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Feeding Habitats of Juvenile Reef Fishes in a Tropical Mangroveâœseagrass Continuum Along a Malaysian Shallow-Water Coastal La

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Feeding Habitats of Juvenile Reef Fishes in a Tropical Mangroveâœseagrass Continuum Along a Malaysian Shallow-Water Coastal La Bull Mar Sci. 96(3):469–486. 2020 research paper https://doi.org/10.5343/bms.2018.0093 Feeding habitats of juvenile reef fishes in a tropical mangrove–seagrass continuum along a Malaysian shallow-water coastal lagoon 1 Institute of Oceanography Dung Quang Le 1 * and Environment, Universiti 1 Malaysia Terengganu, 21030 Siau Yin Fui 2 Kuala Nerus, Terengganu, Kentaro Tanaka Malaysia Suhaimi Suratman 1 2 Atmosphere and Ocean Yuji Sano 2 Research Institute, The 2 University of Tokyo, 5-1-5, Kotaro Shirai Kashiwanoha, Kashiwa-shi, Chiba 277-8564 Japan * Corresponding author email: ABSTRACT.—We conducted stable isotope (δ13C and <[email protected]>, <le. δ15N) and gut content analyses to understand habitat use [email protected]> of juvenile reef fishes (Lethrinus lentjan, Lutjanus russellii, and Epinephelus coioides), particularly the influence of spatial habitat structure along seagrass–mangrove continua. Sampling was conducted in Setiu Lagoon, located in the southern waters of the South China Sea (Malaysia). Gut content analysis indicated that the focal fishes preyed mainly on benthic invertebrates and other smaller fishes; these were used as potential prey items for isotopic tracers to track fish habitat use. Stable isotope analyses highlighted that the juvenile reef fishes were highly associated with seagrass beds as feeding grounds; however, site-specific analyses suggest differences in fish feeding habitats. The juvenile fishes, particularly large juveniles, preyed in both mangrove and seagrass areas from the central lagoon, whereas all juveniles showed preferential foraging within seagrass meadows in the nearby lagoon mouth. Furthermore, the mean stable isotope values of muscle tissue differed among fish size classes, indicating their ontogenetic habitat/diet shifts, especially for L. lentjan and E. coioides. This study provides important information to support current efforts in protecting and Guest Editor: Amy Y Then preserving mangroves and seagrasses as crucial nursery Date Submitted: 11 December, 2018. habitats for juvenile reef fishes from the anthropogenic Date Accepted: 6 September, 2019. activities influencing Setiu Lagoon. Available Online: 11 September, 2019. Mangrove and seagrass habitats in tropical shallow-water coastal lagoons are con- sidered crucial nursery and feeding grounds for numerous fish species including reef fishes (Blaber 2000, Sheaves and Molony 2000, Beck et al. 2001) because they provide protection from predators and rich food resources, which maximize growth during the juvenile stage (Sheaves et al. 2015). They also serve to replenish and sustain adult populations on coral reefs (Beck et al. 2001, Nagelkerken et al. 2008, Sheaves et al. Bulletin of Marine Science 469 © 2020 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 470 Bulletin of Marine Science. Vol 96, No 3. 2020 2015). The interlinked mangrove and seagrass habitats have been intensively studied due to their importance as feeding habitats for juvenile reef fishes, particularly in the Caribbean region (Nagelkerken and van der Velde 2004, Vaslet et al. 2015). In this region, substantial areas exist where mangrove prop-roots are inundated during low tide, thus juvenile reef fishes can shelter in mangrove habitats and make feeding forays into nearby seagrass beds (Rooker and Dennis 1991, Nagelkerken and van der Velde 2004). Additionally, some studies conducted on size-related dietary shifts of reef fishes suggested that small juveniles utilize mainly seagrass beds and then in- crease their range of foraging grounds (a mangrove–seagrass continua) as they grow before migrating to coral reefs (Nagelkerken and van der Velde 2004, Mumby 2006, Vaslet et al. 2015). Fish feeding activities can also be site-specific and depend on geographic regions as well as tropical estuary environments (Barletta et al. 2005, Lugendo et al. 2007). In the Indo-Pacific region, mangroves and seagrasses also form continua of intertidal mosaic habitats in lagoons and estuaries; however, the man- grove habitats are alternately inundated and exposed by the high-tide/low-tide cycle. During low tidal periods, such habitats are often not continuously available for most fishes, thus seagrass meadows provide food and shelter while mangroves are unavail- able (Sheaves 2005, Nagelkerken 2009). Several studies suggest that mangroves may not be the main sources of carbon for fish assemblages in mangrove estuaries, as the isotopic ratios in fish species were more enriched in13 C than mangrove-derived carbon sources (Kieckbusch et al. 2004, Lugendo et al. 2007, Nyunja et al. 2009, Tue et al. 