016 (Vigoe 2016). These fish ranged between 26 cm

and 32 cm TL. The capture of the Guadiana weakfish

(our specimen) was reported by regional media on

23 June 2016 (A Voz do Algarve 2016), and posted

on social networks (CCMAR 2016). As a result of

the media coverage, anglers came forward with

information that weakfish were present in the Sado

estuary (west coast of Portugal) for “some” years

(C Morais, P Santos, Portugal, pers. comm.). The

first online posting about weakfish in Sado estuary

including a photograph of the fish was made in a

personal blog on 24 September 2015 (OsPescas

2015). The Sado weakfish was similar in size to that

P. Morais and M.A. Teodósio

from the Guadiana estuary. Other weakfish were

caught by anglers in June and July 2016, one in the

southern coast of Portugal at Barranco das Belharucas

Beach (Olhos de Água county) on 5 June 2016

(E Pedro, pers. comm.) and two in the Sado estuary

(27 and 28 July 2016) (OsPescas 2015). Later on, an

anglers magazine also covered the report of

weakfish in the Guadiana estuary, and stated that

they mentioned the presence of weakfish in the Sado

estuary in July 2014 (Mundo da Pesca 2016).

Discussion

Weakfish in Europe

Hanel et al. (2009) described the occurrence of

seven Sciaenidae species along the European

coastline and adjacent seas: Argyrosomus regius

(Asso, 1801), Cynoscion nebulosus (Cuvier, 1830),

Pseudotolithus senegalensis (Valenciennes, 1833),

Sciaena umbra Linnaeus, 1758, Umbrina canariensis

Valenciennes, 1843, Umbrina cirrosa (Linnaeus,

1758), and Umbrina ronchus Valenciennes, 1843.

Our reporting of Cynoscion regalis in the Iberian

coast raises the number of Sciaenidae in Europe to

eight, and the second native to the northwestern

Atlantic—the other species present is spotted seatrout

Cynoscion nebulosus (Froese and Pauly 2016).

Weakfish distribution in the Iberian coast encom-

passes ~800 km of coastline, from Galicia (Vigoe

2016) to the Gulf of Cadiz (Europapress 2016);

however, it was reported from only five sites—Rías

de Vigo and O Barqueiro in Galicia, Sado estuary,

Gulf of Cadiz and the adjacent Guadiana estuary.

First reports of weakfish in the Iberian Peninsula

date back to July 2014 (Mundo da Pesca 2016) but

the year of introduction was likely before 2012, as

anglers mention that weakfish were collected in the

Sado estuary for “some” years before being

described in a magazine devoted to recreational

angling (OsPescas 2015; Mundo da Pesca 2016).

Weakfish of approximately 30 cm TL are 1–2 years

old, while fish of 50 cm are 2–3 years old (Hatch

2012). Thus, weakfish spent at least 3–4 years

without being noticed by the scientific community in

the Iberian Peninsula. The potential expansion of

weakfish to the northern European coast and adjacent

seas will likely be controlled by water temperatures

because they cease feeding at 7.9 C and die at 3.3 C

in the native range (Bigelow and Schroeder 1953).

Thus, weakfish has the potential to expand its range

in Europe up to the English Channel, to the Irish Sea

and the western coast of Scotland, where winter

water temperature coincides with their cease-feeding

temperature (SeaTemperature 2016).

Introduction, establishment, and dispersion

Aquarium and/or aquaculture release are unrealistic

introduction vectors for weakfish because the

species is not used in the aquarium trade or in

Portuguese and Spanish aquaculture practices (Laura

Ribeiro and Pedro Pousão Ferreira, Instituto Português

do Mar e da Atmosfera, person. comm.). So, we

hypothesize that ballast water was the most likely

vector of weakfish introduction in Europe. The short

duration of transoceanic ship travel between the east

coast of North America and the western Iberian

Peninsula coast (e.g. nine days, SeaRates 2016), and

the physiological plasticity of weakfish larvae and

young-of-the-year (i.e. present in the inner

continental shelf and in the brackish and oligohaline

estuarine sites) (Able and Fahay 2010) suggests that

weakfish were able to circumvent ballast water

exchange regulations. Ballast water management

guidelines include practices that minimize the uptake

of organisms and sediment into ballast tanks at the

port of origin, exchange of ballast water at sea, and

the discharge of water to shore reception facilities at

the port of destination, treatment and even the non-

release of ballast water (IMO 2016).

