1Introduction
Zostera marina (eelgrass) is the most common seagrass species in temperate coastal areas, and increases habitat complexity and provides living space and shelter for marine animals (Klumpp et al., 1989; Connolly et al., 1999; Hemminga and Duarte, 2000). Many fish and decapod species use eelgrass beds as feeding and nursery grounds, including many economically important fishes (Nelson, 1981; Edgar and Shaw, 1995; Huh and Kwak, 1997a; Huh and An, 1997; Guidetti and Bussotti, 2000). Some studies have been made on eelgrass bed in Korea to determine seasonal variation in species composition and abundance of fishes in Kwangyang Bay, Hamduck around Cheju Island and Angol Bay (Huh and Kwak, 1997a; Go and Cho, 1997; Lee et al., 2000) and feeding habits of particular fish species (Acanthogobius flavimanus, Platycephalus indicus, Liparis tanakai and Pleuronectes yokohamae) in the Southern sea, Korea (Huh and Kwak, 1999; Kwak and Huh, 2002; 2003a; 2003b).
Large eelgrass beds are developed in Jindong Bay, southern Korea, and provide a habitat for variety of invertebrates and small fish, which in turn are the potential food of large fishes.
Although some ecological studies on fish in the eelgrass bed have been conducted in the Bay, their interest in the studies is confined to feeding habits of some fish species (Kwak and Huh, 2004; Kwak et al., 2004; Kwak et al., 2005).
The objective of this study was to examine the seasonal variation in species composition and abundance of fishes and decapods inhabiting an eelgrass bed of Jindong Bay, Korea and to determine the relationships between environmental factors and fish and decapod abundance.
2Materials and Methods
The eelgrass bed of Jindong Bay (Fig. 1) is forming subtidal bands (500~700 m wide) in the shallow water (< 3 m), and forming patches for about 4 km along the shore.
Fish and decapod samples were collected monthly by 5-m beam trawl (1.9-cm mesh wing and body, 0.6-cm mesh liner). Four 6-min tows in each sampling time were carried out during the day in an eelgrass bed throughout 2002. Specimens were preserved immediately in 10 % formalin after capture and later transferred to 70 % isopropanol. These samples were identified according to Masuda et al. (1984), Kim (1973), NFDRI (2001) and Kim et al. (2005) and weighed to the nearest gram in wet weight. Specimens were measured to the nearest millimeter (fish, standard length SL; shrimp, carapace length CL; crabs, carapace width CW). Crabs were separated on the basis of sex.
Surface water temperature (by thermometer) and salinity (by salinometer) were monitored monthly on each sampling occasion. The eelgrass biomass was estimated from all plant bodies taken in a sea bottom of 0.01 m2. The plants were separated into the above- and below-ground parts, dried at 80 °C for 24h then weighed to the nearest gram.
The fish and decapod data was analyzed to obtain the following community variables. Diversity H' (Shannon and Weaver, 1949) was calculated as:
where n is the number of individuals of each i species in a sample and N is the total number of individuals.Association of fish and decapod species, Pianka's similarity index (Pianka, 1973), Aij was calculated as:
where Aij is the similarity of species j on species i; Pih is the proportion of individuals of a species i in a particular month h; Pjh is the proportion of individuals of a species j in a particular month h. Values for the similarity index may vary between 0, if no similarity occurs, and 1 for complete similarity. The Pianka's similarity index was subjected to an average linkage cluster analysis.A one-way ANOVA with orthogonal design was used to analyze variations in fish abundance and environmental factors with season. The relationships between fish and decapod abundance and eelgrass biomass were analyzed using Pearson's correlation coefficient.
3Results
3.1Water temperature, salinity, and eelgrass biomass
Water temperature at the study site ranged from 7.4 °C to 27.7 °C and varied significantly with months (one way ANOVA, df=11, F=13.77, p < 0.05). The peak of water temperature was around July, a decline in October and a minimum during winter (Fig. 2A). Salinity ranged from 28.7 ‰ to 34.2 ‰ and did not vary significantly among months (one way ANOVA, df=11, F=2.11, p > 0.05) with display a similar pattern except in July when it dropped (about 28 ‰) (Fig. 2B). The average eelgrass biomass ranged from 21.8 g DW/m2 to 378.7 g DW/m2 and varied significantly with months (ANOVA, p < 0.05). The peak of eelgrass biomass was around May, and a sharp decline in June and a minimum in December (Fig. 2C).
