The ready availability of abundant food sources can be a key factor in the success of biological invasions. This study provides information about feeding habits, dietary niche, and seasonal and ontogenetic diet changes of the American invasive weakfish Cynoscion regalis in the Gulf of Cádiz, where its population is increasing exponentially since 2011 when its presence was reported in the area. By content analysis of 340 stomachs, we assessed the diet composition, prey diversity and abundance of juveniles and adults present in the Guadalquivir River Estuary. Fish and crustaceans accounted for more than 90% of their diet. Mysids are the main food intake for juveniles and piscivory becomes more important as C. regalis grows in size. Stomachs were significantly fuller during the summer and autumn months, coinciding with the higher abundance of small pelagic fish during that time in the estuary, especially the anchovy Engraulis encrasicolus, the main prey consumed through all months of the year, that showed a consumption peak in September and October. Adults also show significant monthly variations in the diet composition (P < 0.01) respect to Total Length. Juveniles show a specialist behaviour feeding almost exclusively on Mesopodopsis slabberi, while adults show a mixed feeding strategy. This research constitutes a comprehensive study of weakfish diet along the year in the non-native area, including for the first time, juvenile’s stages.
Research Article
Abundant feasts: Favoring the invasion of an American fish species in Europe
https://doi.org/10.21203/rs.3.rs-3882111/v1
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Feeding habits
Gulf of Cádiz
invasive species
stomach content analysis
weakfish
Abundant food resources can play a significant role in facilitating the success of invasive species in new environments (Byers 2000). When an exotic species enters a new ecosystem, having access to a readily available and plentiful food source favours reproduction and out competition with native species for these resources, being able to become invasive if they have traits that allow them to exploit those resources.
The Gulf of Cadiz, located along the southwestern coast of Europe, is a highly productive marine ecosystem (Torres et al. 2013). Its productivity is closely linked to the long-term productivity of the Guadalquivir Estuary, which is one of the most significant contributors of nutrients and juvenile rearing to the Gulf's ecological richness (González-Ortegón et al. 2015; De Carvalho-Souza et al. 2019). This coupled ecosystem is a clear proof of productivity which plays a vital role in sustaining marine life, supporting local economies (Carvalho-Souza et al. 2019). The ready availability of abundant food sources can be a key factor in the success of biological invasions, in a vulnerable area to the introductions of non-native species due to the high volume of shipping, rising seawater temperatures and extensive anthropogenic changes (González-Ortegón et al. 2010, 2020).
In recent years several non-native species have been identified in Europe, including the American weakfish Cynoscion regalis (Bloch and Schneider, 1801) (Béarez et al. 2016; Bañón et al. 2017), a sciaenid fish native to the east coast of North America. The presence of C. regalis was first documented outside of its native range in the Schelde estuary in Belgiumin 2009 (Agentschap voor Natuur en Bos 2011) and later in the Gulf of Cádiz in 2011 (Béarez et al. 2016; Bañón et al. 2017). Since then, it has been reported in various locations along the Iberian Peninsula such as the Guadiana River, the Sado Estuary, the Tagus Estuary and the central-west coast of Portugal (Béarez et al. 2016; Morais and Teodósio 2016; Bañón et al. 2017; Gomes et al. 2017), and in the north of the Iberian Peninsula in Galician waters (Bañón et al. 2018). In Europe, and specifically in Iberian waters of the Gulf of Cádiz, the weakfish has become one of the most successful introduced fish species (Oliva-Paterna et al. 2020), with a well-established population (Bañón et al. 2017), and an exponential rise of landings since 2015. Currently, catches have increased from 1.3 tonnes in 2016 to a total of 75 tonnes in 2023 (as registered in the regional fish captures database (IDAPES 2023)) especially at Chipiona and Sanlúcar de Barrameda fishing harbors (Cádiz) where most of the landings occur (Fig. 1). Paradoxically, East coast of North America native populations(Lowerre-Barbieri et al. 1996; McEachran and Fechhelm 2010; Willis et al. 2015) have been declining since the 1990s(ASMFC 2016, 2019) to the extent of being classified as Endangered (EN) and currently included in the Red List of the International Union for Conservation of Nature (Barbieri and Barbieri 2020; IUCN 2023).
The American weakfish is a demersal fish species that inhabits shallow coastal waters, but highly dependent on estuaries for food, shelter spawning and breeding (Mercer 1989; Boutin 2008; Turnure et al. 2014; Boutin and Targett 2019;). In the Gulf of Cádiz, the Guadalquivir River Estuary is the main feeding and nursery area for the early life stages of many marine species with commercial interest (Fernández-Delgado et al. 2007; González-Ortegón et al. 2012). Juveniles and larvae of the weakfish were detected for the first time in August 2019 in the Guadalquivir Estuary by the Guadalquivir Long-Term Ecological Research (GUADALQUIVIR-LTER 2023) monitoring program (1997–2023). This first record of a juvenile weakfish in the Iberian Peninsula were individuals ranging from 38 to 64 mm total length (TL). Since then, it is not unusual to find them as part of the fauna sampled in that area, especially in summer and autumn.
Although the introduction of a new non-native species into an ecosystem does not necessarily implies a negative impact - only about 10% of marine exotic (non-native) species are pointed out as invasive (Anton et al. 2019) - there is indeed, a widespread fear among scientists and society in general that these invasions and following new species establishment will cause dramatic consequences, alter invaded ecosystems and declines in native populations (Coll et al. 2007; Costello et al. 2010; Bianchi et al. 2012;). Food webs can be restructured, leading to changes in the ecosystem function, productivity and degradation of ecosystem goods and services (Clavel et al. 2011; Gallardo et al. 2016). Feeding ecology studies are particularly relevant in this field, as determining the diet and feeding habits is crucial for predicting how non-native species will affect the food webs of receiving systems (Brandner et al. 2013; Garvey and Whiles 2017).
If a recent organism has access to a significant amount of food resources in its new environment, then it is more likely to experience greater success in terms of survival, reproduction, and long-term persistence in that ecosystem. This work aims to explore whether the success of the introduction of the American weakfish may be related to the high abundance of prey species, such as the abundant small pelagic fish in the Gulf of Cádiz.