Assuming that the introduction via ballast water

is possible, then there are two main hypotheses that

could explain the apparent establishment of weakfish

in the Iberian Peninsula shores. Weakfish may form

a population that does not reproduce in Europe, but

mantain its presence through continuous and success-

ful introductions via ballast water; alternatively, the

species is able to reproduce in the non-native range.

The validation of these hypotheses minimally requires

the collection of ichthyoplankton samples to detect

their presence (or not), and analysis of gonadal tissues

from adult fishes. However, the size of the indivi-

duals collected and its broad distribution range suggest

that weakfish reproduce in the non-native range.

Weakfish are present in three Iberian regions,

with the extreme regions separated by ~800 km of

coastline. This fact suggests that the introduction of

weakfish occurred in either: a) three distinct regions

with subsequent establishment of three localized

populations; b) one region located in one of the

extreme regions of distribution (Gulf of Cadiz or

Galicia) and subsequent dispersion; or c) one central

area with subsequent establishment and dispersion.

The first hypothesis is the least likely since the

establishment of fish after their introduction through

ballast water is unusual (Wonham et al. 2000). Thus,

the introduction and establishment of weakfish in a

specific region and its subsequent dispersion and

establishment in other areas seems to be the most

feasible scenario. Based on the available information,

Transatlantic fish introduction into Europe

we hypothesize that the Sado estuary was the

introduction site as it is the region with the highest

number of non-indigenous marine species in

Portugal (Chainho et al. 2015) and the first report on

the presence of weakfish dates back to July 2014.

Three main factors contribute to this hypothesis.

First, local anglers mentioned the presence of weakfish

for “some” years in the Sado estuary. Second, this

estuary has a harbor with the intense traffic of

transoceanic ships, which increases propagule pressure.

Lastly, the Sado estuary and adjacent coastal area is

a highly productive ecosystem with adequate abiotic

conditions to enhance fish survival and growth

(Lankford and Targett 1994; Able and Fahay 2010)

and could allow the establishment and subsequent

transport and migration of weakfish larvae and

adults to other regions.

Ecological overlap between weakfish and meagre

Weakfish and meagre share several ecological

characteristics, including: feeding upon similar types

of prey (e.g. fish, penaeid and mysid shrimps, crabs,

amphipods, clams, annelids); using estuaries as

nurseries during the same period (from spring until

late summer and early autumn); and seeking

protection in holes and deep channels (Bigelow and

Schroeder 1953; Froese and Pauly 2016). However,

they differ in longevity, maximum size and weight,

time of the first maturity and fecundity. Weakfish

usually live 9–12 years, although the oldest fish

reported was 17 years old (Lowerre-Barbieri 1994).

Most fish are <98 cm and <8.9 kg (Froese and Pauly

2016). Meagre can live to 44 years (Prista et al.

2009) and reach 2.3 m and 103.0 kg (Froese and

Pauly 2016). Weakfish mature at an early age. For

example, in North Carolina, 52% of females and

62% of males mature at age 0, and at age 1 all

females >17.5 cm are mature, and fecundity can

reach 5.0 million eggs for a fish of 57 cm (SL)

(Merriner 1976). In contrast, the first sexual maturity

of male and female meagres is at 45 cm and 47 cm,

respectively (~2 years old) (Abou Shabana et al.

2012), while fecundity ranges between 2.1–31.1

million eggs for females with sizes ranging from

1.0–1.7 m (Gil et al. 2013).

It seems the native meagre would have an

advantage over weakfish because it grows to a larger

size, its fecundity is up to 6.2 higher, and weakfish

larvae and juveniles can eventually serve as prey to

meagre. However, weakfish mature sooner, and

might acquire higher fitness if they are able to leave

their parasites behind (i.e. enemy release hypothesis)

(Torchin et al. 2001) after their introduction in the

Iberian Peninsula coast. Thus, given the lack of

knowledge about meagre ecology during their

estuarine phase (e.g. abundance, feeding habits, realized

niche), plus the uncertainties about the outcome of

competition between meagre and weakfish (coexistence

in the same habitats, exclusion of meagres, dominance

of meagres over weakfish and thus controlling weakfish

invasion success) and the economic importance of

meagre in the Guadiana estuary, at least since the

18th century (de Lacerda Lobo 1815), we recommend

the establishment of a monitoring program for these

two Sciaenidae species in the Gulf of Cadiz and

adjacent estuarine nursery areas.

