Abstract
The present paper investigates the diet and the food composition of Trachinotus ovatus in the central Mediterranean Sea (Strait of Messina). Moreover, the first documented data on plastic ingestion by T. ovatus are also reported. Samples ranging between 16.5 and 28.0 cm fork length were collected between May and November 2012 in the Strait of Messina (central Mediterranean Sea) by trolling lines. T. ovatus fed mainly on pelagic crustaceans and fishes, although the contribution of mollusks was also important. The absence of dominant prey indicated a generalist feeding behavior. The plastic debris was found in the stomach content of T. ovatus with a high percentage of occurrence (%O = 24.3%). Considering the commercial interest that T. ovatus has in some small-scale fishery markets, the potential impact of plastics on the trophic web and human consumption should be investigated.
Introduction
During recent years, climate change has influenced and modified the abundance and distribution of marine species worldwide (Occhipinti-Ambrogi Citation2007) and it is included among the main factors determining the phenomena of tropicalisation and meridionalisation of the Mediterranean Sea (Francour et al. Citation1994; Andaloro & Rinaldi Citation1998). As regards Mediterranean fish species, changes concern distribution (a spread of indigenous thermophilic species towards northern areas), species composition, competition and quantitative and qualitative variation in fishery catches (Andaloro & Rinaldi Citation1998; Bianchi Citation2007; Azzurro et al. Citation2011).
Trachinotus ovatus (L., 1758), Carangidae, is a thermophilic species (Bianchi et al. Citation2014), which has extended during the last decade its distribution in some northeastern Mediterranean areas (Lipej & Dulčić Citation2004; Raya & Sabatés Citation2015) and has been recorded as increasing in catches of artisanal fishery in the southern Tyrrhenian (Azzurro et al. Citation2011). The positive trend in catches of this carangid in part compensates for a decrease of other commercial fish and represents a valid alternative to common target species for maintaining the economic sustainability of small-scale fishing activities. Despite the fact that this species is becoming more important for local fisheries (AA.VV Citation2014), few data are still available on its biology and ecology, part of which is focused on farming studies (Tutman et al. Citation2004; Assem et al. Citation2005), aimed to check the potential value of T. ovatus as an aquaculture product, also thanks to its quick adaptation to confinement and tolerance of captivity conditions (Tutman et al. Citation2004). The analysis of age and growth of T. ovatus from southern Mediterranean Sea shows that this fish can reach 4 years of life (within the investigated size range of about 7–26 cm total length; Mourad Citation1999), whereas Abdallah (Citation2002) calculated the length–weight relationship (a = 0.022; b = 2.73; total length (TL) range = 3.4–23.3 cm). Recently, T. ovatus was also found among prey of swordfish in the central Mediterranean (Romeo et al. Citation2009). The few data on the feeding activity of T. ovatus concern only juvenile specimens (less than 100 mm TL) from southern Adriatic Sea (Batistic et al. Citation2005), coast of Israel (Chervinski & Zorn Citation1977) and Canary Islands (Moreno & Castro Citation1995). Dietary data on adult T. ovatus are needed, as well as on those fishes which are extending their distribution areas, in order to evaluate their role in the Mediterranean trophic web and to understand the interactions with other species, feeding relationships and competition, and their impact on the food chain.
The present paper investigates the diet and the food composition of adult T. ovatus in the central Mediterranean Sea (Strait of Messina). Moreover, the first documented data on plastic ingestion by T. ovatus are also reported. This finding allows us to also discuss in this paper the growing problem of plastic presence in Mediterranean waters and the introduction of dangerous chemicals into the marine food web. The extent of plastic ingestion by Mediterranean fishes is still largely unknown, but some authors (e.g. Deudero & Alomar 2014; Romeo et al. Citation2015) have already underlined the warning of this phenomenon also in relation to human consumption and health.
Materials and methods
Specimens of T. ovatus were collected between May and November 2012 by trolling lines and artificial bait in the Strait of Messina (central Mediterranean Sea), close to Cape Peloro ().
Figure 1. Study area off the Sicilian coast of the Strait of Messina.
The fork length (FL) was measured to the nearest 0.1 cm, and total weight (TW) was recorded to the nearest 0.01 g. The stomachs were dissected out and their contents examined by stereomicroscope. Prey remains were identified to the lowest possible taxon, using taxonomic keys (Whitehead et al. Citation1984–1986; Riedl Citation1991; Falciai & Minervini Citation1992; Avancini et al. Citation2006). Individuals of each prey taxon were counted, weighed (blotted dry for measurement of wet weight) and preserved in 70% ethanol.
