The seasonal fish diversity of Aliağa, a heavy industry zone on the Turkish coast of the Aegean Sea

The stress on the marine environment caused by industrialization in developing economies is indisputable. The Aliağa region, which has unique features such as being heavily influenced by industrialization and having different types of marine habitats was preferred as a monitoring point. By determining the current status of fish density and diversity, the focus was on obtaining data that could allow future comparisons. Without the seasonal variability, 39 fish species representing 14 families were identified, with two abundant families: ten species in both Sparidae and Labridae. The greatest fish diversity was recorded respectively in the spring, summer and autumn. Abundant species were Boops boops with 19.3%, Chromis chromis (17.4%), Spicara smaris (15.0%) and Atherina boyeri (12.5%) in total abundance. A total of 1.89 individuals/m 2 that weighed 20.43 g/m 2 were identified in the study period.


Introduction
Fishes are an essential component in marine ecosystems; however, at present, they are threatened by anthropogenic stressors (Pauly et al., 2002;Lotze et al., 2006). Fish biodiversity which represents an important indicator in determining ecosystem health (McField & Kramer, 2007), is an assessment of different fish species living in a particular area, and also * Corresponding author E-mail address: acaglaroruc@gmail.com (A. Ç. Oruç) provides numerous and valuable ecosystem goods and services (Worm et al., 2006;Beaumont et al., 2007;Halpern et al.,2012).
The advantages of fish-based monitoring of the ecosystem health described in detail in Whitfield & Elliott (2002) are that; they are present in almost all aquatic ecosystems; have information about the extensive life history and environmental response; they are easy for species identification; harmless

Oruç (2022) Marine Science and Technology Bulletin 11(3): 361-368
362 sampling is available; various trophic levels that provide a longterm record of environmental stress.
Industrial activities play a significant role in the economies of the countries. Aliağa is one of the most important heavy industry zones in Turkey and has the only shipbreaking industry among OECD countries in the Mediterranean region.
The negative effects of marine traffic and port activities on marine habitats are ship pollution and emissions, collisions and noise, grounding and anchoring damage, and transportation of non-indigenous species (Abdulla & Linden, 2008;Brynolf et al., 2016). Increasing industrial activities in Aliağa and the environmental effects of these activities make the region riskier.
Long-term data is required to determine the changes in marine ecosystems directly affected by intense industrial activities. This study aimed to determine the current status of fish biodiversity in a marine industrial zone and provide a comparison source for future research.

Figure 1. Study area
The non-destructive underwater visual census (UVCs) method (Harmelin-Vivien et al., 1985;Engin et al., 2018) was used following the 700 meters route marked on the map by two free divers both with experience in situ identification of fish species. UVCs were carried out in four seasons (December 2019-October 2020) and on a random date for each season between 9.00 a.m. and 11.00 a.m. The study was conducted on shallow waters between 0-10 meters in depth as they generally have high primary and secondary productivity levels maintaining the richest ichthyofauna (García-Rubies & Zabala, 1990). Two replications were performed (2 × 700 m in the same route) per season. Species, abundances, and size structure of fishes were recorded on a waterproof notepad. Divers simultaneously recorded their observations on the same route.
The mean density data were used in the calculations to reduce the error rate that may arise from the divers.
Fish species richness and dominancy were evaluated using the Shannon-Weiner diversity index (H'), Margalef richness index (Dmg) and Pielou's evenness (J') index. Bray-Curtis similarity index, non-metric multidimensional scaling (nMDS), and similarity percentage (SIMPER) were performed using the Primer-E v7 package software to detect seasonal differences.

Results
A total of 10607 individuals (weighing 114.453 kg) of 39 species belonging to 14 families were observed in the study area.
The most diverse families of the fish assemblage were Labridae and Sparidae, with 10 species each (Labridae 25.6%; Sparidae 25.6% of the total number of species). Blenniidae and Gobiidae were the other species-rich families, with 4 and 3 species (Table   1; Figure 2).
The highest fish density was found in spring (2.88 fish/m 2 ), and the highest biomass was found in autumn (28.2 g/m 2 ). The lowest density (0.5 fish/m 2 ) and biomass (11.75 g/m 2 ) were found in winter.
On the basis of the species richness, the highest number of species (38) was registered in spring, most of the species were belonging to Sparidae (10) and Labridae (9) families. In contrast, the lowest number of species (30) were registered in winter dominance with sparid fishes (9) and wrasses (8) again.
A decrease was observed in the number of total recorded species after spring, and equal numbers were determined in summer (35) and autumn (35) (Table 1, Figure 2).    The highest value of the Pielou's evenness (J') index was calculated in winter (0.68) and the lowest in spring (0.61) ( Table   2). Comparisons of diversity indices did not reveal significant differences between seasons (p<0.05).
Bray-Curtis similarity analysis based on the counted number of individuals for the seasons were calculated (p<0.05), the maximum similarity between summer and autumn the minimum similarity between winter and summer-autumn ( Figure 3). Non-metric multidimensional scaling (nMDS) based on Bray-Curtis similarities data showed approximately 90% similarity among the spring, summer, and autumn, however, the cold season (winter) was the least similar to others (70%) (Figure 4).