Citizen Science

The putative introduction of weakfish in the Sado

estuary, perhaps earlier than 2012, suggested that the

species had gone unnoticed by the Portuguese

scientific community. Recent budget cuts made by

the Portuguese government can only explain part of

this lack of awareness since this could have been

circumvented with effective communication strategies

between scientists and the general public. Indeed,

citizen science has shown its utility in the detection

of non-native and cryptic invasive species in a way

that would be impossible to be made solely by

scientists or at exorbitant costs (Epps et al. 2014;

Scyphers et al. 2015). For example, the detection of

weakfish in the Iberian Peninsula was only possible

due to fishermen’s contributions. This initial aware-

ness pressures the scientific community to establish

more efficient means of communication with the

public to allow the detection of non-native species

and other ecological threats. The use of new

smartphone technologies, social media platforms,

and other applications is a path that needs to be

further explored. Applications allowing the upload

of a species photograph to alert a group of specialists

(after determining whether the specimen is a plant-

or animal-like specimen, or aquatic or terrestrial

specimen) could aid in the detection of non-native

species. Ideally, this could allow the establishment

of more efficient programs of species control or

eradication, and ultimately help to determine their

suitability for commercial exploitation (e.g. food

consumption, biomedical active compounds).

The dialogue between aquatic scientists and the

general public has to acknowledge and promote the

“Research Responsible and Innovation” concept,

which proposes that the research questions should be

derived from societal problems and formulated with

their collaboration and thus responding to their

concerns (European Commission 2016). For example,

scientific workshops on non-native species can demon-

strate that scientists can assist local communities in

P. Morais and M.A. Teodósio

tackling this issue and also explore new business

opportunities, while scientists increase the temporal

and spatial resolution of long-term monitoring

programs of aquatic ecosystems. Aquatic invasions

scientists need to implement more efficient ways of

communication with society, especially with local

fishermen, to facilitate earlier detection of non-

native species and other ecological problems that

affect aquatic ecosystem services with negative

potential social and economic consequences.

Acknowledgements

We thank A Fernandes and J Estica for giving us the first

specimen of weakfish collected in the Guadiana estuary and J

Babaluk for proof-reading the paper. C Morais, E Pedro, and P

Santos provided information on the capture of weakfish in

Portugal. R Bañón (Grupo de Estudo do Medio Mariño, Spain)

provided information on the identification of weakfish in Spain,

while L Ribeiro and P Pousão Ferreira, both from “Instituto

Português do Mar e da Atmosfera”, provided information on the

aquaculture of Sciaenidae in the Iberian Peninsula. MAT was

funded by Foundation for Science and Technology (FCT,

Portugal) through a sabbatical fellowship (SFRH/BSAB/113684/

2015) and the European Regional Development Fund

(COMPETE program- Operational Competitiveness Programme

and national funds through FCT-PEst-C/MAR/LA0015/2011).

We also thank three anonymous reviewers, CW Martin and JM

Hanson for their suggestions on how to improve the initial

versions of this paper.

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Invasive fish keeps native feeding strategy despite high niche overlap with a congener species

Article

Aug 2021

Weakfish Cynoscion regalis (Bloch and Schneider, 1801) is one of the most recent invasive fish in the Iberian Peninsula (Europe). Weakfish has established in the Sado estuary (Portugal) since the early 2010s, and fishers and anglers have expressed concern about its impacts on native prize fish. However, almost a decade later, there is no information on the ecology of weakfish in the non-native area. So, we aimed to assess weakfish feeding strategy and feeding plasticity through stomach content analysis to evaluate if these factors may contribute to its invasiveness, as well as to determine the ecological overlap between weakfish and three native prize fish – European bass, white seabream, and particularly meagre (since they are taxonomically closer), through carbon and nitrogen stable isotopes. Our results demonstrate that Sado’s weakfish has a generalist feeding strategy and preys the same functional groups it targets in the native area, therefore feeding strategy may weigh on invasiveness but not feeding plasticity. Weakfish, meagre, and European bass were in the same trophic level and weakfish exhibited higher trophic overlap with meagre, suggesting that weakfish could directly impact meagre if food and habitat become limiting. This study is the first assessment about weakfish ecology in the non-native area and our findings are an excellent starting point to understand this invasion. It can also be useful for management programs that promote weakfish consumption to minimize its impacts, alleviate fishing pressure on native species, and raise public awareness.

