Spreading and Establishment of the Non Indigenous Species Caprella Scaura (Amphipoda: Caprellidae) in the Central Region of the Aegean Sea (Eastern Mediterranean Sea)

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Journal of Marine Science and Engineering

Article Spreading and Establishment of the Non Indigenous Species Caprella scaura (Amphipoda: Caprellidae) in the Central Region of the Aegean Sea (Eastern Mediterranean Sea)

Alexios Lolas * , Ioannis T. Karapanagiotidis , Panagiota Panagiotaki and Dimitris Vaﬁdis

Department of Ichthyology and Aquatic Environment, School of Agriculture Sciences, University of Thessaly, 38446 Volos, Greece; [email protected] (I.T.K.); [email protected] (P.P.); dvaﬁ[email protected] (D.V.) * Correspondence: [email protected]

Abstract: Caprella scaura is an invasive amphipod, native to the Indian Ocean, which has already spread to several regions of the world, including the Mediterranean Sea. The present study reports the first occurrence of the species on fish farms cages in Greece, in the Pagasitikos Gulf. Specimens were collected from colonies of the bryozoan Bugula neritina. Basic aspects of the population dynamics of the species, such as the population structure, sex ratio, and size frequency were studied for 13 months and tested for differences between two depth levels (30 cm and 5 m). Population density was significantly different between the two sampled depths. All the demographic categories were present during the whole study period, indicating that the species follows a continuous reproduction pattern in the region. Males were typically larger than females, but females were more abundant in most samples. It seems that the species is well established in the region and is probably moving Citation: Lolas, A.; Karapanagiotidis, towards the northern parts of the Aegean Sea. I.T.; Panagiotaki, P.; Vafidis, D. Spreading and Establishment of the Keywords: Non Indigenous Species Caprella population dynamics; biofouling; invasive species; biodiversity threats; integrated multi- scaura (Amphipoda: Caprellidae) in trophic aquaculture; Pagasitikos Gulf the Central Region of the Aegean Sea (Eastern Mediterranean Sea). J. Mar. Sci. Eng. 2021, 9, 857. https:// doi.org/10.3390/jmse9080857 1. Introduction The spreading of marine non-indigenous species (NIS) is considered a great threat Academic Editor: to the marine environment [1,2]. Their impact on the structure, function and biodiversity Francesco Tiralongo of native ecosystems and communities can be very strong, thus they are very often being referred to as a form of “biological pollution” [3,4]. The implications of marine NIS Received: 26 June 2021 invasions to the environment are becoming a huge concern to scientists and legislators. Accepted: 5 August 2021 This concern is reflected within the Marine Strategy Framework Directive (MSFD) and the Published: 9 August 2021 EU Biodiversity Strategy, which specifically stress the need to assess the threats posed by the introduction and spread of marine NIS [1,2]. Publisher’s Note: MDPI stays neutral The successful introduction of a NIS to a new environment depends on many factors, with regard to jurisdictional claims in and is usually a multi-step process [5]. First, the species need to be transported from published maps and institutional affil- iations. their original area to a new location, in which case ballast water, fouling of the hull from commercial vessels and aquaculture are generally considered the main vectors responsible for NIS movement across the oceans [2,6–9]. The second step requires a potential recipient community where the transported species will settle and start their expansion in their new “home”, in which case recreational marinas, harbors and off-coast aquaculture facilities Copyright: © 2021 by the authors. and equipment provide the adequate substrate for NIS to establish and thrive [10–15]. Licensee MDPI, Basel, Switzerland. However, the most important factor that facilitates a successful invasion is the ability of This article is an open access article NIS to actually survive, both during the transportation and after their relocation to the distributed under the terms and conditions of the Creative Commons new area, which usually involves living through rather unfavorable conditions [5]. This Attribution (CC BY) license (https:// adaptability to new and challenging environments is usually linked to certain life-cycle creativecommons.org/licenses/by/ features such as high reproductive potential and dispersal ability, especially for marine 4.0/). species [6]. These features are included in the study of the population dynamics, along

J. Mar. Sci. Eng. 2021, 9, 857. https://doi.org/10.3390/jmse9080857 https://www.mdpi.com/journal/jmse J. Mar. Sci. Eng. 2021, 9, 857 2 of 12

with other aspects, such as abundance, seasonal variation, distribution, breeding, sex ratio and population structure. Knowledge of these characteristics from NIS is an important step in order to understand the invasion process and its impacts on the invaded ecosystems and, to an extent, in the developing of management policies and practices [16]. The subphylum Crustacea is probably among the most successful taxonomic groups of aquatic NIS, since they fulfill most of the requirements for a potential invader such as rapid growth, production of several generations per year, early maturity and high fecundity and, of course, their association with fouling communities [6,17,18]. Within the Crustacea, the family Caprellidae has a fair share of species characterized as NIS, with most of them being part of a long list of invaders in the Mediterranean [1,2,19]. Caprellids are common inhabitants in coastal and deep water marine environments, with a worldwide distribution [20–23]. Their populations can reach high densities under favorable conditions, but with potential variations on a spatiotemporal scale, mostly depending upon a range of biotic and abiotic factors, such as temperature, food supply, depth and predation [10,24–26]. Additionally, seasonal patterns of caprellid populations have been correlated positively with the respective seasonal cycles of the natural substrate they inhabit [16,22,27]. They seem to play an important role in trophic cascades, as the connecting link between primary producers and higher trophic levels, while the discovery of high concentrations of polyunsaturated fatty acids in certain species has recently made them a promising aquaculture resource [15,25,28]. Their ability to swim is rather limited, due to their reduced pleopods, which hinders their active dispersal, thus making them good candidate species to carry out population and ecological studies [29]. On the other hand, their unique morphological features favor the clinging on both natural (e.g., macroalgae, hydroids, bryozoans) and artificial substrate (e.g., ship hulls, buoys, marine litter) [30,31]. This facilitates their passive dispersal, which is a crucial factor in the case of successful invasive species such as Caprella scaura [32,33]. Caprella scaura was originally described from Mauritius and later reported from several regions of the world [32]. Its native region is the Western Indian Ocean, while its first occurrence in the Mediterranean Sea was recorded in Venice (Italy), in 1994 [34]. Subse- quently, it has been reported in locations along the coastlines of several Mediterranean countries [14,15,32,33,35–39]. Even though the geographical distribution of C. scaura is well documented, especially for the Western part of the Mediterranean, there are still areas that remain unexplored and, as a result, the total extent of its expansion in the Mediter- ranean remains unknown. Furthermore, population dynamics studies of the species are very scarce and only focused in the Western Mediterranean [8,16], contrary to the Eastern Mediterranean where no such study exists. The aim of this study was, first of all, to report a new occurrence of C. scaura for Greece and describe the temporal variation of basic aspects of its population and set the baseline in the effort to assess and explain the successful adaptation of the species in the region.

