Diet composition and feeding strategy of John Dory, Zeus faber, in the coastal waters of Korea

Most fish undergo prey switch from juvenile to adult. It is thought that slightly different feeding habits occur among adult fishes due to growth, spawning, habitat change, and so on. Therefore, the diet of the John Dory Zeus faber (≥ 24 cm TL) was studied in the coastal waters of Korea by analysis of stomach contents, with comparison by season and size class of diet composition and prey diversity. Monthly samples were taken from February 2017 to January 2018. The results showed that the John Dory was a piscivorous predator, and pisces had occupied 82.3% of IRI%. Trichiurus lepturus and Trachurus japonicus were important preys in all size classes and seasons. Diet composition differed among the size classes and seasons (Chi-square test, P < 0.05). As body size of Z. faber increased, the occurrence of benthic fish (Glyptocephalus stelleri) tended to increase. The seasonal prey composition also changed depending on the abundant species of each season. Z. faber is a piscivorous predator. The consumption habits of Z. faber appear to different results by their size and seasons. This study suggests that Z. faber could be considered an opportunistic predator.


Background
John Dory (Zeus faber Linnaeus, 1758) is widely distributed in the Atlantic, Pacific, and Indian oceans, as well as along the entire West African coast (Janssen 1979;Akyol 2001;Yoneda et al. 2002). In Korea, they are distributed on the South Sea and East Sea of Korea (Choi et al. 2011). This species is a demersal fish, inhabiting depths of 50-140 m (Vrgoč et al. 2006;Kim et al. 2013). In Korea, the commercial value of Z. faber has recently increased but is treated as bycatch. It is thought that research on their basic ecology is necessary.
Previous studies on feeding habits of Z. faber were conducted in eastern Mediterranean Sea (Stergiou and Fourtouni 1991), Portuguese coast (Silva 1999), North Aegean Sea (Ismen et al. 2013), and South Sea in Korea (Choi et al. 2011;An et al. 2012). All results of them shown that Z. faber is a piscivorous predator. However, these studies lack the ecological study on feeding habits because there is only descriptive information about the prey composition of Z. faber. To understand the overall dynamics of community feeding ecology, it is necessary to investigate higher predators within marine trophic food webs.
Most fish undergo prey switch. Diet shifts in fish can be influenced by season, environmental factors, interspecific composition, ontogeny, and body size (Gerking 1994;Preciado et al. 2006;Cusa et al. 2019). The prey composition of Z. faber also vary with ontogeny. Stergiou and Fourtouni (1991) suggested that changes in feeding can occur based on 14 cm TL. When > 14 cm TL, Z. faber consumes benthic and demersal fish exclusively (Stergiou and Fourtouni 1991). On the other hand, diets of Z. faber from along the Portuguese coastline do not show distinct changes (Silva 1999). These studies focused on the dietary changes from juvenile to adult. However, this study thought that the diet of adult Z. faber varies with body size, season, and feeding strategy. The objectives of this study were to reveal the overall diet composition and feeding strategy for specimens of ≥ 24 cm TL in the coastal waters of Korea.

Sample collection
A total of 711 samples were monthly collected between February 2017 and January 2018 by commercial bottom trawl net in the coastal waters of Korea (35°58′N 129°50′E). Bottom trawl mesh size was 54 mm, and net length was about 40.8 m. The samplings were conducted around 2 h at a time. All samples were brought in thermos cool boxes to the laboratory. Fish specimens were collected in the range from 24 to 47 cm (mean ± SD: 34.10 ± 4.21) in total length (TL) and from 221.01 to 2458.35 g (mean ± SD: 679.42 ± 278.17) in total weight (TW) ( Table 1).

Analysis of stomach contents
Stomachs of 711 individuals were dissected, and prey items in the stomachs were classified to the lowest taxonomic level by the naked eye and under microscope. Biomass and length of all prey items were measured with an electronic balance to the nearest 0.01 g and the nearest millimeter. A regression analysis was performed using excel to observe the changes in lengths of prey items according to the sizes of Z. faber.
Feeding habits were determined by using the index (Hyslop 1980): (1) the frequency of occurrence (%F), (2) the numerical percentage (%N), (3) the weight percentage (%W), and (4) the index of relative importance (IRI). Indices were calculated for each stomach as follows: A i is the number of fish with prey i (th) in their stomach, N is the total number of fish with stomach contents, N i is the number of prey i (th), N total is the total number of prey items W i is the mass of prey i (th), and W total is the total mass of prey items. IRI was converted into a percentage and expressed as %IRI.
Seasonal variation of diet was investigated for four seasons: spring (March-May, n = 150), summer (June-August, n = 161), autumn (September-November, n = 210), and winter (December-February, n = 190). Statistical differences in diet composition among size classes and seasons were employed by a chi-square test of the frequencies of a given prey categories (Sokal and Rohlf 1995). Niche breadth analysis was conducted using the Shannon-Wiener diversity index (H') (Colwell and Futuyma 1971), where P i is the proportion of individuals belonging to i th species. s is the total number of different prey categories consumed by predator. The value of H' increases with species diversity.