Citizen Science and Biological Invasions: A Review

Article

Full-text available

Jan 2021

Biological invasions are among the most challenging ecological and conservation riddles of our times. Fortunately, citizen science projects became a valuable tool to detect non-indigenous species (NIS), document their spread, prevent dispersion, and eradicate localized populations. We evaluated the most undisputed definitions of citizen science and proposed that a combination of two of them is a better reflection of what citizen science has become. Thus, citizen science is any environmental and/or biological data collection and analysis, including data quality control, undertaken by members of the general public, as individuals or as organized groups of citizens, with the guidance and/or assistance of scientists toward solving environmental and/or community questions. With this review, we also assessed how citizen science has been advancing biological invasions research and its focus, by analyzing 126 peer-reviewed articles that used citizen science methods or data concerning NIS. Most of the articles studied terrestrial species (68%) and terrestrial plants were the most studied group (22.7%). Surprisingly, most first detection reports were of non-indigenous marine fish probably due to the constraints in accessing aquatic ecosystems which delays the detection of new NIS. Citizen science projects running over broad geographical areas are very cost-effective for the early detection of NIS, regardless of the studied environment. We also discuss the applicability and need to adapt the methods and approaches toward the studied ecosystem and species, but also the profile of the participating citizens, their motivations, level of engagement, or social status. We recommend authors to better acknowledge the work done by contributing citizens, and the putative limitations of data generated by citizen science projects. The outreach planning of citizen science projects is also evaluated, including the use of dedicated web platforms vs. pre-existent and disseminated web platforms, while discussing how such outreach actions can be maximized. Lastly, we present a framework that contextualizes the contributions of citizen science, scientific research, and regional and national stakeholders toward the integrated management of biological invasions.

Non‐native Fishes in Estuaries

Chapter

Mar 2022

Non‐native fishes are part of estuarine ecosystems worldwide, but especially in temperate regions. In some estuaries, entirely new assemblages of native and non‐native fishes with global origins have arisen. Major findings include: (i) large temperate estuaries heavily modified by human activity are most likely to support non‐native fishes; (ii) most successful non‐native fishes are euryhaline; (iii) there are no taxonomic restrictions as to which euryhaline fish species can invade estuaries as long as they have means and opportunity; (iv) few non‐native fishes have demonstrably done harm to estuarine ecosystems or fish assemblages; (v) most successful non‐native species eventually become naturalized and fit into local assemblages; (vi) most colonization events are not successful. Many estuaries have been modified so thoroughly and rapidly that they are increasingly inhospitable to both native and naturalized species, as demonstrated by the San Francisco Estuary.

Low-Cost Citizen Science Effectively Monitors the Rapid Expansion of a Marine Invasive Species

Article

Full-text available

Nov 2021

Citizen science and informed citizens have become fundamental in providing the first records and accounts about the expansion of numerous non-indigenous species. However, implementing a successful citizen science campaign can be expensive and particularly difficult for aquatic species. Here, we demonstrate how a low-cost citizen science campaign and its outreach plan in social and traditional media enabled to track the expansion of the Atlantic blue crab Callinectes sapidus Rathbun, 1896 along the coast of Algarve (southern Portugal, Europe). We describe the outreach strategy and a cost-benefit analysis of the first year of the citizen science campaign. Social media platforms allowed us to reach a significant number of citizens (over 31,500 clicks in Facebook publications), while traditional media gave national visibility to the citizen science campaign and biological invasions. In only 1 year, we documented the spread of the invasive Atlantic blue crab across the entire 140 km of the Algarve coast with 166 valid observations referring to 1747 specimens, submitted by 62 citizen scientists. We spent 0 € on the citizen science campaign, but considering the time invested in the campaign the cost would have summed up to 3,751 €, while the total minimum cost for one scientist to go to the field and retrieve the equivalent information would have exceeded 11,000 €. We used free online tools of communication to obtain the records about the Atlantic blue crab, instead of a dedicated web platform or mobile app, and handled social media accounts ourselves, which saved us at least 18,815 €. The citizen science campaign revealed that the Atlantic blue crab is unequivocally established in southern Portugal and that females appear to exhibit summer migrations to coastal areas to spawn as in the native area. Overall, our low-cost citizen science campaign effectively documented the rapid spread of a marine invasive species while providing some insights into its ecology. Our strategy can be easily replicated and implemented elsewhere in the world to tackle the ever-growing problem of biological invasions while increasing the scientific literacy of local populations.