2. Materials and Methods 2.1. Sampling Design A preliminary study of the biofouling communities from the two fish farms in the Pagasitikos Gulf, in search for caprellids to analyze their nutritional content for potential use in aquaculture applications [40–42], led to an unexpected finding. Based on previous studies in the region [43] we were expecting to find common native caprellids such as Caprella acanthifera or Phtisica marina, instead we found an exclusive abundance of C. scaura. Since it was a new record of a NIS for the region, we decided to investigate the seasonal population dynamics of the alien species. Furthermore, since there might be a potential interest in using C. scaura as a candidate species in Integrated Multi-trophic Aquaculture (IMTA) systems [28], we thought it would be useful to have some information regarding the potential effects of depth on the population dynamics of the species, since this would affect the optimal deployment of their culturing system in the future. The initial planning for the study included both fish farms, but because of a major reconstruction and relocation J. Mar. Sci. Eng. 2021, 9, 857 3 of 13

J. Mar. Sci. Eng. 2021, 9, 857 regarding the potential effects of depth on the population dynamics of the species, since3 of 12 this would affect the optimal deployment of their culturing system in the future. The initial planning for the study included both fish farms, but because of a major reconstruction and relocation of the fish cages from one of the farms, we were unable to continue the of the ﬁsh cages from one of the farms, we were unable to continue the samplings there, so samplings there, so all data analyzed and presented in the paper are from one fish farm all data analyzed and presented in the paper are from one ﬁsh farm (Figure1). (Figure 1).

Figure 1. Map of the region and the location of the study area. Red outlines in main map indicate Figure 1. Map of the region and the location of the study area. Red outlines in main map indicate the the fish cages where the sampling meshes were deployed. Red star in mini map indicates the loca- fishtion cages of the where other thefish samplingfarm, which meshes eventually were deployed.was not included Red star in inthe mini study. map indicates the location of the other fish farm, which eventually was not included in the study. For the collection of the samples, we adopted the design proposed by Boos (2009) [26].For We theused collection plastic meshes of the samples,(40 cm × 25 we cm, adopted mesh size the 2 design mm) as proposed a substrate by for Boos biofouling (2009) [ 26]. Weand used colonization plastic meshes by C. scaura (40 cm. In× order25 cm, to mesh test for size potential 2 mm)as differences a substrate in forthebiofouling population and colonizationstructure of bytheC. species scaura .in In a orderdepth to gradient, test for potential the meshes differences were attached in the populationto ropes and structure sub- ofmerged the species in two in different a depth depth gradient, levels: the The meshes first level were was attached about to30 ropescm below and surface submerged (re- in twoferred different to as “surface”, depth levels: hereafter) The firstand levelthe second was about level at 30 5 cmm depth below (hereafter surface (referred referred to to as “surface”,as “deep”). hereafter) Five replicates and the were second used for level each at depth 5 m depth level and (hereafter they were referred deployed to as in “deep”). two Fivegroups. replicates The first were group used (5 forsurface each and depth 5 deep level meshes) and they was were deployed deployed in May in two 2018 groups. and the The firstsecond group group (5 surface (another and 5 surface 5 deep and meshes) 5 deep was me deployedshes) wasin deployed May 2018 4 weeks and the later, second in June group (another2018. After 5 surface the initial and deployment, 5 deep meshes) the meshes was deployed of each group 4 weeks were later, collected in June and 2018. replaced After the initialby new deployment, ones in monthly the meshes intervals, of eachso each group group were was collected exposed andfor a replaced period of by 8 newweeks ones in(Figure monthly 2). At intervals, each sampling so each date, group sea waswater exposed temperature for a (T, period resolution of 8 weeks 0.1°C), (Figure salinity2 (S,). At eachresolution sampling 0.1‰) date, and sea dissolved water temperatureoxygen (DO, resolution (T, resolution 0.01 0.1mg◦ C),L−1) salinitywere recorded (S, resolution in 3 0.1replicated‰) and dissolvedmeasurements oxygen at 1 (DO, m depth, resolution by a 0.01handheld mg L −digital1) were multiparametric recorded in 3 replicated probe J. Mar. Sci. Eng. 2021, 9, 857 4 of 13 measurements(WTW GmbH, atWeilheim, 1 m depth, Germany). by a handheld digital multiparametric probe (WTW GmbH, Weilheim, Germany).

Figure 2. GraphicGraphic representation representation of of the the sampling sampling sch schemeeme depicting depicting the the sampling sampling depths depths and and the the collectioncollection schedule. schedule.

2.2. Laboratory Processing Immediately after collection, the meshes were placed in separate labeled containers, fixed in a 4% formalin solution and transferred to the laboratory. Each sample was then repeatedly rinsed with tap water and sieved through a 250 μm mesh in order to retain mobile organisms. Caprella scaura male and female individuals were identified by the distinctive external characteristics described in several studies [32,33,44], sorted out from the rest of the fauna and fixed in 85% ethanol. Small individuals without visible signs of sex and/or maturity were classified as juveniles [15]. The total number of individuals (N) was counted from each sample, and population density (D) was expressed as the number of individuals per m2. Due to the large number of individuals, a representative subsample for each sampling was created by randomly selecting 50 males, 50 females and 15 juveniles in order to perform a balanced statistical design for length comparisons (i.e., between sexes, depth level and among samplings) as well as to construct the length-frequency distribution (LFD) of the population from each sampling [8]. Digital photos of specimens were taken using an Olympus SZX-9 stereomicroscope, and each individual was measured from the anterior margin of the head to the posterior margin of the telson to the nearest 0.1 mm [16], using the image processing and analysis software ImageJ (v. 1.53e National Institute of Mental Health, Bethesda, Maryland, USA) [45]. Females were further classified as non-breeding (when no eggs were visible in the brood pouch) and breeding (visible eggs in the brooding pouch), in which case the total number of eggs was counted. Sex ratio (SR) of the population was calculated for each sample, as the proportion of females in the whole sample (SR = F/F + M) and tested for significant difference from the expected sex ratio (SR = 0.5, i.e., equal proportion of two sexes) using the chi-squared test [16,46]. Temporal differences in population densities and total body were tested with one- way ANOVA, whereas Student’s t-test was used to detect differences between the two depth levels. The number of eggs found in the pouch of breeding females was tested for correlation with total body length using Spearman’s rank correlation, and the Student’s t- test was used to detect potential differences between the two depth levels. Significant pair- wise comparisons by the Fisher’s LSD procedure were performed post hoc, to identify the potential individual group differences. All statistical analyses were performed by the “Statgraphics Centurion” software package (v.18.1 Statgraphics Technologies, Inc., The Plains, VA, USA) and values of p < 0.05 were considered significant.