3.2Fish and decapod species composition
A total of 2,143 fish belonging to 26 species were collected (Table 1). Numerically dominant fish were Hexagrammos otakii (17.9 %), Pholis nebulosa (15.6 %), P. fangi (14.9 %), Acanthopagrus schlegeli (9.4 %), Lateolobrax japonicus (9.3 %), Leiognathus nuchalis (5.3 %) Acentropagrus pflaumi (4.6 %), A. flavimanus (4.2 %), and Pseudoblennius cottoides (4.0 %), together accounting for 85.3 % of the catch and 80.9 % of biomass. The dominant fish species were primarily small fish species or young juveniles. Only about 10 % exceeded 5 cm SL.
A total of 2,039 decapods, belonging to 29 species (15 shrimp, 2 hermit crab and 12 crab species) were collected (Table 2). Numerically dominant species were Palaemon macrodactylus (19.4 %), Charybdis japonica (15.2 %), Pagurus minutus (8.9 %), C. bimaculata (8.4 %), Alpheus digitalis (7.0 %), Hemigrapsus penicillatus (6.5 %), Crangon affinis (6.2 %), and C. uritai (5.8 %). These made up 77.3 % of numbers of individuals and 85.0 % of total biomass. Most individuals were relatively small: 0.2 to 1.8 cm CL for shrimps and 0.2 to 7.2 cm CW for crabs.
3.3Seasonal variation in abundance of fish and decapods
The number of fish species (5~17 species) varied with seasons (one-way ANOVA, df=11, F=4.85, p < 0.05). Fish species was abundant in April and May (Fig. 3A). Number of individuals varied significantly with seasons (one-way ANOVA, df=11, F=11.13, p < 0.05, Fig. 3B). A large number of fish were collected from April to July when H. otakii, P. nebulosa. P. fangi, L. japonicus, and A. schlegeli were abundantly occurred. Fish numbers was low in January and February (Appendix 1). The fish biomass differed substantially between different seasons (one-way ANOVA, df=11, F=6.65, p < 0.05, Fig. 3C). Higher biomass was in July and August when big-sized H. otakii, A. schlegeli, L. japonicus, A. flavimanus, and Sillago japonicus were present (Appendix 2). The range of diversity index was 0.72~2.32, and higher value was in May and August (Fig. 3D).
The one-way ANOVA revealed that the number of decapod species (df=11, F=17.86, p < 0.05), number of decapod individuals (df=11, F=8.88, p < 0.05), and decapod biomass (df=3, F=8.45, p < 0.05) differed significantly between seasons. Number of decapod species was more than 14 species from March to June, and number of decapod individuals was the highest in May which were dominated P. macrodactylus, C. japonica, Trachysalambria curvirostris, and A. digitalis (Fig. 4A, 4B). The biomass of decapods was high in August and September (Fig. 4C), when an abundance of large C. japonicus and C. bimaculata were found (Appendix 2). The study area had similar value of diversity regardless of month, suggesting that the number and relative abundances of decapods were similar over study periods (Fig. 4D).
The dendrogram shows three clusters which identify the fish species (Fig. 5). The group 1 was composed of P. fangi, P. nebulosa, H. otakii, A. flavimanus, L. japonicus, A. pflaumi, Hippocampus japonica, A. schlegeli, and Silago japonicus with occurring predominantly over study periods. This group can be further divided into two subgroups: subgroup 1 contains P. fangi, P. nebulosa and H. otakii, with large numbers from March to May when eelgrass biomass was large in the study area, while subgroup 2 composed of A. flavimanus, L. japonicus, A. pflaumi, H. japonica, A. schlegeli, and S. japonicus with peak numbers from June to August. The group 2 was composed of L. nuchalis, Rudaris ercode, Takifugu niphobles, Repomucenus valenciennei, Ditrema temmincki, and Pleuronectes yokohamae which were peak numbers from September to November. These periods were coincided with the period of small eelgrass biomass. The group 3 was composed of Sebastes schlegeli, Syngnathus schlegeli, S. inermis, Pseudoblennius cottoides and P. percoides. This group was high numbers from March to June when water temperature was increased. while, individuals were few in other periods.