What’s for Dinner? Assessing the Value of an Edible Invasive Species and Outreach Actions to Promote Its Consumption

Article

Full-text available

Mar 2022
BIOL INVASIONS

The consumption of edible aquatic invasive species has gained popularity as a means to minimize their impacts while easing pressure on native resources and ecosystems. Weakfish Cynoscion regalis (Bloch & Schneider, 1801) is one of the most recent invasive fish species in the Iberian Peninsula (Europe) which once sustained an important fishery in the native range (Northwest Atlantic Ocean). Portugal ranks third in the list of the world’s fish consumers, so promoting a weakfish fishery could at least minimize the impacts upon native species, since weakfish have innate traits that are appreciated by Portuguese fish consumers. However, introducing a new species to consumers is challenging owing to consumers’ habits and unfamiliarity with the species. So, we aimed to (i) evaluate the acceptance of weakfish by a panel of Portuguese fish consumers and (ii) create outreach actions—partnerships with local Chefs and press releases—to explain to a broader audience what invasive species are and promote the consumption of edible aquatic invasive species. We conducted a consumers survey that showed that weakfish has great chances of being well accepted by Portuguese fish consumers– 90% would buy weakfish because they appreciated its appearance, flavor, and texture, besides being a wild fish. The outreach actions reached a few million people because 46 online articles were published, and three news pieces were broadcasted on national television. Our strategy increased the public’s awareness about weakfish as an invasive species, which could be adapted for other non-indigenous marine species elsewhere in the world.

Undetected non-indigenous species in the Sado estuary (Portugal), a coastal system under the pressure of multiple vectors of introduction

Article

Full-text available

Sep 2023
J Coast Conservat

Research effort concerning biological invasions has increased significantly but the pressure of multiple vectors of introduction (MVI) on coastal areas is still poorly understood. The aim of this work is to provide a comprehensive list of non-indigenous species (NIS) occurring in the Sado estuary, identify and prioritize MVI to deliver recommendations for bioinvasions management. Fouling communities were sampled in five artificial systems during 2021 and 2022. Additionally, a thorough literature review was performed to provide a comprehensive NIS database for the Sado estuary. Native distribution of NIS was classified based on biogeographic realms and the most likely pathways and vectors of introduction were assigned to each introduction. A total of 52 NIS were catalogued, predominantly arthropods, 22% of which were reported until 2005, while 40% were recorded in the last 2 years. We also reported four new NIS to Portugal. Most NIS were native from the Temperate Northern Pacific and the Temperate Northern Atlantic. Shipping related vectors were dominant (61%). Aquaculture was not directly linked to many invasions (8%), however contaminants on animals was the second most significant vector (23%). Our results highlight the need for managing MVI in locations that may act as invasion hotspots. Additionally, it provides support for future policy and management measures by identifying areas that are vulnerable to biological invasions. The introduction of NIS is an important driver of changes on biodiversity, and it should be included as a key element for the creation of an integrated management tool for the Sado estuary.

Coastal Countercurrents Increase Propagule Pressure of an Aquatic Invasive Species to an Area Where Previous Introductions Failed

Article

Jun 2022
ESTUAR COAST

The establishment of many non-indigenous species is primarily controlled by propagule pressure, local environmental conditions, and biological interactions. An introduction is doomed to fail if any one of these factors is unsuitable. A few Atlantic blue crab Callinectes sapidus Rathbun, 1896 specimens have been collected along a limited stretch of the central Portuguese coast since the late 1970s, but a viable population was never detected. However, starting in 2016, a population of the Atlantic blue crab has established and expanded along the southern Portuguese coast. The objective of the present study was to provide insights into the invasion of the Atlantic blue crab in Portugal based on unpublished museum collection records and new records made by citizen scientists on the western coast and to provide a mechanistic explanation for the recent expansion based on observational oceanography data. Citizen science records along with observational oceanography data from 2019 and 2020 suggest that the southern Portugal population is expanding towards the western coast due to warmer coastal countercurrent events that form in the Gulf of Cadiz during the reproductive period of the Atlantic blue crab (summer–early fall). This oceanographic feature facilitates the transport of larvae towards the western coast of Portugal, which increases propagule pressure, while estuaries along the southwestern coast may serve as stepping stones supporting the northwards expansion of the species in tandem with increasing sea temperature. This study also highlights the value of citizen science in detecting the range expansion of invasive species over wide geographical areas.