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2.2. Laboratory Processing Immediately after collection, the meshes were placed in separate labeled containers, fixed in a 4% formalin solution and transferred to the laboratory. Each sample was then repeatedly rinsed with tap water and sieved through a 250 µm mesh in order to retain mobile organisms. Caprella scaura male and female individuals were identified by the distinctive external characteristics described in several studies [32,33,44], sorted out from the rest of the fauna and fixed in 85% ethanol. Small individuals without visible signs of sex and/or maturity were classified as juveniles [15]. The total number of individuals (N) was counted from each sample, and population density (D) was expressed as the number of individuals per m2. Due to the large number of individuals, a representative subsample for each sampling was created by randomly selecting 50 males, 50 females and 15 juveniles in order to perform a balanced statistical design for length comparisons (i.e., between sexes, depth level and among samplings) as well as to construct the length-frequency distribution (LFD) of the population from each sampling [8]. Digital photos of specimens were taken using an Olympus SZX-9 stereomicroscope, and each individual was measured from the anterior margin of the head to the posterior margin of the telson to the nearest 0.1 mm [16], using the image processing and analysis software ImageJ (v. 1.53e National Institute of Mental Health, Bethesda, MD, USA) [45]. Females were further classified as non-breeding (when no eggs were visible in the brood pouch) and breeding (visible eggs in the brooding pouch), in which case the total number of eggs was counted. Sex ratio (SR) of the population was calculated for each sample, as the proportion of females in the whole sample (SR = F/F + M) and tested for significant difference from the expected sex ratio (SR = 0.5, i.e., equal proportion of two sexes) using the chi-squared test [16,46]. Temporal differences in population densities and total body were tested with one- way ANOVA, whereas Student’s t-test was used to detect differences between the two depth levels. The number of eggs found in the pouch of breeding females was tested for correlation with total body length using Spearman’s rank correlation, and the Student’s t-test was used to detect potential differences between the two depth levels. Significant pair-wise comparisons by the Fisher’s LSD procedure were performed post hoc, to identify the potential individual group differences. All statistical analyses were performed by the “Statgraphics Centurion” software package (v.18.1 Statgraphics Technologies, Inc., The Plains, VA, USA) and values of p < 0.05 were considered significant.

3. Results All abiotic factors measured during the study ﬂuctuated between seasons, following a typical temporal pattern, as expected in the Mediterranean region (Figure3). Water temperature had the strongest variation in recorded values, ranging between 27.9 ◦C in August 2018 and 12.3 ◦C in February 2019. Salinity values were within the typical seawater range, with a small variation between 36.3‰ and 38.1‰. Dissolved oxygen concentration values ranged between 6.90 mg L−1 in December 2018 and 5.13 mg L−1 in August 2018. The biofouling on the sampling meshes included several taxa, which are common in these communities in the Mediterranean, such as hydroids (Eudendrium spp) or algae (Gellidium spp., Jania spp. and Polysiphonia spp.), but the dominant species through the whole study period was the bryozoan Bugula neritina. In regard to the motile epifauna, apart from the obvious dominance of C. scaura, Jassa spp. and Elasmopus spp. were the next species with the strongest presence. It is worth noting that another caprellid, Caprella equilibra was also identiﬁed, but its presence was quite scarce (0–10 individuals per sampling, mostly males). J. Mar. Sci. Eng. 2021, 9, 857 5 of 13

3. Results All abiotic factors measured during the study fluctuated between seasons, following a typical temporal pattern, as expected in the Mediterranean region (Figure 3). Water temperature had the strongest variation in recorded values, ranging between 27.9°C in Au-

J. Mar. Sci. Eng. 2021, 9, 857 gust 2018 and 12.3°C in February 2019. Salinity values were within the5 oftypical 12 seawater range, with a small variation between 36.3‰ and 38.1‰. Dissolved oxygen concentration values ranged between 6.90 mg L−1 in December 2018 and 5.13 mg L−1 in August 2018.

FigureFigure 3. Temporal3. Temporal variation variation of abiotic of abio parameterstic parameters measured measured (A) temperature, (A) temperature, (B) salinity and (B ()C salinity) and (C) dissolveddissolved oxygen, oxygen, during during the study the study period. period. Bars indicate Bars standardindicate deviation. standard deviation.

Student’sThe biofouling t-test revealed on the that sampling population meshes densities included had significant several differences taxa, which between are common in thethese two communities depth levels (p in< the 0.05), Mediterranean, with higher values such found as hydroids on the surface(Eudendrium populations. spp) or algae (Gel- Average density for the surface populations was estimated 1,292.8 ± 550.1 ind m−2, with alidium minimum spp., of Jania 500 and spp. maximum and Polysiphonia of 2,930 ind spp.), m−2 ,but whereas the dominant deep population species density through the whole rangedstudy betweenperiod 400was− 2,370the bryozoan and had an Bugula average neritina of 1,092.9. In± regard476.6 indto mthe−2 .motile One-way epifauna, apart ANOVAfrom the on obvious population dominance densities among of C. monthsscaura, revealedJassa spp. significant and Elasmopus differences spp. for were both the next spe- Surfacecies with (F12,64 the= strongest 42.75, p < 0.05)presence. and Deep It is (F worth12,64 = noting 21.86, p that< 0.05) another populations. caprellid, Fisher’s Caprella equilibra LSDwas procedure also identified, identified but June, its October presence and Marchwas qu as theite monthsscarce with(0–10 the individuals highest values per sampling, for both depth levels, whereas January, February, May and August were the months with mostly males). the lowest values (Figure4). Student’s t-test revealed that population densities had significant differences between the two depth levels (p < 0.05), with higher values found on the surface populations. Average density for the surface populations was estimated 1,292.8 ± 550.1 ind m−2, with a minimum of 500 and maximum of 2,930 ind m−2, whereas deep population density ranged between 400−2,370 and had an average of 1,092.9 ± 476.6 ind m−2. One-way ANOVA on population densities among months revealed significant differences for both Surface (F12,64

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= 42.75, p < 0.05) and Deep (F12,64 = 21.86, p < 0.05) populations. Fisher’s LSD procedure identified June, October and March as the months with the highest values for both depth levels,= 42.75, whereas p < 0.05) January, and Deep February, (F12,64 = 21.86,May and p < August0.05) populations. were the months Fisher’s with LSD the procedure lowest val- J. Mar. Sci. Eng. 2021, 9, 857 uesidentified (Figure June, 4). October and March as the months with the highest values for both6 of 12 depth levels, whereas January, February, May and August were the months with the lowest values (Figure 4).