The feeding incidence (%FI = individuals with identifiable prey remains/total number of fishes × 100) was used to evaluate the rate of feeding activity, whereas the degree of stomach fullness was estimated by the stomach content index (%SCI = wet weight of stomach content/body wet weight × 100).
To assess the importance of prey items in the diet of T. ovatus, the following dietary indices were calculated: abundance percentage (%N = number of individuals of prey i/total number of prey × 100), weight percentage (%W = weight of prey i/total weight of all prey × 100) and frequency of occurrence (%F = number of stomachs containing prey i/total number of stomachs containing prey × 100). Moreover, the percentage index of relative importance (%IRI) was estimated (Hyslop Citation1980) as follows: IRI = (%N + %W)*(%F) and %IRIi = (IRIi ⁄ ∑IRI) × 100.
The feeding behaviour of T. ovatus was assessed using the Costello graphical method (Costello Citation1990) modified by Amundsen et al. (Citation1996), plotting the prey-specific abundance against the frequency of occurrence in a two-dimensional graph. The prey-specific abundance is calculated as follows:
where Pi is the prey-specific abundance of prey i, Si is the total abundance (as weight or number) of prey i, and Sti is the total stomach contents in only those specimens with prey i in their stomachs. According to Amundsen et al. (Citation1996), information on prey importance, feeding strategy and niche width contribution can be inferred through the position of prey types in the two-dimensional plot.
The trophic level of T. ovatus was estimated according to Pauly and Christensen (Citation1995), as follows:
where TROPHj is the fractional trophic level of prey j and DCj represents the fraction of j in the diet of the consumer species (here, T. ovatus). The TROPH can vary between 2.0, for herbivorous/detritivorous, and 5.0, for piscivorous/carnivorous organisms (Pauly et al. Citation1998, Citation2000; Pauly & Palomares Citation2000). TROPH value was calculated using the weight contribution and the trophic level of each prey species to the diet. Trophic level values of prey were assigned according to Pauly et al. (Citation2000) and Stergiou and Karpouzi (Citation2002).
To evaluate potential seasonal-related diet variations, a non-parametric multivariate analysis of variance (PERMANOVA) was performed on prey abundance. Data were transformed to square root and analysed on the basis of Gower distance using 4999 permutations. Pair-wise comparisons were computed when significant differences (p < 0.05) among factor levels were detected. Then, a multivariate multiple permutation test (SIMPER) was performed to determine the contribution of each prey category to the average dissimilarity between groups. All of these analyses were conducted using the statistical software PRIMER6 and PERMANOVA+ (Clarke & Warwick Citation2001; Anderson et al. Citation2008).
Finally, the stomach content of each specimen was visually inspected under a stereomicroscope (80× magnification) in order to individuate the potential presence of plastic fragments. When plastic particles were found, they were photographed by stereomicroscope Zeiss Discovery V8 coupled with Axiovision AxioVs40 version 4.8.2.0 digital image processing software. The following data for each plastic fragment were recorded: colour (according to a chromatic scale), shape (assigned following geometrical criteria), length, width and weight. The percentage of occurrence (%O) of plastic debris in the stomach content of T. ovatus was calculated as the proportion of individuals containing plastics on the total samples (including also stomachs without prey items):
The plastics ingested were then categorised as macroparticles (> 25 mm), mesoparticles (5–25 mm) and microparticles (< 5 mm), following Galgani et al. (Citation2013), and the percentage of each category was calculated as the proportion of each plastic category against the total amount of plastic found in the stomachs.
Results
Overall, 115 individuals of T. ovatus ranging between 16.5 and 28.0 cm FL (mean FL = 23.4 cm; standard deviation = 2.5) and 68.2 and 368.84 g (mean TW = 220.3 g; standard deviation = 68.3) were collected. On 115 stomachs analysed, 42 were empty, producing a feeding incidence value %FI = 58.3. The degree of stomach fullness (SCI) for the whole sampling ranged between 0.03 and 2.49%, with a median value of 0.19%. The prey list and dietary index values (%N, %W, %F and %IRI) for each item are reported in together with the information on their developmental life stage (A = adult; J = juvenile; L = various stages of larvae).
Table I. Diet composition of Trachinotus ovatus and percentage values of dietary indexes calculated for each prey item: abundance (%N); weight (%W); frequency of occurrence (%F); index of relative abundance (%IRI). Life stage of prey is also reported (A = adult; J = juvenile; L = various stages of larvae).