In its native area, C. regalis shows a generalist feeding strategy, with occasional opportunistic behaviour on a wide variety of prey (Merriner 1975; Willis et al. 2015). It shows ontogenetic dietary shifts (Nemerson and Able 2004; Deary 2015; Willis et al. 2015), with mysid shrimps dominating the diet of juvenile weakfish (Thomas 1971; Chao and Musick 1977; Boutin and Targett 2019), transitioning to piscivory as they grow older, but also feeding on a lesser extent on crustaceans, polychaetes, molluscs, shrimp, squid and other estuarine preys (Merriner 1975; Nemerson 2001; Litvin and Weinstein 2004; Able and Fahay 2010; Willis et al. 2015).
Weakfish has been well studied in its native area as an important commercial and recreational fishing resource, but little is known about how it behaves in the newly invaded areas. A first study examining the diet of weakfish along the Portuguese coast, (Cerveira et al. 2021), although limited in time and the number of individuals analysed, confirmed that weakfish also shows a generalist feeding strategy, being likely one of the many reasons for its invasiveness.
Our study aims to provide a comprehensive overview of the feeding habits, dietary niche, and seasonal and ontogenetic dietary changes. This information is essential to comprehend the success of the invasive weakfish in the Gulf of Cádiz, its ecological role in this new ecosystem for the species and provide relevant information for future management measures of this species.
Study area
The present study was carried out in the Gulf of Cádiz and the Guadalquivir River Estuary (Fig. 2), currently the main area of establishment and invasion of weakfish in Europe (Bañón et al. 2018).The Gulf of Cádiz (Atlantic Ocean) is strongly influenced by the Guadalquivir Estuary outflow and a high biological production and fisheries (De Carvalho-Souza et al. 2019). This estuary is recognized as a key nursery area for many marine species (Baldo and Drake 2002; González-Ortegón et al. 2015; De Carvalho-Souza et al. 2019), with the weakfish being added to this list of marine species in the last four years.
Field methods
Adult fish individuals were collected monthly from local fishermen captures from March 2021 to April 2022. A total of 340 adult weakfish (TL > 18 cm) were sampled from the fishing fleet landings operating in the Gulf of Cádiz, mainly within the coastal waters surrounding the Guadalquivir River mouth. Fish were obtained from the fish markets of Chipiona and Sanlúcar de Barrameda (Cádiz) (Fig. 2). Main fishing gears used were trammel nets anchored at low depths along the coast and bottom trawls, which usually operate at greater depths. Fish from different boats and consecutive days in a week were pooled in order to get the closest possible to 60 individuals per month. Once captured, fish were transferred in ice to the laboratory within the next 24h after the capture.
Juveniles were collected monthly by GUADALQUIVIR-LTER team from a traditional river fishing boat with a 1 mm mesh net at a standstill in 2 different locations: Bonanza and Tarfía (as described inGonzález-Ortegón et al. (2015)) (Fig. 2). Historical stored samples were reviewed to identify juvenile C. regalis specimens that might have been mixed up with other species or misidentified. A total of 26 specimens were found in August and September 2019, October 2020 and June 2022. Fish were preserved in 4% formaldehyde and remained in these conditions until the moment of dissection in the laboratory. From now on we will refer to these 2 different sets of samples as adults and juveniles.
Stomach content analysis
All specimens were sexed, measured (Total Length, TL, and Standard Length, SL, ± 1 mm) and weighed (Total Weight, TW, and Gutted Weight, GW, ± 1 g). Guts were extracted, weighed and stored for different analysis. Stomachs contents (excluding the intestinal tract) were examined by binocular microscopes and preys identified using different manuals and books (Zariquiey Alvarez 1968; Drake and Arias 1990; Ballesteros and Llobet 2015) to the lowest taxonomic level possible. Hard structures such as otoliths or scales were used to identify the prey groups (Categories) and, in some cases, species were identified by the otoliths shape using an otoliths atlas (Tuset et al. 2008). All prey were counted, measured and weighed if allowed by the level of digestion. Preys were classified into 9 main categories: bivalves, cephalopods, crustacean, echinoids, fish, gastropods, polychaetes, scyphozoans and vegetal. In some cases, prey items could only be identified at the group level due to high degree of digestion and labeled as 'unknown' as the species level. These items were initially included in the analysis under broader categories but excluded when conducting species-specific analysis.
For each prey, a percentage of relative presence (%RP) in each stomach was assigned during the visual assessment of the stomach contents. Each stomach was assigned a total percentage of 100% and portions of this percentage were assigned to the different preys according to their estimated contribution to the stomach volume (Hynes 1950; Amundsen and Sánchez-Hernández). Percentage of the total number of prey items (%N) was also used to express the dietary composition, which is the percentage that a particular prey species or group represents of the total number of prey items found (Hynes 1950; Amundsen and Sánchez-Hernández 2019). Frequency of occurrence (%F) of each prey item was calculated as the percentage of stomachs containing food in which a given prey item occurred (Hynes 1950; Hyslop 1980; Amundsen and Sánchez-Hernández 2019). When expressing all these indices by category, we considered prey items that were identified up to category level, while when expressing them by prey species, we only consider preys items that were identified up to species level, thus excluding unidentified fish or crustaceans.
Stomach fullness index was used according to Garrido et al. (2008) and AFSC (2015) ranging from 1 to 9 (where: 1: empty, 2: traces-25%, 3: 25%, 4: 25–50%, 5: 50%, 6: 50–75%, 7: 75%, 8: 75–100%, 9: 100% distended).
Costello (1990) diagram modified by Amundsen was used to assess the feeding behavior of weakfish, by plotting the percentage of occurrence against the prey-specific abundance of each prey taxon (Costello 1990; Amundsen et al. 1996), where:
Percentage of occurrence: \({F}_{i}=\left(\frac{{N}_{i}}{N}\right)\), where Ni is the number of predators with prey i in their stomach and N is the total number of predators with stomach contents.
Prey-specific abundance in terms of relative presence (%RP): \({P}_{i}=\left(\frac{\sum {S}_{i}}{\sum {S}_{ti}}\right)x100\), where Pi is the prey-specific abundance of prey i, Si is the stomach content comprised of prey I, and Sti is the total stomach content in only those predators with prey i in their stomachs.