Diet compositions
Of the 711 stomachs examined, a total of 24 prey species were found. Percentage of empty was 47.3%. Prey items were divided into three categories: pisces, crustacean, and Cephalopoda. The index of relative importance (IRI) analysis recovered pisces as the most important prey category (82.3%), followed by crustaceans (17.5%) and Cephalopoda (0.3%) ( Table 2). Z. faber were shown to be piscivorous that consume fishes as principal prey items.

Difference of diet by size class
For each of the four size classes, Trichiurus japonicus and Trachurus japonicus were the most common prey by biomass (Fig. 1). Engraulis japonicus was an important prey in the 24-30 cm and 31-35 cm size classes, but the occurrence of E. japonicus from the 36-40 cm group was greatly reduced. In the large fish (> 38 cm), the proportion of Glyptocephalus stelleri increased markedly. There is no significant difference in the size of the prey items (Trichiurus japonicus, E. japonicus, Trachurus japonicus, and G. stelleri) according to the TL (P > 0.05). There was a significant difference in the proportions of prey categories consumed by the four size classes (x 2 = 318.24, df = 24, P < 0.001).

Difference of diet by season class
In all seasons, Trichiurus japonicus and Trachurus japonicus were consumed (Fig. 2). Trichiurus japonicus was the most common prey item by %IRI in spring (34.9%) and summer (31.3%). Overall crustacean prey biomass increased during summer and autumn. In autumn, E. japonicus dominated the prey mass, making up 37.4% of the total diet, respectively. %IRI of Trachurus japonicus and G. stelleri increased in winter to 16.8% and 11.9%, respectively. We found a significant difference in diet compositions among seasons (x 2 = 499.41, df = 24, P < 0.001).

Difference of diet by size and season
There were variation of diet in size group by season, as shown in the percentage of IRI (Fig. 3). Dominant preys of 24-30 cm group consisted of pelagic fishes in all the seasons; Trichiurus japonicus in spring (93.5%) and summer (29.3%), E. japonicus (63.4%) in autumn, and Trachurus japonicus (50.0%) in winter (Fig. 3). In 31-35 cm group, Trichiurus japonicus (35.5%) was consumed as dominant preys in spring, and crustacean was mainly prey items in summer (45.9%) and autumn (59.8%). In winter, Acropoma japonicum and Trachurus japonicus were dominant, making up 46.0% and 31.5%, respectively. In 36-40 cm group, Trichiurus japonicus was the most important prey item in all the seasons. In 41-47 cm group, G. stelleri was consumed as a main prey item in all the seasons expect autumn in which Psenopsis anomala (58.4%) and Larimichthys crocea (29.4%) were consumed.

Trophic diversity
Trophic diversity of Z. faber was generally low. Among the size classes, trophic diversity was highest in the 31- 35 cm group and lowest in the 24-30 cm group (Fig. 4a). This confirmed that as body size increased, dietary variability also increased. In terms of season, autumn and summer obtained the highest trophic diversity (Fig. 4b), indicating that more prey items were consumed during this time period than in other seasons.