Figure 4. Temporal variation of the surface and deep population density of Caprella scaura from a Figure 4. Temporal variation of the surface and deep population density of Caprella scaura from a Figurefish farm 4. Temporal in the Pagasitikos variation of theGulf. surface Bars and indicate deep population standard densitydeviation. of Caprella scaura from a fish fish farm in the Pagasitikos Gulf. Bars indicate standard deviation. farm in the Pagasitikos Gulf. Bars indicate standard deviation. Population structure was consistent during the study period, with all the demo- graphicPopulationPopulation categories structure structure (i.e., was males, was consistent consistentbreeding during /during thenon study breeding the period, study females, with period, all thejuveniles) with demographic all the present demo- in all categoriessamplingsgraphic categories (i.e., (Figure males, (i.e., breeding5). The males, total / nonbreeding number breeding / ofnon females, indi breedingviduals, juveniles) females, from present both juveniles) indepths, all samplings present was 18,090 in all out (Figureofsamplings which5). The 7,731 (Figure total (42.7%) number5). The were oftotal individuals, males,number 3,416 of from indi (18.9%) bothviduals, depths, breeding from was both 18,090females, depths, out 5,199 ofwas which 18,090 (28.7%) out non- 7731of which (42.7%) 7,731 were (42.7%) males, 3,16 were (18.9%) males, breeding 3,416 females,(18.9%) 5199breeding (28.7%) females, non-breeding 5,199 females(28.7%) non- breeding females and 1,744 (9.6%) juveniles. Number of breeding females peaked in Au- andbreeding 1744 (9.6%) females juveniles. and 1,744 Number (9.6%) ofjuveniles. breeding Number females peakedof breeding in August, females November peaked in Au- gust, November and during February−April, whereas juveniles had increased numbers andgust, during November February and−April, during whereas February juveniles−April, had whereas increased juveniles numbers had during increased November– numbers during November–December and March–April. Sex ratio followed a different pattern be- Decemberduring November–December and March–April. Sex and ratio March–April. followed a different Sex ratio pattern followed between a different depths. pattern Al- be- thoughtween indepths.depths. most of AlthoughAlthough the samplings in in most most female of of the individuals the samp samplingslings were female morefemale individuals than individuals males (inwere absolutewere more more than than numbers),males (in sex absoluteabsolute ratio wasnumbers), numbers), not significantly sex sex ratio ratio was differentwas not not significantly fromsignificantly 1:1 for different the different surface from from population, 1:1 for1:1 thefor sur-the sur- except from the last sampling in July 2019. On the contrary, sex ratio of the deep population face population, except except from from the the last last sampling sampling in inJuly July 2019. 2019. On On the the contrary, contrary, sex sexratio ratio of of was significantly different from the expected equilibrium and always in favor of the females the deep populationpopulation was was significantly significantly different different from from the the expected expected equilibrium equilibrium and and always always in most samplings, except from November−February (Figure6). in favor ofof thethe females females in in most most samplings, samplings, except except from from November November−February−February (Figure (Figure 6). 6).

Figure 5. Temporal variation of all demographic categories of Caprella scaura from a fish farm in the Figure 5. Temporal variation of all demographic categories of Caprella scaura from a fish farm in the FigurePagasitikos 5. Temporal Gulf. variation of all demographic categories of Caprella scaura from a ﬁsh farm in the Pagasitikos Gulf. Pagasitikos Gulf.

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Figure 6. Temporal variation of Sex ratio of the surface and deep population of Caprella scaura from a fishFigure farm in 6. the Temporal Pagasitikos variation Gulf. Red asterisks of Sex (*)ratio indicate of the deviation surface from and 1:1. deep Values population over the dashed of Caprella scaura from linea fish indicate farm female in the dominance, Pagasitikos whereas Gulf. values Red below asterisks the dashed (* line) indicate indicate maledeviation dominance. from 1:1. Values over the dashed line indicate female dominance, whereas values below the dashed line indicate male domi- The total length (TL) of the 2990 measured individuals (1300 males, 1300 females and 390nance. juveniles), from both depths, ranged between 2.6−21.1 mm. TL values ranged between 5.4−21.1 mm for males, 5.0−10.3 mm for females and between 2.6−4.9 mm for juveniles (Table1).The Student’s total t-testlength revealed (TL) thatof the TL values2,990 hadmeasured significant individuals differences between (1,300 the males, 1,300 females twoand depth 390 levelsjuveniles), (p < 0.05). from One-way both depths, ANOVA, ranged on the otherbetween hand, 2.6 did− not21.1 detect mm. any TL values ranged be- differences in TL among the sampling months, either for surface (F = 0.67, p = 0.782) tween 5.4−21.1 mm for males, 5.0−10.3 mm for females12,1494 and between 2.6−4.9 mm for juve- or for deep (F12,1494 = 1.30, p = 0.212) populations. Fisher’s LSD procedure identified that maleniles size (Table was significantly 1). Student’s different t-test between revealed depths, that contrary TL values to female had and significant juvenile size. differences between Thethe length–frequency two depth levels distribution (p < 0.05). (LFD) One-way differed between ANOVA, sexes, withon th malese other exhibiting hand, a did not detect any wider size range than females. Females were more abundant in smaller TL size classes, differences in TL among the sampling months, either for surface (F12,1494 = 0.67, p = 0.782) but their numbers decreased significantly with the increase in size and no females larger thanor for 11 mm deep were (F found12,1494 = (Figure 1.30,7 ).p In= 0.212) fact, the populations. larger female (10.3 Fisher’s mm) was LSD smaller procedure in identified that sizemale than size the averagewas significantly size of all males different (10.7 mm between from Deep depths, and Surface contrary pooled data,to female data and juvenile size. notThe shown). length–frequency distribution (LFD) differed between sexes, with males exhibiting a

Tablewider 1. Minimum, size range maximum than and females. mean (± SD) Females total length were values (mm)more of theabundant different demographic in smaller TL size classes, categoriesbut their from numbers the surface anddecreased deep population significantly of Caprella scaurawithfrom the the increase Pagasitikos in Gulf. size and no females larger than 11 mm were found (Figure 7). In fact, the larger female (10.3 mm) was smaller in size Breeding Non-Breeding TL (mm) Males Juveniles than the average size of all malesFemales (10.7 mm fromFemales Deep and Surface pooled data, data not shown). Surface Minimum 5.8 5.6 5.1 2.6 TableMaximum 1. Minimum, maximum 21.1 and mean 10.1 (± SD) total 10.2 length values 4.9 (mm) of the different demo- ± ± ± ± ± graphicMean categoriesSD from 11.1 the3.0 surface 8.3and deep1.2 population 7.3 1.1 of Caprella 3.8scaura0.5 from the Pagasitikos Gulf. Deep Minimum 5.4 5.3 5.0Non-Breeding 2.8 Fe- TL (mm) Males Breeding Females Juveniles Maximum 19.0 10.2 10.3males 4.9 Mean (SD) 10.4 ± 2.6 8.3 ± 1.2 7.3 ± 1.3 3.9 ± 0.6 Surface Minimum 5.8 5.6 5.1 2.6 Maximum 21.1 10.1 10.2 4.9 Mean ± SD 11.1 ± 3.0 8.3 ± 1.2 7.3 ± 1.1 3.8 ± 0.5 Deep Minimum 5.4 5.3 5.0 2.8 Maximum 19.0 10.2 10.3 4.9 Mean (SD) 10.4 ± 2.6 8.3 ± 1.2 7.3 ± 1.3 3.9 ± 0.6

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Figure 7. Length–frequency distributions of (A). Male and (B). Female individuals from the Surface Figure 7. Length–frequency distributions of (A). Male and (B). Female individuals from the Surface and Deep populations of Caprella scaura, from a fish farm in the Pagasitikos Gulf. and Deep populations of Caprella scaura, from a ﬁsh farm in the Pagasitikos Gulf.

NumberNumber of of eggs eggs found found in in the the pouch pouch of of breeding breeding females females was was not not signiﬁcantly significantly different differ- betweenent between depths depths (t-test, (t-test,p < 0.05)p < 0.05) and and it was it was positively positively correlated correlated with with female female TL TL size size (Spearman’s(Spearman’s r r = = 0.720, 0.720,p p< < 0.05). 0.05). Brood Brood size size ranged ranged between between 11–53 11−53 eggs, eggs, with with an an average average valuevalue (± (±SD) SD) of of 30.3 30.3 ( ±(±9.2) 9.2) eggs eggs per per brood. brood.