Data analysis
Diet of weakfish was analyzed using a multivariate approach with the statistical software PRIMER 7 version 7.0.21 (Clarke and Gorley 2006) with PERMANOVA + (Anderson et al. 2008). Preys were grouped by category or species and a multivariate data analysis was carried out by non-metric multidimensional scaling (MDS) ordination with the Bray-Curtis similarity measurement for diet composition (Clarke and Gorley 2006). Pairwise Bray–Curtis similarity coefficients were calculated for the %RP and %N of prey items, which provide a rough measure of dietary overlap of intra-specific differences (see (González-Ortegón et al. 2010). Main prey categories and the percent contribution of each prey item responsible for similarity and dissimilarity in each considered group were identified using SIMPER (Clarke and Warwick 2001). One-way ANOSIM permutation test was used to assess if diet composition differences between adults and juveniles were statistically significant. In addition, PERMANOVA analysis were carried out to evaluate adults’ differences in stomach contents (using weakfish total length) and to detect significant differences on the interactions between months/seasons, sex and total length. The biodiversity indexes species richness (S) and Shannon-Wiener (H´) were calculated.
Adults population
The adult weakfish sampled consisted of 340 individuals, with 53.53% females, 43.24% males, and only 3.24% undetermined. Individual sizes ranged from 19.8 to 54 cm (TL) and 78.82 to 1412.64 g (TW), with 60% of the population falling between 25 and 35 cm (TL). Only one individual smaller than 20 cm (TL) was sampled, while two were larger than 50 cm (TL). Larger individuals over 40 cm were mostly females (78%). Of the 340 stomachs analyzed, 228 contained food (67.1%) while 112 remained empty (32.9%). Relative index of stomach fullness showed that half (53.51%) of the stomachs containing food belonged to the category 2 while only 10.09% fell into category 9. The average number of prey items consumed by weakfish was 2.88 prey items per individual, with a higher number of prey items per stomach during the summer months compared to the rest of the year.
Fish and crustaceans were the two main groups consumed by C. regalis both in terms of number (52.05% and 42.01% respectively) and relative presence (73.80% and 19.95% respectively), indicating that these two groups represented more than 90% of the diet. Frequency of occurrence was 79.59% for fish and 34.69% for crustaceans.
The relative presence of fish in the diet was always above 59%, regardless of the season. Other prey groups found in the stomachs were bivalves, polychaetes, cephalopods, echinoderms, gastropods and scyphozoans. The European anchovy (Engraulis encrasicolus) and Processa sp. were the most abundant prey in each group, representing 75.51% and 47.25% of the total relative presence of preys in each group, respectively (Table 1).
Table 1. Groups and identified prey species found in the stomach content from adults and juveniles of C. regalis. Results of different indexes (Numerical percentage (N%), relative presence percentage (%RP) and frequency of occurrence percentage (F%) are shown for each prey group and identified prey species by season. For juveniles, no season differentiation is made.
Prey species vary according to the seasons, but only 3 species are always present: Processa sp., E. encrasicolus and Aphia minuta. In all seasons, the consumption of crustaceans and fish was always the main food intake, showing in spring a bigger variability of preys consumed (Table 1). This is also shown by the biodiversity indices (S and H´), where there is a greater diversity of preys in spring (1.30 and 0.18 respectively) as they all present higher values compared to summer (1.24 and 0.11), autumn (1.19 and 0.09) and winter (1.19 and 0.11) (S and H´ respectively).
E. encrasicolus is the main prey found in the stomachs, both in terms of %RP and %N (Table 1). It shows a temporal variability, being consumed in lower amounts in the winter months and towards early spring, progressively increasing towards summer and early Autumn, reaching the highest values in September and October (Fig. 3).
The Amundsen et al. (1996) approach to evaluate dietary composition shows that the adult weakfish population mainly exhibits a specialist feeding strategy while in few cases predators exhibit a more generalist behavior (preys located in the lower half of the diagram). The preferred prey chosen by each individual differs in some cases. The diagram reveals that the prey that we find located closer to the top right corner, is the most dominant prey, E. encrasicolus. Preys located closer to the 0 on the x-axis indicate preys consumed by rare predators and are not common preys chosen by the population but by individual predators instead (individual specialization). In this case, the population exhibits a broad niche width and a high inter-phenotype component, indicating that various predators will specialize in different prey species (Fig. 4).
PERMANOVA test to assess differences in the diet composition of the weakfish along the size range (TL) revealed that there were significant differences (p < 0.05) with size, between months and sex. Having an effect on the diet composition in both cases, using the %RP and N values and grouping the preys at group level or species level (Table 2). When examining the size relationship between weakfish predator and the number anchovies (the most abundant prey) in the stomach contents, a positive but weak relationship was found (r = 0.24).
|
Preys identified at group level |
||||||||
|---|---|---|---|---|---|---|---|---|
|
%RP |
N |
|||||||
|
Factor |
df |
MS |
Pseudo-F |
p(MC) |
MS |
Pseudo-F |
p(MC) |
|
|
Total Lenght |
1 |
16976.0 |
12.279 |
0.0003* |
16759.0 |
10.297 |
0.0001* |
|
|
Month |
11 |
5165.4 |
37.363 |
0.0001* |
5873.7 |
36.091 |
0.0001* |
|
|
Sex |
1 |
1438.5 |
10.405 |
0.3225 |
2396.1 |
14.723 |
0.2055 |
|
|
Month x Sex |
10 |
2589.3 |
18.729 |
0.0208 |
3422.5 |
2.103 |
0.0012 |
|
|
Res |
194 |
1382.5 |
1627.5 |
|||||
|
Total |
217 |
|||||||
|
Preys identified at species level |
||||||||
|
%RP |
N |
|||||||
|
Factor |
df |
MS |
Pseudo-F |
p(MC) |
MS |
Pseudo-F |
p(MC) |
|
|
Total Lenght |
1 |
6619.5 |
19.822 |
0.0459 |
6668.8 |
20.084 |
0.0401 |
|
|
Month |
11 |
9062.0 |
27.136 |
0.0001* |
9671.8 |
29.128 |
0.0001* |
|
|
Sex |
1 |
2060.0 |
0.617 |
0.8071 |
1710.4 |
0.515 |
0.8995 |
|
|
Month x Sex |
9 |
3933.5 |
11.779 |
0.1497 |
4444.0 |
13.384 |
0.0329 |
|
|
Res |
90 |
3339.4 |
3320.4 |
|||||
|
Total |
112 |
|||||||
Stomach fullness of weakfish showed significant differences along the year on the different months. PERMANOVA test to assess differences in the fullness state along the size range (TL), sex and months revealed that size, sex and mainly months had significant effect (Table 3). The individuals caught between June and November (summer and autumn) had fuller stomachs than those captured between December and May (spring and winter) (Fig. 5).