Elm zigzag sawfly, Aproceros leucopoda (Hymenoptera: Argidae), recorded for the first time in North America through community science

Article

Full-text available

Sep 2021

The elm zigzag sawfly, Aproceros leucopoda Takeuchi (Hymenoptera: Argidae), was reported for the first time in North America during the summer of 2020. Characteristic zigzag defoliation was reported in the province of Québec, Canada, on the community science website, iNaturalist. Field trips conducted to the site resulted in the collection of live specimens (a few larvae and a cocoon from which an adult emerged) and onsite observation of diagnostic defoliation and empty cocoons, confirming the presence of this exotic species in Canada. Subsequent inspection of elm trees by naturalists and scientists in the south of the province led to the conclusion that the species is more widely distributed than first expected and that the invasion is not localised to a small area. Preliminary genetic data pointed to a possible European origin of the Canadian population, but conclusive assignment to source will require examination of more specimens and the collection of reference sequences from different European and Asian populations. This is a good example of the importance of community science in the detection of new invasive species.

Possible impacts of non-native plant, pathogen, invertebrate and fish taxa on the indigenous ichthyofauna in South African estuaries: a preliminary review

Article

Full-text available

Sep 2021
BIOL INVASIONS

We review the possible impacts of non-native biota on the indigenous fishes of South African estuaries, including macrophytes, algae, pathogens, invertebrates, and fishes. Freshwater macrophytes are one of the primary non-native groups in the oligohaline reaches of some predominantly open estuaries, lake and river mouth type estuaries, as well as the entire area of certain low salinity, temporarily closed estuaries. Anoxia and hypoxia in the water column below Salvinia molesta and Pontederia crassipes floating mats have caused fish kills in certain temporarily closed estuaries. Mass mortalities of fish in estuaries have arisen from harmful algal blooms (HABs) and a catchment-derived pathogenic water mould, Aphanomyces invadans. Non-native invertebrate species in local estuaries are derived from freshwater, estuarine and marine sources. The freshwater gastropod Tarebia granifera has invaded many subtropical estuaries and may be negatively impacting their food webs, with estuarine zoobenthivorous fishes not appearing to consume this mollusc. The marine polychaete Ficopomatus enigmaticus has invaded many South African estuaries and, in some of them, changed the zoobenthic food web by encrusting on hard surfaces and filtering particulate matter from the water column. This species also does not appear to be eaten by zoobenthivorous fishes within these systems. No non-native marine or estuarine fish species have been recorded in South African estuaries but non-native freshwater fish species now occur in 25% of estuaries in the region. Degraded estuaries in particular are more vulnerable to colonisation by non-native and translocated fish species than unimpacted systems. During the 1990s, a fish survey of 191 estuaries revealed that only 0.04% of the catch comprised non-native or translocated species but this percentage has increased in many estuaries in recent decades. Non-native and translocated freshwater fish species have successfully colonised the oligohaline and mesohaline reaches of many systems and there may be an impact due to predation on the eggs and larvae of resident estuarine taxa and the recruitment success of catadromous and some estuarine-associated fish species. However, most non-native fishes have a limited tolerance for the salinity regimes found in the lower and middle reaches of many South African estuaries, with an even larger threat to the indigenous estuarine ichthyofauna coming from non-native plant, invertebrate and pathogen invaders. Based on this review, and other similar global studies, there is a developing paradigm that non-native invasions by fishes and other organisms into South African and global estuaries are driven primarily from freshwater taxa and not estuarine or marine species.

The impact of trammel nets as an MPA soft bottom monitoring method

Article

Full-text available

Sep 2020
ECOL INDIC

With the global increase of marine protected area (MPA) implementation, the need for monitoring and the evaluation of their effectiveness becomes ever more important. Currently there is a severe lack of information about the protection effects of soft-substrate ecosystems. While many different methods have been established for the monitoring of hard-substrate ecosystems, most of these minimally invasive methods prove ineffective for soft- bottom habitats. Information and quantification of the impact of monitoring methods is needed to provide decision makers with the necessary knowledge to choose appropriate and feasible monitoring methods. In this study we quantify the impact of experimental trammel net fishing as a monitoring method of the soft-substrate demersal fish community using the Arrábida MPA (Portugal) as a case study. Over the 14 biannual sampling campaigns (between 2010 and 2019) 21,873 individuals and 5.61 tonnes of fish were caught. The gear is highly effective with an average catch per unit effort higher than reported for commercial fisheries in adjacent areas. When excluding the pelagic species, mortality rates are 41.2% and 30.4% in numbers and biomass, respectively. Most of the dead individuals belong to small, non-protected species with relatively little commercial value while MPA conservation target groups such as Soleidae and Rajidae have high survival rates. Due to its low size- and species-selectivity and the high survival rate of protected valuable species, the trammel net experimental fishing proved to be an effective monitoring method for soft-substrate demersal fish communities. Given their relatively low impact on the local ecosystem experimental trammel nets are a good alternative for areas where non-extractive methods are not effective. Nevertheless, quantification of the impact of other monitoring methods is necessary to enable the determination of the methods with the lowest mortality and impact for future soft-substrate MPA monitoring.