4.4. Discussion Discussion InIn the the present present paper, paper, a newa new occurrence occurrence of Caprellaof Caprella scaura scaurais reported is reported for Greece,for Greece, raising rais- theing total the numbertotal number of country of country records records to three. to Contrary three. Contrary to the previous to the previous two reports two [ 32reports,47], where[32,47],C. where scaura wasC. scaura found was in marinas,found inthis marinas, is the firstthis is occurrence the first occurrence of the species of the on fishspecies farm on cagesfish farm and the cages first and in the the northern first in the part northern of the Aegean part of Sea, the thus Aegean expanding Sea, thus the northernmostexpanding the distributionnorthernmost range distribution of the species range in theof the region. species Additionally, in the region. this Additionally, is the first occurrence this is the of thefirst speciesoccurrence on a cageof the from species a sea on bream/sea a cage from bass a se farm,a bream/sea since to thebass previous farm, since record to the occurrence previous wasrecord from occurrence tuna farms was [14 ].from The tuna fact thatfarms there [14]. are Th overe fact 20,000 that there floating are fish over cages 20,000 along floating the Mediterraneanfish cages along coastline the Mediterranean and almost coastline half of them and are almost located half in of Greece them are [48 located] highlights in Greece the key[48] role highlights of fish farms the key as potentialrole of fish vectors farms andas potential facilitating vectors factor and for facilitating the establishment factor for and the spreadingestablishment of NIS and in thespreading whole Mediterraneanof NIS in the whole basin. Mediterranean basin. CaprellaCaprella scaura scaurawas was present present in in throughout throughout the the whole whole study study period period and, and, even even though though it wasit was not not possible possible to collectto collect relevant relevant data data from from the the other other fish fish farm farm in in the the region, region, our our initial initial resultsresults from from that that area area were were quite quite similar similar so so it it would would be be safe safe to to assume assume that that the the species species is is successfullysuccessfully established established in in the the Pagasitikos Pagasitikos Gulf. Gulf. The The presence presence of of the the species species did did not not seem seem toto be be affected affected directly directly by by the the fluctuations fluctuations of of the the measured measured abiotic abiotic factors factors (i.e., (i.e., temperature, temperature, salinity,salinity, dissolved dissolved oxygen), oxygen), which which indicates indicates a relative a relative tolerance tolerance to environmental to environmental variability. variability.Ovigerous females were present during the whole study, indicating that the species followsOvigerous the common females pattern were of present continuous during reproduction the whole throughout study, indicating the year, that which the species most caprellidsfollows the share common [30]. pattern A positive of continuous correlation repr betweenoduction body throughout and brood the sizeyear, was which found, most whichcaprellids is also share to be [30]. expected, A posi nottive only correlation in caprellids, between but in body amphipods and brood in general size was [30]. found, Most breeding females were recorded in summer and autumn, which probably marks the peak of which is also to be expected, not only in caprellids, but in amphipods in general [30]. Most the reproduction of the species for the Mediterranean, since similar findings were reported breeding females were recorded in summer and autumn, which probably marks the peak

J. Mar. Sci. Eng. 2021, 9, 857 9 of 12

in other studies [8,16]. Males were typically larger than females, which is considered an evolutionary trait associated with the reproductive process, either because females invest more energy in the production of eggs or because the aggressive behavior among males reduces the number of smaller-sized individuals [49]. Body size of males and females in our study are within the size range of other studies [8,16,32,33,50], with small differences between values, which can be attributed to the apparent ecophenotypic adaptation of the species to the different biotic and abiotic factors of each sampling location. The population density exhibited a periodic pattern for both depths, with peaks in June, October and March and the lowest values in January and February, but deeper populations had significantly lower densities. This small difference could be attributed to higher predation from fish. Fish farms are known to attract large aggregations of wild fish in mid waters around fish cages, as well as fish that escaped from within the cages [51], which may lead to an increase in predation since fish tend to select caprellids because of their clinging behavior, large size and visual contrast with their substrate [24,25]. Population density values from our study were similar to those recorded in the Ionian Sea [16], but lower than the high densities recorded in the Iberian Peninsula [8,33]. This variability could be attributed to the apparent differences in abiotic and biotic factors between the locations, as well as differences in the sampling methods. In any case, the results from all studies support the claim that C. scaura is a strong invader and is well established in the Mediterranean. The sex ratio was followed different patterns between depths. The shallow populations exhibited small monthly fluctuations with more females in one sampling and more males in another, but the ratio almost never deviated statistically from 1:1, except from the last sampling. On the contrary, the deeper populations displayed a strong female-biased sex ratio during the whole study and with most cases being statistically different from the 1:1 equilibrium. Usually, fluctuations in sex ratio can be attributed to different rates in growth, mortality or lifespan between sexes [30]. Female dominance could be explained again by the presence of more fish in deeper waters and males, because of their larger size are more visible and more susceptible to predation. This is probably why, apart from the difference in the sex ratio, larger males were also more scarce in deeper populations compared to the shallow population of our study. According to Fernandez-Gonzalez and Sanchez-Jerez [14], the different conditions in a sea bream/sea bass farm comparing to a tuna farm, especially high predation from fish, were preventing factors for the establishment of C. scaura on farm structures. Our finding shows that, even though predation could be a regulating factor, which could affect the growth of the population, it is possible for C. scaura to adapt and establish its presence even in sea bream farms. Most caprellid amphipods do not exhibit specific substrate preference [27,52], whereas C. scaura, although it has been reported from several habitats, seems to have a strong association with the bryozoan Bugula neritina [8,11,33,50,53]. The results from our study appear to support this association, since B. neritina was the dominant representative of the biofouling community during the whole sampling period and C. scaura was present throughout the whole study period. This affinity could be attributed to the cryptic adaptation of C. scaura to the bryozoan, since both species have similar coloration and external morphology. A similar association between a caprellid and B. neritina was reported for Caprella californica, a very close species to C. scaura, which seems to have the ability to undergo physical color changes in order to adapt to its substrate, contrary to C. equilibra, which was unable to adapt completely to dark substrates, such as B. neritina [54]. This is probably why C. equilibra was scarcely found during our study. Recent studies [8,11,14,55] seem to indicate that C. scaura is displacing C. equilibra from locations where it has been established, since they both compete for substrate use and C. scaura seems to perform better in terms of successful adaptation. Furthermore, since B. neritina is also considered as a NIS for the Mediterranean [56] and, apparently, it acts as a favorable substrate for the establishment of C. scaura, then J. Mar. Sci. Eng. 2021, 9, 857 10 of 13