Table 3. PERMANOVA and Pairwise test to evaluate the influence of sex and the time of the year (months) on the stomach fullness state on C. regalis. Data on the top-right triangle represent p-value, triangle in the bottom-left contains T-value data. Symbols: MS=mean squares of factors; p(MC) = Monte Carlo p-value. Significant terms p(MC) < 0.05 and p(MC) < 0.01 are highlighted in bold, p(MC) < 0.01 values are also identified by an asterisk.
Juveniles
A total of 26 juvenile weakfish from the Guadalquivir River Estuary were sampled, ranging from 2.4 to 8.4 cm in TL and 0.082 and 6.6 g in TW. Of the 26 stomachs analyzed only 1 of them was found empty. Among the 25 stomachs containing food, 48% were completely full (n = 12), while only 12% (n = 3) were filled up to 25% of the stomach capacity, the rest (n = 10) showed different degrees of fullness between 25–100%. The average number of preys consumed by juvenile weakfish was 9.92 prey items per individual.
The diet of juveniles was based on crustaceans and early stages of fish, showing a clear preference for crustaceans which made 94.33% of the preys consumed. More specifically the mysid Mesopodopsis slabberi constituted 99.57% of the preys (n = 230), with the exception of 1 individual of the shrimp Palaemon longirostris found. Relative presence showed that crustaceans constituted 77.37% of the diet, polychaetes 11.77%, and fish 10.86% (Table 1).
Juveniles show a very clear specialist behavior with M. slabberi as the dominant prey species (Fig. 4).
There were significant ontogenetic differences in the composition of the weakfish diet between adults and juveniles (r = 0.32, p = 0.001) when they cohabited during the months of autumn and summer.
After performing a SIMPER analysis, we found that the average similarity in the adult diet was 23.86%, of which E. encrasicolus contributed a 92.16% to it. For juveniles the similarities were greater (57.58%), with M. slabberi being the main contributor of this similarity (96.51%). Among the groups, adults and juveniles, the dissimilarity is 94.78%, with both E. encrasicolus and M. slabberi as the main preys contributing to these differences.
Biological invasions can lead to unpredictable effects in the recipient ecosystem, especially in the marine environment where ecosystems are highly connected across broad spatial scales (Giakoumi et al. 2019). One way to understand the ecological impacts and effects of these species is to investigate their diet composition. Based on our results, it is plausible that C. regalis invasive success is closely related to high prey abundance and similarity of physiological characteristics and life cycles between native and invaded areas.
Currently, there is a lack of information and studies in the invaded area. A preliminary study on C. regalis was carried out in the Guadiana estuary in June 2017, evaluating the diet of a limited number of individuals of homogeneous size (33 individuals between 27.2 and 60.0 cm TL) collected over a period of one month (Cerveira et al. 2021). Their results showed that C. regalis has a generalist feeding strategy, mainly based on a diversity of benthic crustacean and fish. In this study, it has a diet composed mainly of crustaceans and bony fishes, especially the anchovy E. encrasicolus, which was the dominant prey through all the year. In adult weakfish, fish appeared as prey in more than 76% of the stomachs, a value very similar to the one obtained in previous studies (63%) in its native area (Merriner 1975; Willis et al. 2015). In terms of volume, weakfish diet in Gulf of Cádiz is mainly based on fish and crustaceans, similar to diet described at its native area. There, the main food sources are bony fishes such as anchovies and herrings and crustaceans such as penaeids and mysid shrimps (Merriner 1975; Nemerson and Able 2004; Willis et al. 2015). Although cannibalism has been detected before (Cerveira et al. 2021; Merriner 1975) and this behaviour seems to be common in other Sciaenidae species (such as Argyrosomus regius), we did not detect any sign of cannibalism in our study. However, due to the high degree of degradation of some of the stomach contents analysed, some fish could not be identified. Therefore, we cannot exclude the possibility that some weakfish were among the preys.
Among adult main preys, E. encrasicolus was the dominant prey, followed by Sardina pilchardus and A. minuta, and Processa sp. as the main crustacean constituting the weakfish diet. Probably, the availability of abundant food sources in the Gulf of Cadiz, such as anchovies, is causing this American fish species to successfully invade southwestern Europe.
Monthly differences were found in stomach fullness, with stomachs being fuller in the summer and autumn months than in spring and winter. This could be due to the increase in food availability during the warm months as well as by a possible more active predation behaviour. The fact that the average number of prey items consumed is higher in summer than in other seasons is due to the higher intake of small crustaceans. The number of small crustaceans they need to eat to satisfy their dietary needs is much higher than when feeding on, for example, anchovies.
Estuarine species were common preys in the diet of weakfish in the Gulf of Cádiz in all seasons. The composition of the estuarine fauna in the Guadalquivir Estuary is mainly dominated by the anchovy E. encrasicolus and A. minuta in summer and winter, respectively (González-Ortegón et al. 2015), which explains the higher consumption of E. encrasicolus by weakfish during the months of August, September and October. The fact that the samples were collected close to the mouth of the Guadalquivir Estuary, may probably explain the presence of the species Processa sp., E. encrasicolus and A. minuta in their stomach contents in all seasons.
Our results confirm that weakfish is using the Guadalquivir River Estuary ecosystem as its nursery area. There are no previous studies of juvenile diet in the invaded areas, so this is the first assessment of juvenile diet outside of its native range. Juveniles weakfish collected inside the Guadalquivir Estuary behaved as specialists with a clear food preference for the mysid shrimp M. slabbery. Similar to the most abundant species of estuarine macrofauna and fish juveniles present in the Guadalquivir Estuary (Baldo and Drake 2002; Vilas et al. 2008; González-Ortegón et al. 2010). In addition, other three species were found in the juvenile stomachs in very small proportion: E. encrasicolus, Palaemon longirostris and the polychaeta Glycera sp. In the Guadalquivir estuary, E. encrasicolus and the white shrimp P. longirostris are the most dominant nektonic macrofauna species (González-Ortegón et al. 2006, 2010, 2015), so there is a high probability that these were more casual encounters rather than active predation by weakfish, as it can also be deducted from the Amundsen (1996) plot, in which these are part of rare preys identified.
Results of juveniles from the native area (Boutin and Targett 2019) were extracted from a study conducted along summer and autumn so data are comparable to our study. That is, fish and polychaeta were also part of the diet in the native area in smaller proportions than mysids (Boutin and Targett 2019). In another study, Merriner (1975) also stated that the principal food items of age 0 weakfish were shrimp and anchovy. If we compare our results to previous studies conducted in the native area, we can conclude that juveniles are also maintaining the same feeding behaviour, feeding on the same functional groups and on similar proportions.