Crustacea were the most important prey for T. ovatus, in terms of number and frequency of occurrence, with a dominance of calanoid copepods and euphausiids. This latter group was mainly represented by the species Euphausia krohnii (Brandt, 1851) which had a %IRI value of 24.46. A valuable contribution in weight to the diet of T. ovatus was given by teleosts, in particular Sardinella aurita (Valenciennes, 1847), and Engraulis encrasicolus (Linnaeus, 1758) (%W = 33.70 and 11.90, respectively). The analysis of fish prey highlighted also the ingestion of mesopelagic fishes and a case of cannibalism (a juvenile specimen of T. ovatus preyed by an adult of 26.0 cm FL). T. ovatus fed also on pelagic gastropods, mainly represented by Atlanta sp. (%IRI = 9.88), and occasionally on insects. In some stomachs, the presence of plant seeds and plastic particles was also detected.
The feeding strategy of T. ovatus is shown in , where the frequency of occurrence (%F) is plotted against prey-specific abundance (Pi), expressed as number () and weight (). Results indicate a generalist feeding behavior of T. ovatus, as also demonstrated by the absence of dominant prey. Most of the food categories are located in the lower left corner of the diagrams or close to the y-axis, in a graph region where prey are considered of low importance, since they were consumed at a low frequency.
Figure 2. Costello graph (modified by Amundsen et al. Citation1996): relationship between frequency of occurrence (%F) of prey items and prey-specific abundance (Pi), expressed as A, number and B, weight, respectively, in the diet of Trachinotus ovatus, collected in the Strait of Sicily. The graph background shows the explanatory Costello diagram and its interpretation of feeding strategy (BPC = between-phenotype component; WPC = within-phenotype component).
The calculated value of trophic level (TROPH) for T. ovatus was 3.90.
PERMANOVA analysis on prey abundance in fish caught during the three investigated seasons (autumn: n = 23, FL range = 22.0–27.8 cm; spring: n = 19, FL range = 16.8–28.0 cm; summer: n = 31, FL range = 16.5–27.8 cm) revealed significant differences in diet composition (F = 2.6853, p < 0.01). Pair-wise comparisons showed summer and spring to be different from autumn (p < 0.01). As demonstrated by the SIMPER test, the main contributors to these differences were E. krohnii, more abundant in autumn (average abundance = 1.27), and calanoid copepods, more abundant in spring (average abundance = 1.82), than in the other two seasons.
Finally, shows data on plastic debris found in the stomach content of 28 T. ovatus (ranging between 20.0 and 27.8 cm FL), with a percentage of occurrence (%O) equal to 24.3%. In two cases, more than one piece of plastic was recorded. Plastic fragments had different shapes and colour ( and ). According to the dimensional categories of Galgani et al. (Citation2013), the plastic debris ingested belong to microparticles (83.3%) and mesoparticles (16.7%).
Table II. Data on colour, shape and size of plastic debris in stomach content of Trachinotus ovatus specimens collected in the Strait of Messina. FL = fork length; TW = total weight.
Figure 3. Examples of plastic debris found in the stomach of Trachinotus ovatus.
Discussion
The analysis of the diet of T. ovatus shows that this predator fed mainly on pelagic crustaceans and fishes, although the contribution of mollusks was also important. Cnidarians and annelids were occasional prey, and a small fraction of food was represented by insects. Terrestrial plant seeds were also found in some stomachs, as well as plastic fragments.
The food composition of the diet of T. ovatus in the study area seems to be influenced by hydrodynamic, biological and behavioural factors. The Strait of Messina is characterised by strong upwelling currents, which determine a passive transport and concentration of planktonic species and, in general, slow-swimming organisms (Mazzarelli Citation1909; Berdar et al. Citation1983; Guglielmo et al. Citation1995). Moreover, this hydrodynamism allows the presence in surface waters of vertically migrant mesopelagic fauna (Mazzarelli Citation1909; Genovese et al. Citation1971; Berdar et al. Citation1983; Guglielmo et al. Citation1995), which usually rise at night from deep waters to upper layers to graze or feed on small zooplankton. Nictameral migrations enhance food encounter probabilities, since several prey found in T. ovatus stomachs are usually reported from mesopelagic waters: some copepods (e.g. Pleuromamma gracilis) and decapods (e.g. Primno macropa), euphausiids and mollusks (Atlantidae, Creseidae, Peraclidae), as well as Myctophidae and Sternoptychidae among fish (Berdar et al. Citation1983; Guglielmo et al. Citation1995). The influence of the hydrodynamic system on the trophic web of the Strait of Messina has already been highlighted for large pelagic predators occurring in the area (Romeo et al. Citation2012; Battaglia et al. Citation2013).