2014). However, other studies have measured stable isotope ratios in benthic invertebrates to trace the origins or ontogenetic movements of their consumers, par- ticularly fish species (Nakamura et al. 2008, Berkström et al. 2013, Connolly and Waltham 2015, Escalas et al. 2015) because, given that benthic invertebrates have lower mobility or are habitat-specific, the isotopic signatures of their tissues reflect the relative changes in the isotopic values of local dietary sources, seagrasses or man- groves (Fry 1984, Nagelkerken et al. 2001, Bouillon et al. 2002, Vaslet et al. 2011, 2012, Berkström et al. 2013, Le et al. 2018). While juvenile reef fishes can access mangroves for feeding during tidal inundation, they mainly prey on benthic inver- tebrates that rely on mangrove carbon sources, such as sesarmid crabs (Sheaves and Molony 2000, Le et al. 2018). Such feeding activities of the juveniles reflect complex functional webs integrated across interlinked, intertidal vegetated habitats in tropi- cal regions (Nagelkerken and van der Velde 2004, Igulu et al. 2013). Furthermore, the nursery functions of vegetated habitats are structurally complex and dependent on habitat configuration and environmental conditions (Blaber 2000, Nagelkerken et al. 2008, Taylor et al. 2017). Thus, the loss or damage of one nursery habitat can- not only alter ecological functioning of entire coastal systems, but also profoundly affect juvenile fish biomass and sustainable fishery stocks (Honda et al. 2013). Very little information is available regarding juvenile reef fishes feeding habits in coastal nursery habitats of the Pacific Ocean, particularly around Malaysia. Therefore, such research is urgently needed to improve our understanding of these habitats and the food webs they support in order to successfully design marine reserves and resource management systems to preserve mangrove and seagrass habitats. In recent studies, gut content and stable isotope analyses have been combined as an effective approach to study food web structure and the movement and feeding ac- tivities of juvenile fishes (Cocheret de la Morinière et al. 2003, Vaslet et al. 2011, Igulu et al. 2014, Escalas et al. 2015, Le et al. 2018). Gut contents provide a 1–2 hr snapshot Le et al.: Feeding habitats of juvenile reef fishes in interlinked habitats 471 of information on fish diets (George and Hadley 1979) and can help determine the available prey items within habitats (Vaslet et al. 2011). Stable isotopic values in fish tissue provide information relating to the isotopic signature of fish diets during the preceding days, weeks, or months (Gearing 1991, Fry 2008). According to Post (2002) and McCutchan et al. (2003), the degree of enrichment of stable isotopes between fishes and their diets are slightly enriched (<1‰) or conserved for 13δ C but vary from 2.0‰ to 3.5‰ for δ15N. Furthermore, mangroves often show distinct δ13C signatures (δ13C generally between −34‰ and −27‰) compared to seagrasses (δ13C > −18‰; Fry and Sherr 1984, Bouillon et al. 2008). Thus, stable isotope signatures of fish tissue can reflect the corresponding isotopic signatures of local vegetation-based food webs in which the fish has grown (Nagelkerken and van der Velde 2004, Vaslet et al. 2011, Le et al. 2018). Recently, Bayesian mixing models, such as Stable Isotope Analysis in R (SIAR), have been widely applied for their utility in analyzing isotope data (Parnell et al. 2010, Phillips et al. 2014). SIAR was developed to estimate distributions of con- sumers’ possible diets (Vaslet et al. 2011, Abrantes et al. 2015, Connolly and Waltham 2015), to elucidate species-specific ontogenetic shifts, or to characterize broader food web structure (Cocheret de la Morinière et al. 2003, Nakamura et al. 2008, Vinagre et al. 2012, Abrantes et al. 2015, Artero et al. 2015, Le et al. 2017). In the present study, we used gut content and stable isotope analysis (δ13C and δ15N) to determine the feeding grounds of juvenile reef fishes, especially of emperor fish (Lethrinus lentjan), snapper (Lutjanus russellii), and grouper (Epinephelus coioides) in structurally complex nursery habitats in a shallow-water lagoon. Materials and Methods Study Area.—Setiu Lagoon (Fig. 1) is a critical nursery wetland for the juveniles of many fish species along the eastern coast of Peninsular Malaysia (Azmi 2014). An earlier study indicated that the mangrove and seagrass continua that form along the lagoon are utilized by a number of juvenile fishes, particularly reef fishes (Le et al. 2018). Approximately 14 km long, the lagoon contains several habitat types with a gradient of salinity from the center to the mouth (Nakisah and Fauziah 2003, Azmi 2014). In the central lagoon, where the water is influenced by the Ular rivulet and mangroves are dominated by Rhizophora spp. and Avicennia spp., the salinity varies from 24‰ to 27‰. In contrast, waters which are in the narrow mouth,
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