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diversity Article Biometry, Distribution and Genetic Characterization of Blue Jack Mackerel Trachurus picturatus (Bowdich, 1825), a Rare Pelagic Fish Species in the Adriatic Sea Barbara Zorica , Ivana Bušeli´c* , Vanja Cikešˇ Keˇc,Vedran Vuletin, Ivana Lepen Plei´c, Igor Isajlovi´c,Ivana Radoni´cand Nedo Vrgoˇc Institute of Oceanography and Fisheries, Šetalište Ivana Meštrovi´ca63, 21000 Split, Croatia; [email protected] (B.Z.); [email protected] (V.C.K.);ˇ [email protected] (V.V.); [email protected] (I.L.P.); [email protected] (I.I.); [email protected] (I.R.); [email protected] (N.V.) * Correspondence: [email protected]; Tel.: +385-21-408009 Received: 26 October 2020; Accepted: 1 December 2020; Published: 3 December 2020 Abstract: The blue jack mackerel Trachurus picturatus (Bowdich, 1825) specimens (N = 155) were collected during the MEDITS survey, done along the eastern side, precisely, of the Croatian fishing ground in July 2018. Biometrical analysis of ten morphometric and five meristic characters, as well as genetic analysis proved that the collected specimens were blue jack mackerel. The total length (TL) and weight (W) of all observed specimens ranged from 9.2 to 33.7 cm (12.15 2.95 cm) and from 5.79 to ± 384.94 g (17.64 39.42 g), respectively. All calculated length–length relationships were linear (r > 0.923). ± Sex was determined only on two larger specimens (28 cm < TL < 32.8 cm), which were females. In the length–weight relationship, positive allometry was established (b = 3.1789). Based on 37 partial cytochrome b sequences, the overall haplotype diversity (h) of 0.812 0.048 and nucleotide diversity ± (π) of 0.0064 0.0007 indicated high levels of haplotype and low nucleotide diversity. The obtained ± sequences were compared to previously published research within the Northeast Atlantic Ocean and the Mediterranean Sea, confirming the absence of genetic structure among these populations. Keywords: central Mediterranean; mitochondrial DNA; morphometry; pelagic fish; phylogeography; Trachurus 1. Introduction Over the years, environmental variables have changed, mostly due to increasing globalisation processes [1]. The modification of those variables directly influenced whole marine ecosystems. Consequently, fish assemblage has either accommodated or transformed. Appearance and increased abundance of new and/or rare species surely affected the structure and functioning of species communities; therefore, systematic monitoring is compulsory. The blue jack mackerel Trachurus picturatus (Bowdich, 1825) is a benthopelagic fish species widely distributed and exploited in the area of East Atlantic (southern Bay of Biscay to south Morocco, including the Macaronesian archipelagos, Tristan de Cunha and Gough Islands). In the area of the Mediterranean Sea and its adjacent seas, this species can be found in its western part and the area of the Black Sea [2]. Within the distribution area of this species, its economic value is the lowest in the Mediterranean. In general, its specimens appear over the continental shelf and around offshore islands down to 400–500 m sea depth [3]. As with other pelagic fish species, it forms schools and tends to migrate from open sea to coastal areas [4]. In the area of the Adriatic, this species is rare and its specimens, in the past, were sporadically caught and noted [5–10]. Until now, only Bolognini et al. [11] reported the minor catch (N = 4) of blue jack mackerel in the Adriatic Sea. Diversity 2020, 12, 463; doi:10.3390/d12120463 www.mdpi.com/journal/diversity Diversity 2020, 12, 463 2 of 12 Recently, during the scientific surveys, a Croatian scientist noticed a higher amount of not so common Trachurus species in the catches. As geographical expansion of this rare species might have an impact on Adriatic biodiversity, its monitoring is crucial. It is believed that ocean warming is among the main driving forces of species abundance and distribution changes and, consequently, of changes in species biodiversity and marine ecosystem functioning [12,13]. Žužul et al. [14] offered ocean warming as one of the explanations behind the increase in the number of wild gilthead seabream noted in the costal parts of the Adriatic Sea [15]. The authors further argued that it is possible that wild gilthead seabream, as a species that thrives in warmer areas, is becoming more numerous at its northern distribution areas [16], as a consequence of increased larval survival and recruitment success [14]. Hence, to better understand what could be expected from the possible emergence of a blue jack mackerel population in the Adriatic Sea, the aim of this study was to investigate the biometrical analysis, the length–weight relationship and genetic diversity of the blue jack mackerel caught in the Adriatic Sea and compare the results to previously published research within the Northeast Atlantic Ocean and the Mediterranean Sea. The present paper provides phenotypic and genetic characteristics of this rare fish species in the Adriatic Sea, which might help us define this population that has obviously entered the Adriatic over the last decade. 