The dendrogram shows five clusters which identify the decapods species (Fig. 6). The group 1, consisting of P. macrodactylus, A. digitalis, C. japonica, and C. bimaculata, occurred predominantly over the study period in the study area, being comparatively large in number of individuals in May and June, when the eelgrass biomass was large. This group also occurred predominantly over the study period. The group 2 was composed of C. affinis, C. uritai, P. minutus, Pugetiia quadridens, and H. penicillatus, which occurred with large number in March and April when water temperature was being increased. The group 3 consists of Upogebia major, Eualus leptognathus, and C. hakodatei, which occurred in February and March. The group 4 was composed of P. ortmanni, Trachysalambria curvirostris, Marsupenaeus japonicus, Metapenaeus joyneri, Tritodynamia rathbuni, Tozenuma tomentosum, and Heptarcarpus pandaloides with occurrence from March to June, and the group 5 was composed of Portunus trituberculatus, Latreus anoplonyx, and P. gravieri with occurrence from August to October when eelgrass biomass and water temperature were decreased.
3.4Relationships between abundance and environment factors
Water temperature, salinity and eelgrass biomass variations corresponded closely with seasonal variation of the abundance of fishes and decapods over the study period. There are only signigicant relationships between water temperature and salinity and abundance of fish (p < 0.05). However, number of individuals of both fish (r2=0.80, p < 0.05) and decapods (r2=0.83, p < 0.05) were correlated with eelgrass biomass (Fig. 7).
4.Discussion
A total of 26 fish species was recorded from an eelgrass bed of Jindong Bay and of these H. otakii, P. neulosa, P. fangi, A. schlegeli, L. japonicus, L. nuchalis, A. pflaumi, A. flavimanus, and P. cottoides were numerically dominant. Most of fish species are of commercial and recreational importance. For example H. otakii, A. schlegeli and L. japonicus are valued as live fish in the Southern area, Korea, and P. nebulosa and P. fangi harvested as a food fish (Kim and Kang, 1993; Kim et al., 2005).
Broad-scale surveys of fish communities in the eelgrass beds from other regions of Korea suggest a similar community structure. Very similar species composition of fish showed in Myoungjuri eelgrass bed where close to present study area (Baeck et al., 2005). Comparing with other regions, H. otakii, P. fangi, P. cottoides, and P. nebulosa also dominated the fish community in Kwangyang Bay (Huh and Kwak, 1997a), A. schlegeli, P. nebulosa in Angol Bay (Lee et al., 2000), and H. otakii, P. nebulosa in Hamduck around Cheju Island (Go and Cho, 1997). Kikuchi (1966; 1974) reported that the genera Hexagrammos, Pseudoblennius, Pholis were also dominant fish groups in the eelgrass beds of Tomioka Bay, Japan. Although there are some difference in dominant species among regions, it seems that the seagrass habitats of Northwestern Pacific show similar fish and decapod species composition.
The 29 decapod species collected from an eelgrass bed of Jindong Bay were mostly shrimps. P. macrodactylus and A. digitalis were the dominant species followed by C. affinis and C. uritai. Studies of the eelgrass bed of Kwangyang Bay showed that C. affinis, C. uritai, A. digitalis, and genera Palaemon were dominant in that order (Huh and An, 1997). Compared with eelgrass beds of temperate regions in worldwide, the genera Alpheus and Crangon were common groups in Tomioka Bay, Japan (Kikuchi, 1966), and Crangon and Palaemon were also dominated the decapod communities of seagrass beds in Western Port Bay, Australia (Howard, 1984; Connolly et al., 1999). Caridean shrimps in particular were in high abundance, as well as the genera Palaemon, Crangon, and Alpheus. These taxonomical groups were abundant in seagrass beds regardless of locations and sampling gear used.
Fish collected from the Jindong Bay eelgrass bed appeared to be dominated by small fish and juveniles of most species. This indicated that an eelgrass bed of Jindong Bay function as nursery areas. Such conclusions are in general agreement with other studies of seagrass beds (Huh and Kwak, 1997a; Go and Cho, 1997; Rozas and Minello, 1998; Lee et al., 2000; Nagelkerken et al., 2002). A significantly greater abundance of decapod juveniles than that of adults in our study site at Jindong Bay confirmed that also these species were likely to be dependent on seagrass beds for shelter and survival during the early life cycle stages (Coles and Lee Long, 1985; Turnbull and Mellors, 1990; Haywood et al., 1995; Vance et al., 1996; and An, 1997).