The feeding strategy was characterized using the modified Costello (1990) diagram, showing that adult weakfish in the Gulf of Cádiz exhibit a mixed feeding strategy. This is consistent with the feeding strategy shown by weakfish in its native area (Willis et al. 2015). Outside of its native range, in Portuguese waters, the same feeding strategy has been observed (Cerveira et al. 2021). This strategy is not entirely effective in the Gulf of Cádiz compared to the native area, as the proportion of anchovies in adults or mysids in juveniles (which are the most abundant prey in the Gulf of Cádiz and the Guadalquivir Estuary) was very significant and there is a low diversity of prey. In addition, juveniles showed a very narrow diet, mainly preying on M. slabberi, with a much more specialized behavior in contrast to adults. This suggest that there is an ontogenetic shift in the diet, transitioning from crustaceans to fish as they grow, with the relative proportion of fish increasing together with the size. Adults consume mainly fish while juveniles prey mainly on crustaceans, present in 88% of the stomachs vs. 23% fish. Similar dietary shifts from crustaceans to fish are typical for other sciaenidae species(Griffiths 2011; Spitz et al. 2013; Hubans et al. 2017) and have been previously shown for the weakfish in its native area, where it feeds mainly on crustaceans, more specifically on the mysid shrimp Neomysis americana, transitioning to fish as it increases in size (Nemerson 2001; Litvin and Weinstein 2004). The fact that we found such clear differences in diet between the two groups: juveniles and adults and that we did not see a transition in the results as in other studies (Nemerson 2001; Litvin and Weinstein 2004; Boutin and Targett 2019), can be due to the lack of intermediate sizes of the sampled individuals. We did not have access to individuals in the size range between 8.4–19.8 cm which may explain the lack of sizes at which they go through the transition from predating almost exclusively on crustaceans to a diet based mainly on fish and crustaceans. Mysids consumption appears to be a key factor in driving the spatial dynamics of nursery productivity for juvenile weakfish (Boutin and Targett 2019). In any case, the fact that the weakfish is growing at the expense of the most abundant prey might be related to its invasive success in this area. Predation on relatively abundant preys throughout the year, including those that are part of the diet of similar native species (Baldo and Drake 2002; Torres et al. 2013), could explain the invasion success of C. regalis.
In recent years there has been concern about whether this new species will or has already caused damages on the populations of important commercially species in the area, and after evaluating its diet it would be logical to assume that the species most directly affected is E. encrasicolus, as it is the main prey of the weakfish across the year. As an invasive species, besides predation, weakfish can also compete for food with other local species that feed on the same preys such as A. regius, Dicentrarchus labrax or Dicentrarchus punctatus. Based on data from official landings in the Gulf of Cádiz, populations of A. regius have been declining since 2015, which coincides with the year in which weakfish began to appear in greater numbers and was included in official landings.
The counterparts species A. regius shows a generalist feeding strategy and a similar ontegenic diet shift: while small sizes (5–15 cm) prey mainly on small decapods (Crangon crangon) and mysids, bigger decapods as Processa sp. and fishes (E. encrasicholus y A. minuta) become main preys for A. regius > 15 cm (unpublished data: Alconchel 2006). Hence, based on high diet similarity, a strong resource competition between C. regalis and A. regius might be occurring in the area. In any case, further studies are needed to determine whether this depletion is related to the invasion of weakfish or whether it is a mere coincidence and the reason for this decrease is due to any other factor or population dynamics.
Realistically, eradication is unlikely for established invasive populations, and the aim of management is generally to reduce their populations to levels that have lower impacts that are considered acceptable (Usseglio et al. 2017). Although weakfish is already being exploited as a food resource it is not yet very known among the consumers or valued enough as other similar species (Nuñez et al. 2012). One of the only possible means to control the exponential growth of the population would be to increase the fishing pressure on this species and hope for a self-regulation and balanced integration into the ecosystem. It can also be a valuable resource for other multiple species that are struggling to survive in an over-exploited marine area and might find their resources limited. Since weakfish are the dominant prey of bottlenose dolphins Tursiops truncates in their native area (Gannon and Waples 2004), and bottlenose dolphins are common in the Gulf of Cádiz, they could play an important role in the ecosystem as top-down controllers (Coll et al. 2007; Giménez et al. 2017), controlling weakfish population in this area.
Weakfish is a well-established species in the Gulf of Cádiz, and the current population is growing exponentially, with catches around 60 times higher than in 2016. It feeds mainly on fish and crustaceans, being E. encrasicolus its main food resource in this area. It shows monthly variations in the diet, probably linked to the availability of resources in the Estuary. During juvenile stages, crustaceans are the main food resource, and as they grow in size, diets shift to fish as the main prey consumed. Understanding how the addition of this species to the ecosystem will affect it, is very important in order to make informed decisions. Probably, the availability of abundant food sources in the Gulf of Cádiz is causing American fish species to invade and establish themselves in European waters. This would explain the success that many other species have in their establishment and invasive characteristics.
Contributions
GG: Conceptualization, data collection, data curation, formal analysis, investigation, methodology, validation and writing original draft. CV: resources and supervision. FB: supervision. JAC: funding acquisition and resources. EGO: Conceptualization, formal analysis, methodology, funding acquisition, resources and supervision. All authors reviewed, edited and approved the final manuscript.
Acknowledgements
This work was carried out within the framework of the EcoInvadiz project (P18-RT-5010) funded by the regional government of Andalusia. The authors have declared that no competing interests exist. The authors would like to thank the fishermen from Chipiona and Sanlúcar de Barrameda for collaborating and providing the fish samples throughout the study.