Discussion
The diet of Z. faber consisted of a limited range of prey items from cephalopods to pisces. It was a total of 24 prey species. Despite the fact that Z. faber fed on a range of prey items, fish dominated the diet in all seasons. In particular, Trichiurus japonicus, Trachurus japonicus, and E. japonicus were consumed in all seasons, which was similar to all the previous studies performed in Korea (Huh et al. 2006;Choi et al. 2011;An et al. 2012). Z. faber has narrow dietary niche width (15-24 prey items) in all previous studies (Huh et al. 2006;Choi et al. 2011;An et al. 2012), which is one of the characteristics of piscivorous fish. This feeding behavior could be attributed to a large mouth, suction capabilities, and extensive swimming maneuverability (Stergiou and Fourtouni 1991;An et al. 2012). In the Gori study, however, the main preys included Psenopsis anomala, Conger myriaster, and Glossando semifasciata (Huh et al. 2006). In Geomun-island, dominant preys consisted of Scomber japonicus and Callanthias japonicus ). These results indicated that the prey items varied with habitats. Z. faber are opportunistic species which consume mainly abundant and diverse species according to habitat. Similar results are observed in other fishes, Lophius litulon (Choi et al. 2011;Park et al. 2014), Coryphaena hippurus (Jeong et al. 2017), and Muraenesox cinereus (An et al. 2011).
In the present study, Trichiurus japonicus was the most commonly consumed species, as reported previously (Huh et al. 2006;Choi et al. 2011;An et al. 2012). T. japonicus inhabits at depths of 40 to 120 m (Martins and Haimovici 1997), which overlaps the habitat of Z. faber (50 to 140 m) (Vrgoč et al. 2006;Kim et al. 2013). Fishes with a long body swim in a head-up state with limited swimming capabilities (Wilson 1958). In addition, the body of T. japonicus is thin, long, and reflective. Therefore, Z. faber can efficiently detect T. japonicus at any depth (Stergiou and Fourtouni 1991). In the eastern Mediterranean, long body fishes such as Cepola macrophthalma are most commonly consumed by Z. faber (Stergiou and Fourtouni 1991).
Z. faber consumed Trichiurus japonicus and E. japonicus, which is schooling fish. Z. faber has a stalking ability to consume prey fish selected in a school or group (Ressell 1983). Two species inhabit the wild layer of the ocean, indicating that Z. faber moves to the surface layer to feed. Previous studies have found Jack Mackerel (Trachurus symmetricus) in the eastern Mediterranean and along the Portuguese coastline (Stergiou and Fourtouni 1991;Silva 1999). Trichiurus japonicus and E. japonicus were the most abundant species in the coastal waters of Korea (Cha 2010), which indicates that Z. faber is an opportunistic feeder by energy effectivity.
In the present study, predation by Z. faber was not significantly dependent on prey size. As there are no distinct morphological changes related to feeding ability with growth (Stergiou and Fourtouni 1991), large specimens of Z. faber expand their prey options by altering feeding behavior. In this study, individuals less than 30 cm preferred surface fish as E. japonicus and Trachurus japonicus, while specimens of Z. faber up to 38 cm were found to feed on the benthic species G. stelleri. In other words, as body size increased, Z. faber preferred fish lived deep water such as Conger myriaster (Huh et al. 2006) and Micromesistius poutassou (Silva 1999). This indicates that Z. faber can exploit the entire water column when feeding. This partial dietary change can reduce intraspecific competition by resource partitioning (Gerking 1994). After consuming a diet of small fish and zooplankton during the juvenile stage, adult Z. faber (> 24 cm) undergo a transformation in prey selection to reduce intraspecific competition.
Z. faber consumed more prey items during summer and autumn than in other seasons. Some fishes that inhabited Korea tend to spend the winter in near Jeju Island and East China Sea. In the spring, as temperature rise, they come back to the coastal waters of Korea due to spawning ground (Noh et al. 2013). Therefore, species abundance in summer becomes higher, compared with winter. We found that crustaceans were the dominant species in summer and autumn in this study because of the behavior and life history of crustacean prey (Xue et al. 2005;Blasina et al. 2010). P. eous used as prey mainly migrate to inshore (< 50 m) for the larval hatch during late winter and early spring Richards 2012). The density of crustaceans increases as the hatched crustaceans recruit in summer. Also, P. eous can be captured more than other invertebrates because P. eous inhabit in various water depths up to 600 m deep . Therefore, larger individuals of Z. faber inhabit in deeper depths and can consume crustaceans abundantly. Stergiou and Fourtouni (1991) found that only individuals up to 14 cm consumed tiny crustaceans, but this study obtained different results, as crustaceans were consumed by specimens of Z. faber up to 38 cm, and up to 168 crustaceans were consumed at a time. Along the Portuguese coastline, crustaceans are also an important food source for specimens up to 25 cm (Silva 1999). The short period of research in the Mediterranean has showed different results to this study and a previous study of Z. faber.

Conclusion
The present study was performed by commercial trawl and collected adult Z. faber (> 24 cm, TL). A total of 24 prey items were found and tropic diversity was low because Z. faber consumes mainly fishes. As Z. faber grew, they consumed the demersal fish species that live near their habitat. We found that prey items of Z. faber also changed depending on the abundant species of each season. As this results, Z. faber could be considered a piscivorous fish and opportunistic predator which consume mainly fish prey items from various depth of waters.