J. Mar. Sci. Eng. 2021, 9, 857 10 of 12 Furthermore, since B. neritina is also considered as a NIS for the Mediterranean [56] and, apparently, it acts as a favorable substrate for the establishment of C. scaura, then this positive interaction could be assumed to be a typical case of “invasional meltdown”, wherethis positive an introduced interaction species could facilitates be assumed the es totablishment be a typical of case another of “invasional NIS [57]. meltdown”,Of course, furtherwhere research an introduced is needed species to confirm facilitates this the interaction, establishment but the of anotherhigh population NIS [57]. densities, Of course, thefurther potential research displacement is needed toof confirmother species this interaction, and the high but theadaptation high population ability of densities, C. scaura the C. scaura stronglypotential support displacement this assumption. of other species Even though and the this high could adaptation pose a ability threat of to local biodiver-strongly support this assumption. Even though this could pose a threat to local biodiversity, there sity, there are some potential benefits, which are probably worth looking into. First of all, are some potential benefits, which are probably worth looking into. First of all, B. neritina B. neritina is a source of a natural anti-cancer agent called “bryostatin”, so there is an in- is a source of a natural anti-cancer agent called “bryostatin”, so there is an increasing creasing interest in studying the species and exploring its exploitation [58–60]. On the interest in studying the species and exploring its exploitation [58–60]. On the other hand, other hand, caprellids have been found to be a potential alternative source of protein and caprellids have been found to be a potential alternative source of protein and lipids in lipids in fish feed production [25,40,41] and recently, C. scaura has been considered as a fish feed production [25,40,41] and recently, C. scaura has been considered as a candidate candidate species for use in Integrated Multi-Trophic Aquaculture (IMTA) Systems [28]. species for use in Integrated Multi-Trophic Aquaculture (IMTA) Systems [28]. Therefore, Therefore, this correlation between B. neritina and C. scaura could prove to be a valuable this correlation between B. neritina and C. scaura could prove to be a valuable asset in asset in the sustainable management of marine ecosystems, which might mitigate their the sustainable management of marine ecosystems, which might mitigate their impact as impact as biodiversity threats. Our study showed that it is possible to “cultivate” both of biodiversity threats. Our study showed that it is possible to “cultivate” both of these NIS on these NIS on artificial substrate around fish-farm cages, but further studies and field ex- artificial substrate around fish-farm cages, but further studies and field experimentations perimentationsare required in are this required direction, in withthis direction, the challenge with being the challenge the establishment being the of establishment safe and stable ofsystems safe and with stable an systems economically with an feasible economically output [ 28feasible]. output [28].

AuthorAuthor Contributions: Contributions: Conceptualization,Conceptualization, A.L. A.L. and and D.V.; methodology,methodology, A.L., A.L., I.T.K. I.T.K. and and P.P.; P.P; software, software,A.L.; A.L.; validation, validation, A.L., A.L., I.T.K. I.T.K. and D.V.;and D.V.; formal formal analysis, analysis, A.L. andA.L. D.V.;and D.V.; investigation, investigation, A.L.; A.L.; resources, resources, A.L. and P.P; data curation, A.L and D.V.; writing—original draft preparation, A.L. and A.L. and P.P.; data curation, A.L. and D.V.; writing—original draft preparation, A.L. and I.T.K.; I.T.K.; writing—review and editing, P.P. and D.V.; visualization, A.L.; supervision, I.T.K., P.P. and writing—review and editing, P.P. and D.V.; visualization, A.L.; supervision, I.T.K., P.P. and D.V.; D.V.; project administration, I.T.K. and P.P; funding acquisition, A.L. All authors have read and project administration, I.T.K. and P.P; funding acquisition, A.L. All authors have read and agreed to agreed to the published version of the manuscript. the published version of the manuscript. Funding: This research was supported by a postdoctoral scholarship program (Project number: Funding: This research was supported by a postdoctoral scholarship program (Project number: 5394.02.01), implemented by University of Thessaly and funded by the Stavros Niarchos Founda- 5394.02.01), implemented by University of Thessaly and funded by the Stavros Niarchos Foundation. tion. The APC was funded by the Stavros Niarchos Foundation. The APC was funded by the Stavros Niarchos Foundation.

InstitutionalInstitutional Review Review Board Board Statement: Statement: NotNot applicable. applicable. InformedInformed Consent Consent Statement: Statement: NotNot applicable. applicable. DataData Availability Availability Statement: Statement: NoNo data data reported. reported.

AcknowledgmentsAcknowledgments:: TheThe authors authors would would like like toto thank thank the the gradua graduatete students students Pasintelis Pasintelis K. K. and and Psyrra Psyrra E.E. and and the the post-graduate post-graduate student student Psofakis Psofakis P. P.for for their their valuable valuable help help during during the the samplings samplings and and lab lab analyses.analyses. They They would would also also like liketo extent to extent their theirgratitude gratitude to the to anonymous the anonymous reviewers reviewers for their for con- their structiveconstructive comments, comments, suggestions suggestions and remarks and remarks in the in preparation the preparation of this of manuscript. this manuscript. ConflictsConﬂicts of of Interest: Interest: TheThe authors declaredeclare nono conﬂict conflict of of interest. interest. The The funders funders had had norole no inrole the in design the designof the of study; the study; in the in collection, the collection, analyses, analyses, or interpretation or interpretation of data; of indata; the in writing the writing of the manuscript,of the manu- or script,in the or decision in the decision to publish to publish the results. the results.

ReferencesReferences 1.1. Tsiamis,Tsiamis, K.; K.; Zenetos, Zenetos, A.; A.; Deriu, Deriu, I.; I.;Gervasini, Gervasini, E.; E.; Cardoso, Cardoso, A. A.C.C. The The native native distribution distribution rang rangee of ofthe the European European marine marine non- non- indigenousindigenous species. species. Aquat.Aquat. Invasions Invasions 20182018, 13, 13, 187–198,, 187–198. doi:10.3391/ai.2018.13.2.01. [CrossRef] 2.2. Galil,Galil, B.S.; B.S.; Marchini, Marchini, A.; A.; Occhipinti-Ambrogi, Occhipinti-Ambrogi, A. A. East East is iseast east and and West West is is west? west? Management Management of of marine marine bioinvasions bioinvasions in in the the MediterraneanMediterranean Sea. Sea. Estuar.Estuar. Coast. Coast. Shelf Shelf Sci. Sci. 20182018, 201, 201, 7–16,, 7–16. doi:10.1016/j.ecss.2015.12.021. [CrossRef] 3.3. Elliott,Elliott, M. M. Biolog Biologicalical pollutants pollutants and and biological biological polluti pollution—-Anon––an increasing increasing cause cause for for concern. concern. Mar.Mar. Pollut. Pollut. Bull. Bull. 20032003, 46, 46, 275–280,, 275–280. doi:10.1016/S0025-326X(02)00423-X.[CrossRef] 4. Occhipinti-Ambrogi, A. Global change and marine communities: Alien species and climate change. Mar. Pollut. Bull. 2007, 55, 342–352. [CrossRef][PubMed] 5. Keller, R.P.; Geist, J.; Jeschke, J.M.; Kühn, I. Invasive species in Europe: Ecology, status, and policy. Environ. Sci. Eur. 2011, 23, 23. [CrossRef]