CHECKLIST OF THE FISHES AND FISH-LIKE VERTEBRATES ON THE EUROPEAN CONTINENT AND ADJACENT SEAS. Bull. Lampetra (2009): 109-179

Article

Full-text available

Jan 2009

Age determination in meagre Argyrosomus regius

Article

Full-text available

Jan 2009

Too big to be noticed: Cryptic invasion of Asian camel crickets in North American houses

Article

Full-text available

Sep 2014

Despite the rapid expansion of the built environment, we know little about the biology of species living in human-constructed habitats. Camel crickets (Rhaphidophoridae) are commonly observed in North American houses and include a range of native taxa as well as the Asian Diestrammena asynamora (Adelung), a species occasionally reported from houses though considered to be established only in greenhouses. We launched a continental-scale citizen science campaign to better understand the relative distributions and frequency of native and nonnative camel crickets in human homes across North America. Participants contributed survey data about the presence or absence of camel crickets in homes, as well as photographs and specimens of camel crickets allowing us to identify the major genera and/or species in and around houses. Together, these data offer insight into the geographical distribution of camel crickets as a presence in homes, as well as the relative frequency and distribution of native and nonnative camel crickets encountered in houses. In so doing, we show that the exotic Diestrammena asynamora not only has become a common presence in eastern houses, but is found in these environments far more frequently than native camel crickets. Supplemental pitfall trapping along transects in 10 urban yards in Raleigh, NC revealed that D. asynamora can be extremely abundant locally around some homes, with as many as 52 individuals collected from pitfalls in a single yard over two days of sampling. The number of D. asynamora individuals present in a trap was negatively correlated with the trap's distance from a house, suggesting that these insects may be preferentially associated with houses but also are present outside. In addition, we report the establishment in the northeastern United States of a second exotic species, putatively Diestrammena japanica Blatchley, which was previously undocumented in the literature. Our results offer new insight into the relative frequency and distribution of camel crickets living in human homes, and emphasize the importance of the built environment as habitat for two little-known invading species of Orthoptera.

The Role of Citizens in Detecting and Responding to a Rapid Marine Invasion

Article

Full-text available

Jul 2014

Documenting and responding to species invasions requires innovative strategies that account for ecological and societal complexities. We used the recent expansion of Indo-Pacific lionfish (Pterois volitans/miles) throughout northern Gulf of Mexico coastal waters to evaluate the role of stakeholders in documenting and responding to a rapid marine invasion. We coupled an online survey of spearfishers and citizen science monitoring programs with traditional fishery-independent data sources and found that citizen observations documented lionfish 1-2 years earlier and more frequently than traditional reef fish monitoring programs. Citizen observations first documented lionfish in 2010 followed by rapid expansion and proliferation in 2011 (+ 367%). From the survey of spearfishers, we determined that diving experience and personal observations of lionfish strongly influenced perceived impacts, and these perceptions were powerful predictors of support for initiatives. Our study demonstrates the value of engaging citizens for assessing and responding to large-scale and time-sensitive conservation problems.This article is protected by copyright. All rights reserved.

Release from Parasites as Natural Enemies: Increased Performance of a Globally Introduced Marine Crab

Article

Full-text available

Dec 2001

Introduced species often seem to perform better than conspecifics in their native range. This is apparent in the high densities they may achieve or the larger individual sizes they attain. A prominent hypothesis explaining the success of introduced terrestrial species is that they are typically free of or are less affected by the natural enemies (competitors, predators, and parasites) they encounter in their introduced range compared to their native range. To test this hypothesis in a marine system, we conducted a global assessment of the effect of parasitism and predation on the ecological performance of European green crab populations. In Europe, where the green crab is native, crab body size and biomass were negatively associated with the prevalence of parasitic castrators. When we compared native crab populations with those from introduced regions, limb loss (an estimator of predation) was not significantly lower in introduced regions, parasites infected introduced populations substantially less and crabs in introduced regions were larger and exhibited a greater biomass. Our results are consistent with the general prediction that introduced species suffer less from parasites compared to populations where they are native. This may partly explain why the green crab is such a successful invader and, subsequently, why it is a pest in so many places.