- Able KW, Fahay MP (2010) Ecology of Estuarine Fishes: Temperate Waters of the Western North Atlantic. Johns Hopkins University Press, Baltimore, MD
- AFSC (2015) Resource Ecology and Ecosystem Modeling Stomach Content Analysis Procedures Manual | NOAA Fisheries. Seattle
- Agentschap voor Natuur en Bos (2011) DNA Ontmaskert de Verdachte. Infoblad Voor de Openbare Visserij in Vlaanderen. Jaargang 28:32
- Amundsen PA, Sánchez-Hernández J (2019) Feeding Studies Take Guts – Critical Review and Recommendations of Methods for Stomach Contents Analysis in Fish. J Fish Biol 95(6):1364–1373. https://doi.org/10.1111/jfb.14151
- Amundsen PA, Gabler HM, Staldvik FJ (1996) A New Approach to Graphical Analysis of Feeding Strategy from Stomach Contents Data—Modification of the Costello (1990) Method. J Fish Biol 48(4):607–614. https://doi.org/10.1111/j.1095-8649.1996.tb01455.x
- Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: Guide to Software and Statistical Methods
- Anton A, Geraldi NR, Lovelock CE, Apostolaki ET, Bennett S, Cebrian J, Krause-Jensen D, Marbà N, Martinetto P, Pandolfi JM, Santana-Garcon J, Duarte CM (2019) Global Ecological Impacts of Marine Exotic Species. Nat Ecol Evol 3(5 3):787–800. https://doi.org/10.1038/s41559-019-0851-0
- ASMFC (2016) Atlantic States Marine Fisheries Commission. Weakfish Benchmarsk Stock Assessment and Peer Review Report. District of Columbia, Washington
- ASMFC (2019) Atlantic States Marine Fisheries Commission. Weakfish Stock Assessment Update Report. Status of the Fishery Management Plan. District of Columbia, Washington
- Baldo F, Drake P (2002) A Multivariate Approach to the Feeding Habits of Small Fishes in the Guadalquivir Estuary. J Fish Biol 61(sa):21–32. https://doi.org/10.1111/J.1095-8649.2002.TB01758.X
- Ballesteros E, Llobet T (2015) Marine Wildlife of the Mediterranean. Gallocanta Ediciones
- Bañón R, Arias A, Arana D, Cuesta JA (2017) Identification of a Non-Native Cynoscion Species (Perciformes: Sciaenidae) from the Gulf of Cádiz (Southwestern Spain) and Data on Its Current Status. Scientia Mar 81(1):19–26. https://doi.org/10.3989/scimar.04494.21A
- Bañón R, Barros-García D, Gómez D, Berta-Ríos M, de Carlos A (2018) Evidence of a Rapid Colonization of the Atlantic European Waters by the Non-Native Weakfish Cynoscion Regalis (Perciformes: Sciaenidae). Marine Biodivers 48(4):2237–2242. https://doi.org/10.1007/s12526-017-0738-8
- Barbieri S, Barbieri L (2020) Cynoscion Regalis. The IUCN Red List of Threatened Species. https://www.iucnredlist.org/species/46104933/49226925. [Accessed on 21.04.2023]
- Béarez P, Gabriel S, Dettai A (2016) Unambiguous Identification of the Non-Indigenous Species Cynoscion Regalis (Sciaenidae) from Portugal. Cybium 40:245–248. https://doi.org/10.26028/cybium/2016-403-007
- Bianchi CN, Morri C, Chiantore M, Montefalcone M, Parravicini V, Rovere A (2012) Mediterranean Sea Biodiversity between the Legacy from the Past and a Future of Change. Life in the Mediterranean Sea: A Look at Habitat Changes. Nova Science Publishers, New York NY, USA 1–55
- Boutin BP (2008) Tidal Tributaries and Nearshore Areas as Nursery Habitat for Juvenile Sciaenid Fishes and Other Estuarine Nekton in Delaware Bay and the Delaware Coastal Bays. PHD Thesis. University of Delaware, Newark, DE
- Boutin BP, Targett T (2019) Density, Growth, Production, and Feeding Dynamics of Juvenile Weakfish (Cynoscion Regalis) in Delaware Bay and Salt Marsh Tributaries: Spatiotemporal Comparison of Nursery Habitat Quality. Estuaries Coasts 42(1):274–291. https://doi.org/10.1007/s12237-018-0457-9
- Brandner J, Auerswald K, Cerwenka AF, Schliewen UK, Geist J (2013) Comparative Feeding Ecology of Invasive Ponto-Caspian Gobies. Hydrobiologia 703(1):113–131. https://doi.org/10.1007/s10750-012-1349-9
- Byers JE (2000) Competition between Two Estuarine Snails: Implications for Invasions of Exotic Species. Ecology 81(5):1225–39. https://doi.org/10.1890/0012-9658(2000)081[1225:CBTESI]2.0.CO;2
- De Carvalho-Souza GF, González-Ortegón E, Baldó F, Vilas C, Drake P, Llope M (2019) Natural and Anthropogenic Effects on the Early Life Stages of European Anchovy in One of Its Essential Fish Habitats, the Guadalquivir Estuary. Mar Ecol Prog Ser 617–618:67–79. https://doi.org/10.3354/meps12562
- Cerveira I, Dias E, Baptista V, Teodósio MA, Morais P (2021) Invasive Fish Keeps Native Feeding Strategy despite High Niche Overlap with a Congener Species. Reg Stud Mar Sci 47:101969. https://doi.org/10.1016/j.rsma.2021.101969
- Chao LN, Musick JA (1977) Life-History, Feeding-Habits, And Functional-Morphology of Juvenile Sciaenid Fishes in York River Estuary, Virginia. Fish Bull 75(4):657
- Clarke KR, Gorley RN (2006) PRIMER v6. User Manual/Tutorial. PRIMER-E. Plymouth
- Clarke KR, Warwick RM (2001) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd Edition. Primer-E, Plymouth. Plymouth, United Kingdom: PRIMER-E 172
- Clavel J, Julliard R, Devictor V (2011) Worldwide Decline of Specialist Species: Toward a Global Functional Homogenization? Front Ecol Environ 9(4):222–228. https://doi.org/10.1890/080216
- Coll M, Santojanni A, Palomera I, Tudela S, Arneri E (2007) An Ecological Model of the Northern and Central Adriatic Sea: Analysis of Ecosystem Structure and Fishing Impacts. J Mar Syst 67(1–2):119–154. https://doi.org/10.1016/j.jmarsys.2006.10.002