A consistent number of prey items can be categorised as larval or juvenile stages and were mainly represented by decapods and fish. Moreover, a case of cannibalism was observed, concerning a young T. ovatus (FL = 1.4 cm) preyed by an adult of 26.0 cm FL. This phenomenon is not frequently encountered in carangids, although it has already been reported in Atropus atropos in the Indian Ocean (Sivakami Citation1997).
The analysis of feeding habits of T. ovatus by the Costello graphical method (Costello Citation1990) modified by Amundsen et al. (Citation1996) did not identify a strict trophic relationship between predator and a specific prey item, but highlighted a broad prey spectrum, made up of non-dominant prey. These results together with the evidence of significant seasonal differences suggest that T. ovatus can be described as an opportunistic feeder, showing a particular voracity, as demonstrated by the ingestion of several plastic particles and some plant seeds, likely confused for planktonic organisms.
While in this paper we examined the diet of adult T. ovatus, some considerations on ontogenic changes could be inferred if our results are compared with those reported by Chervinski and Zorn (Citation1977), Moreno and Castro (Citation1995) and Batistic et al. (Citation2005), who analysed feeding habits of juvenile specimens. Differences among specific prey may vary depending on the study area; however, the food of juvenile T. ovatus seems mainly based on crustaceans and insects (Chervinski & Zorn Citation1977; Moreno & Castro Citation1995; Batistic et al. Citation2005); adults (present paper) rely also on fish prey and pelagic Gastropoda, whereas insects have low importance.
The calculated value of trophic level (TROPH = 3.90) for T. ovatus is higher than 3.73, the value provided by Froese and Pauly (Citation2014), but this may be due to different length ranges of examined samples, and then to dietary changes depending on fish size.
The occurrence of a relatively high amount of plastic debris in the stomach content of T. ovatus may represent a potential risk for this species. However, the impact of plastic ingestion on fish and the contaminant transfer to the trophic web is still poorly known in Mediterranean waters (Deudero & Alomar 2014). Nevertheless, the Mediterranean Sea was recently defined as one of the most impacted areas in the world by plastic pollution (Cozar et al. Citation2014; Fossi et al. Citation2014). The ingestion of plastic particles in this area has been reported in several marine organisms, ranging from zooplankton to top predators (Fossi et al. Citation2012, Citation2014; Cole et al. Citation2013; Collignon et al. Citation2014; Ivar do Sul & Costa Citation2014; Romeo et al. Citation2015). In particular, plastic debris has been already found in the stomachs of some Mediterranean pelagic fish such as bluefin tuna, albacore, swordfish, dolphin fish and bogue (Massutí et al. Citation1998; Deudero Citation2001; Karakulak et al. Citation2009; De la Serna et al. Citation2012; Deudero & Alomar 2014, Citation2015; Romeo et al. Citation2015). As in other pelagic predators, the consumption of plastic debris by T. ovatus may also be in part determined by the predation on gregarious prey. Indeed, according to Romeo et al. (Citation2015), the fish habit of feeding on small prey aggregated in schools may increase the probability of ingesting plastic together with food.
The high percentage of occurrence of plastic fragments in the stomach of T. ovatus may also be related to the morphology and hydrodynamic regime of the study area, characterised by strong currents that may create convergence zones in which floating plastic debris may accumulate. This phenomenon is already known, with higher proportions, in the oceanic gyres (Boerger et al. Citation2010; Davison & Asch Citation2011). The presence of insects and some neustonic organisms (e.g. Porpita porpita) among prey suggests the behaviour of hunting just beyond the surface layer, as observed also during the sampling operations, and this may make T. ovatus more vulnerable to the ingestion of floating plastic debris.
Further studies are needed to investigate the impact of plastic ingestion on the biology of this species, from a toxicological point of view, taking into account also the aspects linked to the transport, accumulation and bioavailability of persistent, bioaccumulative and toxic (PBT) chemicals and other toxic substances (such as phthalates, nonylphenol, bisphenol A and brominated flame retardants) associated with plastics. Considering the commercial interest that T. ovatus has in some small-scale fishery markets, the potential impact on human consumption and health should be investigated more deeply. Moreover, the present data could be useful for the implementation of the Marine Strategy Framework Directive (MSFD; 2008/56/EC) which aims to achieve Good Environmental Status (GES) for European marine waters by 2020, with specific regard to Descriptor 10 on “Marine litter”.
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