2. Materials and Methods 2.1. Sample Processing and Biometric Analysis Specimens presumed to be blue jack mackerel (N = 155) and Mediterranean horse mackerel (N = 2) were collected by bottom trawl during the “MEDITS” research survey in July 2018 performed along the whole Croatian fishing ground. The tows were carried out over the continental shelf, between 40 to 800 m for a duration of 30 to 60 min, depending on the depth, and the mean trawl speed was 3 knots. Studied specimens were caught in 13 out of 63 hauls (Figure1). Collected specimens were immediately frozen and by the end of the survey transported to the laboratory for detailed analysis. In the laboratory, fourteen morphometric variables were measured: total length (TL), standard length (SL), fork length (FL), preanal (PAL) distance, head length (LH), eye diameter (O), maximum (H) body height, length of first (LD1) and second dorsal fin (LD2), length of pectoral fin (LP), as well as five meristic characters: number of rays in first (D1) and second dorsal fin (D2), in pectoral fin (P), in ventral fin (V) and in anal fin (A), according to Jardas [6]. Each body length ( 0.1 mm) and total body weight (W) ( 0.01 g) was measured. Morphometric ± ± characters were expressed as % of TL, with the exception of eye diameter (O), which was expressed as % of LH. Length–length relationships were determined by the method of least squares to fit a simple linear regression model. Length conversion equations were derived for total length (TL) and the head length (LH). The length–weight relationship was calculated by applying the exponential regression W = aTLb, where W = total fish weight in g; TL = total length in cm; a = proportionality constant; and b = allometric growth parameter. The hypotheses of isometric growth were tested using Student’s t-test (p < 0.05). 2.2. Genetic Analysis For genetic analysis, the sub-samples of muscle tissue were collected from 40 individuals and stored in absolute ethanol until genomic DNA (gDNA) extraction. Total genomic DNA (gDNA) was isolated using standard proteinase K digestion and phenol–chloroform extraction protocols [17] and stored in TE buffer at 20 C. Quantity and quality of isolated gDNA were assessed using − ◦ Nanophotometer (IMPLEN), at 260 and 280 nm. Samples with a 260/280 ratio between 1.7 and 1.9 were used as templates in a polymerase chain reaction (PCR). The fragment of cytochrome b locus (cytb) was amplified by PCR using the universal primers L14841 and H15149, described by Kocher et al. [18]. PCR was run in 25 µL reactions combining 0.125 µL of HotStarTaq DNA Polymerase (5 u/µL), 2.5 µL of Diversity 2020, 12, 463 3 of 12 10xPCR buffer, 1 µL of MgCl2 (25 mM), 0.5 µL of dNTP (0.25 mM each), 0.5 µL of each primer (10 µM) and DNase/RNase free PCR water to a volume of 25 µL. PCR conditions were as follows: 15 min at 95 ◦C, 35 cycles of 94 ◦C for 45 s, 51 ◦C for 45 s and 72 ◦C for 1 min, with a final extension at 72 ◦C for 10 min. PCR products were visualized on 1% agarose gel under UV transilluminator. Purification and DiversitySanger 2020, sequencing 12, x FOR PEER was REVIEW performed commercially by Macrogen Europe (Amsterdam, The Netherlands).3 of 12 (A) (B) FigureFigure 1. Map 1. Mapof the of Adriatic the Adriatic Sea Seashowing showing the thesampling sampling stations stations of of the the survey survey MEDITS MEDITS done done in in July 2018 July(A) 2018and (AMEDITS) and MEDITS surveys surveys done done over over the the last last six six summers summers (2013–2018)(2013–2018) (B ()B The) The red red (negative (negative stations)stations) and andblue blue (positive (positive stations) stations) dots dots indicate indicate the samplingsampling stations, stations, where where blue blue dot dot dimensions dimensions varied depending on the number of the blue jack mackerel Trachurus picturatus collected. varied depending on the number of the blue jack mackerel Trachurus picturatus collected. The obtained sequences were analysed for similarity with other known vertebrate sequences using 2.2. GeneticBlast Local Analysis Alignment Search Tool (BLAST) [19]. The obtained sequences (~350 bp) were compiled alongFor genetic all publicly analysis, available the sub-samples partial cytb sequences of muscle of tissueT. picturatus were, collected as well as from selected 40 sequencesindividuals of and stored in absolute ethanol until genomic DNA (gDNA) extraction. Total genomic DNA (gDNA) was isolated using standard proteinase K digestion and phenol–chloroform extraction protocols [17] and stored in TE buffer at −20 °C. Quantity and quality of isolated gDNA were assessed using Nanophotometer (IMPLEN), at 260 and 280 nm. Samples with a 260/280 ratio between 1.7 and 1.9 were used as templates in a polymerase chain reaction (PCR).

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