Reproductive strategy and fecundity of meagre Argyrosomus regius Asso, 1801 (Pisces: Sciaenidae): Implications for restocking programs

Article

Full-text available

Mar 2013
SCI MAR

Because the meagre (Argyrosomus regius) is not currently found around the Balearic Islands (western Mediterranean), the Balearic government is carrying out a restocking programme to recover its population. The success of this programme is critically dependent on improved knowledge of the meagre’s life cycle, and particularly its reproductive biology. Data on key reproductive parameters based on both reared and wild specimens are reported here. Histological examinations and gonadosomatic indices from 342 reared specimens demonstrated that 1) the potential reproductive season ranged from April to June and peaked in May, and 2) length at maturity (L50) was 49.3 cm for males and 57.2 cm for females, age at maturity (A50) was 2.7 years for males and 3.5 years for females, and weight at maturity (W50) was 1396 g for males and 1892 g for females. Histological examinations of 37 wild fish from Cádiz (SW Spain) demonstrated that the meagre has determinate fecundity. The annual potential fecundity of reared females ranged from 0.9 to 4.2 million oocytes, which is exponentially dependent upon female size.

Reproduction and Control of Ovulation, Spermiation and Spawning in Cultured Fish

Chapter

Full-text available

Jan 2009

Fish are the largest phylum of living vertebrates, with around 30,000 fish species out of approximately 50,000 vertebrate species (www.fishbase.com) [1]. Fishes inhabit almost every aquatic environment on the planet, presenting an enormous variation in temperature, salinity, oxygen, and other chemical and physical water properties. These environments have exerted evolutionary pressures that have resulted in the evolution of the enormous number of fishes and an immense variety of reproductive strategies. Fish exhibit various types of sex determination, from genetic to environmental control, sex differentiation from hermaphroditism to gonochorism, age of puberty, from a few months to many years, fecundity, from a few to millions of eggs, internal or external fertilization, a wide range of egg sizes, some that float and others that sink or stick to substrates, uncared eggs scattered into the environment to parental care of eggs to live “birth” (ovoviviparity) [2-4]. The existence of these diverse reproductive strategies has important implications for finfish culture and broodstock management. Finfish culture is the fastest growing food production industry in the world, and in 2005 a total of 28.3 million T of finfish were produced, which is around 20% of the world’s fisheries production (aquaculture and capture fisheries) [5]. The number of species being cultured is also increasing rapidly, and 67 different cultured finfish species in 2005 had an annual production of over 10,000 T, which is twice the amount produced by the 28 species being cultured in 1980 [6]. One of the most important aspects at the basis of this continuing increase in the number of cultured species is our growing understanding of the complexities of the many different reproductive strategies of various fishes and how these behave in captivity. This is perhaps best demonstrated by the development of the culture of the catfishes (Pangasius ssp) in Vietnam. These catfishes do not mature in captivity, but during the 1990s hormone stimulation techniques were developed to induce ovulation/spermiation. This technology gave the control required to produce eggs, larvae and juveniles that formed the basis of an expanding aquaculture industry, producing 40,000 T in 1997 and 376,000 T in 2005 [6]. This chapter aims at giving a general vision of fish reproduction and the reproductive dysfunctions found in captive-reared fishes, and describe how this knowledge is used to develop treatments for the control of fish reproduction in aquaculture. This general view will be covered under four broad areas relevant to the control of gonad maturation and spawning of fish in captivity. First, it will be described the normal gonadal development as can be expected under optimal (natural) conditions, particularly the morphology of gonad development and its endocrine and environmental regulatory mechanisms. Second, the reproductive dysfunctions that are observed in fish held in captivity; often the captive environment does not provide the environmental conditions that a species requires to complete maturation. Third, the available techniques for the stimulation of ovulation and spermiation, both environmental manipulations and hormonal treatments of reproductively dysfunctional fish held in captivity. Finally, the last sections will describe the application of adequate broodstock management protocols and hormonal therapies for the stimulation of fish reproduction in captivity for some of the main food fish species under production, both as a reference and indication of the possible strategies available to stimulate ovulation and spermiation in species considered candidates for new aquaculture developments.

Fishes of the St. Johns River, Florida

Article