- Costello MJ (1990) Predator Feeding Strategy and Prey Importance: A New Graphical Analysis. J Fish Biol 36(2):261–263. https://doi.org/10.1111/j.1095-8649.1990.tb05601.x
- Costello MJ, Coll M, Danovaro R, Halpin P, Ojaveer H, Miloslavich P (2010) A Census of Marine Biodiversity Knowledge, Resources, and Future Challenges. PLoS ONE 5(8):e12110. https://doi.org/10.1371/journal.pone.0012110
- Deary A (2015) Ontogeny of the Feeding Apparatus and Sensory Modalities: Relationship to Habitat Differentiation among Early Life History Stage Drums (Sciaenidae) in the Chesapeake Bay. PDH Thesis. Virginia Institute of Marine Science. https://dx.doi.org/doi:10.25773/v5-pry1-hx22
- Drake P, Arias AM (1990) Hábitos Alimentarios de Estados Juveniles de Peces En Los Caños de Las Salinas de La Bahía de Cádiz. CSIC - Instituto de Ciencias Marinas de Andalucía (ICMAN)
- Fernández-Delgado C, Baldó F, Vilas C, García-González D, Cuesta JA, González-Ortegón E, Drake P (2007) Effects of the River Discharge Management on the Nursery Function of the Guadalquivir River Estuary (SW Spain). Hydrobiologia 587(1):125–136. https://doi.org/10.1007/s10750-007-0691-9
- Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global Ecological Impacts of Invasive Species in Aquatic Ecosystems. Glob Change Biol 22(1):151–163. https://doi.org/10.1111/gcb.13004
- Gannon DP, Waples DM (2004) Diets of Coastal Bottlenose Dolphins from the U. S. Mid-Atlantic Coast Differ by Habitat. Mar Mamm Sci 20(3):527–545. https://doi.org/10.1111/j.1748-7692.2004.tb01177.x
- Garrido S, Murta AG, Moreira A, Ferreira MJ, Angélico MM (2008) Horse Mackerel (Trachurus Trachurus) Stomach Fullness off Portugal: Index Calibration and Spatio-Temporal Variations in Feeding Intensity. ICES J Mar Sci 65(9):1662–1669. https://doi.org/10.1093/icesjms/fsn169
- Garvey J, Whiles M (2017) Trophic Ecology. CRC Press, Hoboken, New Jersey
- Giakoumi S, Katsanevakis S, Albano PG, Azzurro E, Cardoso AC, Cebrian E, Deidun A, Edelist D, Francour P, Jimenez C, Mačić V, Occhipinti-Ambrogi A, Rilov G, Sghaier YR (2019) Management Priorities for Marine Invasive Species. Sci Total Environ 688:976–982. https://doi.org/10.1016/j.scitotenv.2019.06.282
- Giménez J, Marçalo A, Ramírez F, Verborgh P, Gauffier P, Esteban R, Nicolau L, González-Ortegón E, Baldó F, Vilas C, Vingada J, Forero MG, De Stephanis R (2017) Diet of Bottlenose Dolphins (Tursiops Truncatus) from the Gulf of Cadiz: Insights from Stomach Content and Stable Isotope Analyses. PLoS ONE 12(9):1–14. https://doi.org/10.1371/journal.pone.0184673
- Gomes P, Vieira AR, Oliveira R, Silva H, Martins R, Carneiro M (2017) First Record of Cynoscion Regalis (Pisces, Sciaenidae) in Portuguese Continental Waters. J Fish Biol 90(6):2470–2474. https://doi.org/10.1111/JFB.13318
- González-Ortegón E, Cuesta JA, Pascual E, Drake P (2010) Assessment of the Interaction between the White Shrimp, Palaemon Longirostris, and the Exotic Oriental Shrimp, Palaemon Macrodactylus, in a European Estuary (SW Spain). Biol Invasions 12(6):1731–1745. https://doi.org/10.1007/s10530-009-9585-2
- González-Ortegón E, Pascual E, Cuesta JA, Drake P (2006) Field Distribution and Osmoregulatory Capacity of Shrimps in a Temperate European Estuary (SW Spain). Estuar Coast Shelf Sci 67(1–2):293–302. https://doi.org/10.1016/j.ecss.2005.11.025
- González-Ortegón E, Jenkins S, Galil BS, Drake P, Cuesta JA (2020) Accelerated Invasion of Decapod Crustaceans in the Southernmost Point of the Atlantic Coast of Europe: A Non-Natives’ Hot Spot? Biol Invasions 22(12):3487–3492. https://doi.org/10.1007/s10530-020-02345-y
- González-Ortegón E, Baldó F, Arias A, Cuesta JA, Fernández-Delgado C, Vilas C, Drake P (2015) Freshwater Scarcity Effects on the Aquatic Macrofauna of a European Mediterranean-Climate Estuary. Sci Total Environ 503–504:213–221. https://doi.org/10.1016/J.SCITOTENV.2014.06.020
- González-Ortegón E, Subida MD, Arias AM, Baldó F, Cuesta JA, Fernández-Delgado C, Vilas C, Drake P (2012) Nekton Response to Freshwater Inputs in a Temperate European Estuary with Regulated Riverine Inflow. Sci Total Environ 440:261–271. https://doi.org/10.1016/j.scitotenv.2012.06.061
- Griffiths MH (2011) Influence of Prey Availability on the Distribution of Dusky Kob Argyrosomus Japonicus (Sciaenidae) in the Great Fish River Estuary, with Notes on the Diet of Early Juveniles from Three Other Estuarine Systems. Afr J Mar Sci 18(0)
- GUADALQUIVIR-LTER (2023) Guadalquivir Long-Term Ecological Research. https://deims.org/1b43bc23-e69b-4191-8342-20cd7af12647
- Hubans B, Chouvelon T, Begout ML, Biais G, Bustamante P, Ducci L, Mornet F, Boiron A, Coupeau Y, Spitz J (2017) Trophic Ecology of Commercial-Size Meagre, Argyrosomus Regius, in the Bay of Biscay (NE Atlantic). Aquat Living Resour 30:9. https://doi.org/10.1051/ALR/2017004
- Hynes HBN (1950) The Food of Fresh-Water Sticklebacks (Gasterosteus Aculeatus and Pygosteus Pungitius), with a Review of Methods Used in Studies of the Food of Fishes. J Anim Ecol 19(1):36. https://doi.org/10.2307/1570
- Hyslop EJ (1980) Stomach Contents Analysis—a Review of Methods and Their Application. J Fish Biol 17(4):411–429. https://doi.org/10.1111/J.1095-8649.1980.TB02775.X
- IDAPES (2023) Sistema de Informacion Andaluz de Produccion Pesquera. https://www.juntadeandalucia.es/agriculturaypesca/idapes/servlet/FrontController [Accessed 02.12.2023]