J. Mar. Sci. Eng. 2021, 9, 857 11 of 12

6. Hänfling, B.; Edwards, F.; Gherardi, F. Invasive alien Crustacea: Dispersal, establishment, impact and control. BioControl 2011, 56, 573–595. [CrossRef] 7. Martínez-Laiz, G.; Ulman, A.; Ros, M.; Marchini, A. Is recreational boating a potential vector for non-indigenous peracarid crustaceans in the Mediterranean Sea? A combined biological and social approach. Mar. Pollut. Bull. 2019, 140, 403–415. [CrossRef] 8. Guerra-García, J.M.; Ros, M.; Dugo-Cota, A.; Burgos, V.; Flores-León, A.M.; Baeza-Rojano, E.; Cabezas, M.P.; Núñez, J. Geographi- cal expansion of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) to the East Atlantic coast. Mar. Biol. 2011, 158, 2617–2622. [CrossRef] 9. Ashton, G.V.; Boos, K.; Shucksmith, R.; Cook, E.J. Risk assessment of hull fouling as a vector for marine non-natives in Scotland. Aquat. Invasions 2006, 1, 214–218. [CrossRef] 10. Ashton, G.V.; Burrows, M.T.; Willis, K.J.; Cook, E.J. Seasonal population dynamics of the non-native Caprella mutica (Crustacea, Amphipoda) on the west coast of Scotland. Mar. Freshw. Res. 2010, 61, 549–559. [CrossRef] 11. Ros, M.; Guerra-García, J.M.; González-Macías, M.; Saavedra, Á.; López-Fe, C.M. Influence of fouling communities on the establishment success of alien caprellids (Crustacea: Amphipoda) in Southern Spain. Mar. Biol. Res. 2013, 9, 261–273. [CrossRef] 12. Fernandez-Gonzalez, V.; Sanchez-Jerez, P. Fouling assemblages associated with off-coast aquaculture facilities: An overall assessment of the Mediterranean Sea. Mediterr. Mar. Sci. 2017, 18, 87–96. [CrossRef] 13. Ros, M.; Vázquez-Luis, M.; Guerra-García, J.M. The role of marinas and recreational boating in the occurrence and distribution of exotic caprellids (Crustacea: Amphipoda) in the Western Mediterranean: Mallorca Island as a case study. J. Sea Res. 2013, 83, 94–103. [CrossRef] 14. Fernandez-Gonzalez, V.; Sanchez-Jerez, P. First occurrence of Caprella scaura Templeton, 1836 (Crustacea: Amphipoda) on off-coast fish farm cages in the Mediterranean Sea. Helgol. Mar. Res. 2014, 68, 187–191. [CrossRef] 15. Guerra-García, J.M.; Ros, M.; Baeza-Rojano, E. Seasonal fluctuations and dietary analysis of fouling caprellids (Crustacea: Amphipoda) from marinas of southern Spain. Mar. Biol. Res. 2015, 11, 703–715. [CrossRef] 16. Prato, E.; Parlapiano, I.; Biandolino, F. Seasonal fluctuations of some biological traits of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) in the Mar Piccolo of Taranto (Ionian Sea, southern Italy). Sci. Mar. 2013, 77, 169–178. [CrossRef] 17. Weis, J.S. The role of behavior in the success of invasive crustaceans. Mar. Freshw. Behav. Physiol. 2010, 43, 83–98. [CrossRef] 18. Galil, B.S. The Alien Crustaceans in the Mediterranean Sea: An Historical Review. In In the Wrong Place—Alien Marine Crustaceans: Distribution, Biology and Impacts; Galil, B.S., Clark, P.F., Carlton, J.T., Eds.; Springer: Dordrecht, The Netherlands, 2011; pp. 377–401. 19. Galil, B.S. Alien species in the Mediterranean Sea—which, when, where, why? Hydrobiologia 2008, 606, 105–116. [CrossRef] 20. Laubitz, D.R.; Mills, E.L. Deep-sea Amphipoda from the western North Atlantic Ocean. Caprellidea. Can. J. Zool. 1972, 50, 371–383. [CrossRef] 21. Takeuchi, I.; Sawamoto, S. Distribution of caprellid amphipods (Crustacea) in the western North Pacific based on the CSK International Zooplankton Collection. Plankton Biol. Ecol. 1998, 45, 225–230. 22. Guerra-García, J.M.; García-Gómez, J.C. The Spatial Distribution of Caprellidea (Crustacea: Amphipoda): A Stress Bioindicator in Ceuta (North Africa, Gibraltar Area). Mar. Ecol. 2001, 22, 357–367. [CrossRef] 23. Díaz, Y.J.; Guerra-García, J.M.; Martín, A. Caprellids (Crustacea: Amphipoda: Caprellidae) from shallow waters of the Caribbean coast of Venezuela. Org. Divers. Evol. 2005, 5, 1–25. [CrossRef] 24. Caine, E.A. Caprellid amphipods: Fast food for the reproductively active. J. Exp. Mar. Biol. Ecol. 1991, 148, 27–33. [CrossRef] 25. Woods, C.M.C. Caprellid amphipods: An overlooked marine finfish aquaculture resource? Aquaculture 2009, 289, 199–211. [CrossRef] 26. Boos, K. Mechanisms of a Successful Immigration from North-East Asia: Population Dynamics, Life History Traits and Interspecific Interactions in the Caprellid Amphipod Caprella Mutica Schurin, 1935 (Crustacea, Amphipoda) in European Coastal Waters; Freie Univertität: Berlin, Germany, 2009. 27. Guerra-García, J.M. Habitat use of the caprellidea (Crustacea: Amphipoda) from Ceuta, North Africa. Ophelia 2001, 55, 27–38. [CrossRef] 28. Guerra-García, J.M.; Hachero-Cruzado, I.; González-Romero, P.; Jiménez-Prada, P.; Cassell, C.; Ros, M. Towards Integrated Multi-Trophic Aquaculture: Lessons from Caprellids (Crustacea: Amphipoda). PLoS ONE 2016, 11, e0154776. [CrossRef] 29. González, A.R.; Guerra-García, J.M.; Maestre, M.J.; Ruiz-Tabares, A.; Espinosa, F.; Gordillo, I.; Sánchez-Moyano, J.E.; García- Gómez, J.C. Community structure of caprellids (Crustacea: Amphipoda: Caprellidae) on seagrasses from southern Spain. Helgol. Mar. Res. 2008, 62, 189–199. [CrossRef] 30. Caine, E.A. Population structures of two species of Caprellid amphipods (Crustacea). J. Exp. Mar. Biol. Ecol. 1979, 40, 103–114. [CrossRef] 31. Nuñez Velazquez, S.; Rumbold, C.E.; Obenat, S.M. Population dynamics of Caprella dilatata and Caprella equilibra (Peracarida: Amphipoda) in a Southwestern Atlantic harbour. Mar. Biol. Res. 2017, 13, 888–898. [CrossRef] 32. Krapp, T.; Lang, C.; Libertini, A.; Melzer, R.R. Caprella scaura Templeton, 1836 sensu lato (Amphipoda: Caprellidae) in the Mediterranean. Org. Divers. Evol. 2006, 6, 77–81. [CrossRef] 33. Martínez, J.; Adarraga, I. First record of invasive caprellid Caprella scaura Templeton, 1836 sensu lato (Crustacea: Amphipoda: Caprellidae) from the Iberian Peninsula. Aquat. Invasions 2008, 3, 165–171. [CrossRef] J. Mar. Sci. Eng. 2021, 9, 857 12 of 12