Seasonal variation in both species composition and abundance appear to be considerable for fish and decapod communities utilizing eelgrass bed. In Jindong Bay, number of individuals was highest in May. These peaks in abundance corresponded closely with peak eelgrass biomass and prey availability. Seasonal variation of eelgrass biomass in Jindong Bay was marked. When eelgrass biomass increased from March, the number of fish and decapod individuals also increased, and numbers declined with decreases in eelgrass biomass from September. Higher diversity indices of fish have been recorded corresponding with increased species number, abundance and eelgrass biomass. However, the biomass of both fishes and decapods were relatively high when eelgrass standing crops were low. It seems that larger individuals were abundant due to low eelgrass density and can be captured easily by fishing gear. Several other studies have demonstrated a positive correlation between faunal richness and abundance and the aboveground biomass of seagrass beds (Nelson 1981; Leber, 1985; Bell and Pollard, 1989; Heck and Weinstein, 1989; Huh and Kwak, 1997a; Connolly et al., 1999). Other studies have shown similar patterns of variable faunal abundance in fish communities of eelgrass beds, Korea. For example, the fish abundance increased with increasing eelgrass biomass and water temperature in Angol Bay (Lee et al., 2000), and similarly in Hamduck off Cheju Island (Go and Cho, 1997). (1986) have demonstrated that seasonal variation of fish abundance in Hansilpo, Chungmu was correlated positively with water temperature. Features of eelgrass beds such as shoot density and length can influence faunal abundance, and this has been shown best with decapods. The density of caridean shrimps was significantly associated with eelgrass biomass and living-space in an eelgrass bed of Kwangyang Bay (Huh and An, 1997).
Dominant species showed distinct seasonal occurrence patterns. The seasonal abundance of many species can be attributed to their reproductive habits. For example, the increase in abundance of pholidae species including P. nebulosa and P. fangi recorded during the winter and spring was consistent and coincides with their spawning season (Kang et al., 1996; Hwang and Lee, 2001). Panaeid shrimp such as T. curvirostris and M. japonicus mainly occurred their adult individuals during spawning seasons (Minagawa et al., 2000; Oh et al., 2003). Similarly, other species including A. schlegeli, L. japonicus, L. nuchalis, A. pflaumi, A. flavimanus and R. valenciennei occurred as juveniles in large numbers around spawning season. It appears that these species rely on eelgrass bed as a nursery ground. Whereas, the consistent occurrence of some species such caridian shrimps, hermit crabs and Charybdis crabs in this area suggest that these species undergo their whole life-cycle in this zone.
Prey availability may also be an important factor influencing faunal abundance in an eelgrass bed. High seagrass standing crop provides good shelter and food resources for small organisms such as epiphytic epifauna (Amphipods, Isopods, Tanaids etc.) (Klumpp et al., 1989; Klumpp and Kwak, 2005). Small fishes such as dominant fish species (e.g. H. otakii, P. nebulosa, P. fangi, A. schlegeli, and L. japonicus) in Jindong Bay fed mainly on small amphipods and isopods (Kwak unpublished data). The seasonal abundance of epiphytic epifauna coincided with these groups of dominant fishes during the study period. These common fish changed diets from gammarid amphipods and copepods to decapods such as caridean shrimps and crabs as they increased in size (Kwak and Huh, 2004; Kwak et al., 2004; Kwak et al., 2005). Other studies of feeding habits of fishes have reported similar correlated temporal variation in abundance of epiphytic epifauna and fish occurrence in Korean eelgrass beds (Huh and Kwak, 1997b; 1998; Kwak et al., 2005). Huh and Kwak (1997a) demonstrated that the abundance of dominant fishes in an eelgrass bed of Kwangyang Bay was positively correlated with eelgrass biomass and prey availability. Hence we suggest that the high abundance of epiphytic epifauna and caridean shrimps were responsible for the maintenance of fish abundance through predator-prey interactions in this eelgrass bed.