- IUCN (2023) The IUCN Red List of Threatened Species. https://www.iucnredlist.org/species/46104933/49226925 [Accessed 29.08.2023]
- Litvin SY, Weinstein MP (2004) Multivariate Analysis of Stable-Isotope Ratios to Infer Movements and Utilization of Estuarine Organic Matter by Juvenile Weakfish (Cynoscion Regalis). Can J Fish Aquat Sci 61(10):1851–1861. https://doi.org/10.1139/f04-121
- Lowerre-Barbieri SK, Chittenden ME, Barbieri LR (1996) The Multiple Spawning Pattern of Weakfish in the Chesapeake Bay and Middle Atlantic Bight. J Fish Biol 48(6):1139–1163. https://doi.org/10.1111/J.1095-8649.1996.TB01811.X
- McEachran JD, Fechhelm JD (2010) Fishes of the Gulf of Mexico. Scorpaeniformes to Tetraodontiformes, vol 2. University of Texas Press
- Mercer LP (1989) Species Profiles: Life Histories and Environmental Requirements of Coastal Fishes and Invertebrates (Mid-Atlantic): Weakfish. Coastal Ecology Group, US Army Corps of Engineers, Waterways Experiment Station
- Merriner JV (1975) Food Habits of the Weakfish, Cynoscion Regalis. in North Carolina Waters Chesapeake Science 16(1):74–76. https://doi.org/10.2307/1351090
- Morais P, Teodósio MA (2016) The Transatlantic Introduction of Weakfish Cynoscion Regalis (Bloch & Schneider, 1801) (Sciaenidae, Pisces) into Europe. BioInvasions Records 5(4):259–265. https://doi.org/10.3391/BIR.2016.5.4.11
- Nemerson DM (2001) Trophic Dynamics and Habitat Ecology of the Dominant Fish of Delaware Bay (United States of America) Marsh Creeks. Rutgers The State University of New Jersey-New Brunswick
- Nemerson DM, Kenneth WA (2004) Spatial Patterns in Diet and Distribution of Juveniles of Four Fish Species in Delaware Bay Marsh Creeks: Factors Influencing Fish Abundance. Mar Ecol Prog Ser 276(1):249–262. https://doi.org/10.3354/MEPS276249
- Nuñez MA, Kuebbing S, Dimarco RD, Simberloff D (2012) Invasive Species: To Eat or Not to Eat, That Is the Question. Conserv Lett 5(5):334–341. https://doi.org/10.1111/j.1755-263X.2012.00250.x
- Oliva-Paterna FJ, Ribeiro F, Miranda R, Anastácio P, García-Murillo P, Cobo F, Gallardo F, García-Berthou E, Boix D, Medina L, Morcillo F, Oscoz J, Guillén A, Aguiar F, Almeida D, Arias A, Ayres C, Banha F, Barca S, Biurrun I, Cabezas MP, Calero S, Campos JA, Capdevila-Argüelles L, Capinha C, Carpeto A, Casals F, Chainho P, Cirujano S, Clavero M, Cuesta JA, Del Toro V, Encarnação JP, Fernández-Delgado C, Franco J, García-Meseguer AJ, Guareschi S, Guerrero A, Hermoso V, Machordom A, Martelo J, Mellado-Díaz A, Moreno JC, Oficialdegui FJ, Amo R, Otero JC, Perdices A, Pou-Rovira Q, Rodríguez-Merino A, Ros M, Sánchez-Gullón E, Torralva M, Vieira-Lanero R, Zamora-López A, Zamora-Marín JM (2020) List of Potential Aquatic Alien Species of the Iberian Peninsula. Updated List of the Potential Aquatic Alien Species with High Risk of Invasion in Iberian Inland Waters. Informe Técnico Preparado Por LIFE INVASAQUA (LIFE17 GIE/ES/000515) 0–64
- Prieto L, Navarro G, Rodríguez-Gálvez S, Huertas IE, Naranjo JM, Ruiz J (2009) Oceanographic and Meteorological Forcing of the Pelagic Ecosystem on the Gulf of Cadiz Shelf (SW Iberian Peninsula). Cont Shelf Res 29(17):2122–2137. https://doi.org/10.1016/J.CSR.2009.08.007
- Ruiz J, Macías d, Navarro G (2017) Natural Forcings on a Transformed Territory Overshoot Thresholds of Primary Productivity in the Guadalquivir Estuary. Cont Shelf Res 148:199–207. https://doi.org/10.1016/J.CSR.2017.09.002
- Spitz J, Chouvelon T, Cardinaud M, Kostecki C, Lorance P (2013) Prey Preferences of Adult Sea Bass Dicentrarchus Labrax in the Northeastern Atlantic: Implications for Bycatch of Common Dolphin Delphinus Delphis. ICES J Mar Sci 70(2):452–461. https://doi.org/10.1093/ICESJMS/FSS200
- Thomas DL (1971) The Early Life History and Ecology of Six Species of Drum (Sciaenidae) in the Lower Delaware River, a Brackish Tidal Estuary. Middletown, DE 19709
- Torres MA, Coll M, Heymans JJ, Christensen V, Sobrino I (2013) Food-Web Structure of and Fishing Impacts on the Gulf of Cadiz Ecosystem (South-Western Spain). Ecol Model 265:26–44. https://doi.org/10.1016/j.ecolmodel.2013.05.019
- Turnure JT, Grothues TM, Able KW (2014) Seasonal Residency of Adult Weakfish (Cynoscion Regalis) in a Small Temperate Estuary Based on Acoustic Telemetry: A Local Perspective of a Coast Wide Phenomenon. Environ Biol Fish 98(5):1207–1221. https://doi.org/10.1007/s10641-014-0353-5
- Tuset VM, Lombarte A, Assis CA (2008) Otolith Atlas for the Western Mediterranean, North and Central Eastern Atlantic. Scientia Mar 72(S1):7–198. https://doi.org/10.3989/SCIMAR.2008.72S17
- Usseglio P, Selwyn JD, Downey-Wall AM, Hogan JD (2017) Effectiveness of Removals of the Invasive Lionfish: How Many Dives Are Needed to Deplete a Reef? PeerJ 2017. 21–15. https://doi.org/10.7717/peerj.3043
- Vilas C, Drake P, Fockedey N (2008) Feeding Preferences of Estuarine Mysids Neomysis Integer and Rhopalophthalmus Tartessicus in a Temperate Estuary (Guadalquivir Estuary, SW Spain). Estuar Coast Shelf Sci 77(3):345–356. https://doi.org/10.1016/J.ECSS.2007.09.025
- Willis MC, Richardson J, Smart T, Cowan J, Biondo P (2015) Diet Composition, Feeding Strategy, and Diet Overlap of 3 Sciaenids along the Southeastern United States. Fish Bull 113(3):290–301. https://doi.org/10.7755/FB.113.3.5
- Zariquiey AR (1968) Crustáceos Decápodos Ibéricos, vol 32. Investigación pesquera