Discussion
The Mediterranean is the largest and deepest enclosed sea that occupies 0.8% of the surface area of the world's oceans (Bianchi & Morri, 2000;Psomadakis et al., 2012). Although it covers a small area, the Mediterranean Sea is a region of high biodiversity, with 7.5% marine fauna and 18% of the marine flora of the world's oceans (Fossi & Lauriano, 2008). However, the sensitive shallow and deep-sea habitats of the Mediterranean are under the influence of industrialization, such as a high volume of marine traffic and port activities (Abdulla & Linden, 2008).
Results of the Simper analysis based on seasonal abundance data of the species data showed that the maximum dissimilarity among the seasons was spring-winter (26.9%), and the minimum was summer-autumn (5.9%). The fish species that caused the difference between seasons are given in Table 3.  Because fishes are sensitive and mobile organisms, they respond more quickly to ecosystem changes than sessile organisms. Due to this reason, they are suitable indicators of ecosystem changes (Harrison & Whitfield, 2004;Breine et al., 2007;Martinho et al., 2015;Souza & Vianna, 2020). This study focused on fish diversity that was used as an indicator, and seasonal monitoring was carried out for one year using the UVC method.
Previous studies using the UVC method to investigate fish biodiversity on the eastern coast of the Aegean Sea were reviewed, focusing on a particular habitat (artificial habitats, reefs or islands) or fish group (cryptobenthics). In terms of fish biodiversity, in previous studies conducted on artificial habitats such as shipwrecks and sea-cage fish farms, and natural reefs, it has been stated that 27-40 fish species belong to 10-22 families (Gül et al., 2006(Gül et al., , 2011Lök et al., 2008;Akyol et al., 2019;Acarlı et al., 2020). In addition, in the other studies that focused on the cryptobenthic fishes, 19 species were stated by Dalyan et al. (2021), 23 species by Kesici & Dalyan (2020), and 33 gobiid species were stated from the northeastern Aegean by Engin et al. (2018). In the scope of this study, 39 species belonging to 14 families were observed in the natural habitat. In common with Lök et al. (2008), De Raedemaecker et al. (2010, Gül et al. (2011), Akyol et al. (2019 and Acarlı et al. (2020) the most diverse families were Sparidae and Labridae. This was interpreted as a usual case on the Mediterranean rocky shores (Harmelin, 1987;Ruitton et al., 2000). B. boops was the frequently dominant fish species from the family in this study (19.3% in total abundance; 34.1% in total biomass) which is similar to findings from previous studies focused on fish biodiversity in artificial habitats (Fernandez-Jover et al., 2008;Arechavala-Lopez et al., 2011;Šegvić Bubić et al., 2011;Acarlı et al., 2020). B. boops is abundant and widely distributed from the Eastern Atlantic to the Mediterranean and the Black Sea and inhabits all types of habitats (Bauchot & Hureau, 1986). In (2020), and also summer and autumn were stated as highest by Gül et al. (2006). Species distribution and abundance were associated with environmental factors in seasonal changes which typically increased during summer and decreased during winter (Jin & Tang, 1996). In spring and early summer, an increase in abundance with new additions to fish stocks, a decrease in abundance and species number in winter, but an increase in biomass were determined. Also, the simper analysis based on abundance calculated the highest average dissimilarity between spring and winter with 26.9%.
As a result of Simper analysis based on seasonal fish abundance data, the highest average uniqueness was calculated between spring and winter. Also, the simper analysis based on abundance show the maximum average dissimilarity between spring and winter with 26.9%.
The coastal marine area that conducted this study has a unique structure as it includes different habitats such as rocks, sand, seagrass, island slope and also being under the influence of marine traffic and port activities. It is known that the more heterogeneous habitats provide substrata for feeding, recruitment, and refuge from predators (Ruitton et al., 2000;Aburto-Oropeza & Balart, 2001;De Raedemaecker et al., 2010).

Conclusion
The importance of industrialization in the economies of countries is indisputable. However, determining the negative effects of industrialization on marine ecosystems is a global problem that needs long-term observations. Fish biodiversity represents an important indicator in determining ecosystem health. This study aimed to determine the current status of fish biodiversity in Aliağa which is an affected area by heavy industrial activities and marine traffic. Without the seasonal variability, a total of 10607 individuals (weighing 114.453 kg) of 39 species belonging to 14 families were observed in the study area. The most diverse families of the fish assemblage were Labridae and Sparidae, with 10 species each. The greatest fish diversity was recorded in the spring. In the fish-based monitoring studies on Turkish coasts, researchers have focused on artificial reefs or island ecosystems but coastal ecosystems especially those located in industrial areas have not been studied enough. Should be given due sensitivity to this type of marine ecosystem and more intensive, long-term periodical surveys should be carried out in these areas. Long-term data is required to determine anthropogenic activities' effects on marine ecosystems. For this purpose, the current status of a special region that needs continuous assessment of fish biodiversity was determined, and basic data were obtained to reveal the changes in the future.

Conflict of Interest
The author declares that there is no conflict of interest.

Ethical Approval
For this type of study, formal consent is not required.