34. Mizzan, L. Le specie alloctone del macrozoobenthos della Laguna di Venezia: Il punto della situazione. Boll. Mus. Civ. Stor. Nat. Venezia 1999, 49, 145–177. 35. Sconfietti, R.; Mangili, F.; Savini, D.; Occhipinti-Ambrogi, A. Diffusion of the alien species Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the northern Adriatic Sea. Biol. Mar. Mediterr. 2005, 12, 335–337. 36. Bakır, K.; Kata˘gan,T. On the occurrence of Caprella scaura Templeton, 1836 (Crustacea: Amphipoda) in Turkish waters. Zool. Middle East 2011, 52, 125–126. [CrossRef] 37. Cabezas, M.P.; Xavier, R.; Branco, M.; Santos, A.M.; Guerra-García, J.M. Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Iberian Peninsula: Multiple introductions revealed by mitochondrial sequence data. Biol. Invasions 2014, 16, 2221–2245. [CrossRef] 38. Dailianis, T.; Akyol, O.; Babali, N.; Bariche, M.; Crocetta, F.; Gerovasileiou, V.; Chanem, R.; Göko˘glu,M.; Hasiotis, T.; Izquierdo- Muñoz, A.; et al. New Mediterranean Biodiversity Records (July 2016). Mediterr. Mar. Sci. 2016, 12, 608–626. [CrossRef] 39. Chebaane, S.; Shaiek, M.; Zakhama-Sraieb, R. A new record and range extension of an invasive amphipod Caprella scaura Templeton, 1836 in Tunisia, North Africa. J. Black Sea Mediterr. Environ. 2018, 24, 255–262. 40. Guerra-García, J.M.; Martínez-Pita, I.; Pita, M.L. Fatty acid composition of the Caprellidea (Crustacea: Amphipoda) from the Strait of Gibraltar. Sci. Mar. 2004, 68, 501–510. [CrossRef] 41. Cook, E.J.; Shucksmith, R.; Orr, H.; Ashton, G.V.; Berge, J. Fatty acid composition as a dietary indicator of the invasive caprellid, Caprella mutica (Crustacea: Amphipoda). Mar. Biol. 2010, 157, 19–27. [CrossRef] 42. Baeza-Rojano, E.; Hachero-Cruzado, I.; Guerra-García, J.M. Nutritional analysis of freshwater and marine amphipods from the Strait of Gibraltar and potential aquaculture applications. J. Sea Res. 2014, 85, 29–36. [CrossRef] 43. Lolas, A.; Vafidis, D. Population dynamics of two caprellid species (Crustaceae: Amphipoda: Caprellidae) from shallow hard bottom assemblages. Mar. Biodivers. 2013, 43, 227–236. [CrossRef] 44. Guerra-García, J.M. The Caprellidea (Crustacea: Amphipoda) from Mauritius Island, Western Indian Ocean. Zootaxa 2003, 232, 1–24. [CrossRef] 45. Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9, 671–675. [CrossRef][PubMed] 46. Lolas, A.; Vafidis, D. Population Dynamics, Fishery, and Exploitation Status of Norway Lobster (Nephrops norvegicus) in Eastern Mediterranean. Water 2021, 13, 289. [CrossRef] 47. Ros Clemente, M. The spreading of the non-native caprellid (Crustacea: Amphipoda) Caprella scaura Templeton, 1836 into southern Europe and northern Africa: A complicated taxonomic history. Mediterr. Mar. Sci. 2014, 15, 145–155. [CrossRef] 48. Trujillo, P.; Piroddi, C.; Jacquet, J. Fish Farms at Sea: The Ground Truth from Google Earth. PLoS ONE 2012, 7, e30546. [CrossRef] [PubMed] 49. Caine, E.A. Reproductive Behavior and Sexual Dimorphism of a Caprellid Amphipod. J. Crustacean Biol. 1991, 11, 56–63. [CrossRef] 50. Ramalhosa, P.; Canning-Clode, J. The invasive caprellid Caprella scaura Templeton, 1836 (Crustacea: Amphipoda: Caprellidae) arrives on Madeira Island, Portugal. BioInvasions Rec. 2015, 4.[CrossRef] 51. Tim, D.; Pablo, S.-J.; Just, T.B.-S.; Francisca, G.-C.; Carlos, V. Attraction of wild fish to sea-cage fish farms in the south-western Mediterranean Sea: Spatial and short-term temporal variability. Mar. Ecol. Prog. Ser. 2002, 242, 237–252. [CrossRef] 52. Caine, E.A. Ecology of two littoral species of caprellid amphipods (Crustacea) from Washington, USA. Mar. Biol. 1980, 56, 327–335. [CrossRef] 53. Molina, S.; Ros, M.; Guerra-García, J.M. Distribution of the Invasive Caprellid Caprella scaura (Crustacea: Amphipoda) in Cádiz Marina, Southern Spain: Implications for its Dispersal. Thalass. Int. J. Mar. Sci. 2017, 33, 81–86. [CrossRef] 54. Keith, D.E. Substrate selection in caprellid amphipods of Southern California, with emphasis on Caprella californica Stimpson and Caprella equilibra Say (Amphipoda). Pac. Sci. 1971, 25, 387–394. 55. Conradi, M.; López-González, P.J.; Cervera, J.L.; García-Gómez, J.C. Seasonality and Spatial Distribution of Peracarids Associated with the Bryozoan Bugula neritina in Algeciras Bay, Spain. J. Crustacean Biol. 2000, 20, 334–349. [CrossRef] 56. Ryland, J.S.; Bishop, J.D.D.; Blauwe, H.D.; El-Nagar, A.; Minchin, D.; Wood, C.A.; Yunnie, A.L.E. Alien species of Bugula (Bryozoa) along the Atlantic coasts of Europe. Aquat. Invasions 2011, 6, 17–31. [CrossRef] 57. Simberloff, D.; Von Holle, B. Positive Interactions of Nonindigenous Species: Invasional Meltdown? Biol. Invasions 1999, 1, 21–32. [CrossRef] 58. Manning, T.J.; Land, M.; Rhodes, E.; Chamberlin, L.; Rudloe, J.; Phillips, D.; Lam, T.T.; Purcell, J.; Cooper, H.J.; Emmett, M.R.; et al. Identifying bryostatins and potential precursors from the bryozoan Bugula neritina. Nat. Prod. Res. 2005, 19, 467–491. [CrossRef] [PubMed] 59. Fehlauer-Ale, K.H.; Mackie, J.A.; Lim-Fong, G.E.; Ale, E.; Pie, M.R.; Waeschenbach, A. Cryptic species in the cosmopolitan Bugula neritina complex (Bryozoa, Cheilostomata). Zool. Scr. 2014, 43, 193–205. [CrossRef] 60. Ciavatta, M.L.; Lefranc, F.; Vieira, L.M.; Kiss, R.; Carbone, M.; van Otterlo, W.A.L.; Lopanik, N.B.; Waeschenbach, A. The Phylum Bryozoa: From Biology to Biomedical Potential. Mar. Drugs 2020, 18, 200. [CrossRef]