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Fish Stable Isotope Community Structure of a Bahamian Coral Reef

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Fish Stable Isotope Community Structure of a Bahamian Coral Reef Marine Biology (2019) 166:160 https://doi.org/10.1007/s00227-019-3599-9 ORIGINAL PAPER Fish stable isotope community structure of a Bahamian coral reef Yiou Zhu1 · Steven P. Newman1,2 · William D. K. Reid1 · Nicholas V. C. Polunin1 Received: 1 February 2019 / Accepted: 26 September 2019 © The Author(s) 2019 Abstract Stable isotopes have provided important insight into the trophic structure and interaction in many ecosystems, but to date have scarcely been applied to the complex food webs of coral reefs. We sampled white muscle tissues from the fsh spe- cies composing 80% of the biomass in the 4–512 g body mass range at Cape Eleuthera (the Bahamas) in order to examine isotopic niches characterised by δ13C and δ15N data and explore whether fsh body size is a driver of trophic position based on δ15N. We found the planktivore isotopic niche was distinct from those of the other trophic guilds suggesting the unique isotopic baseline of pelagic production sources. Other trophic guilds showed some level of overlap among them especially in the δ13C value which is attributable to source omnivory. Surprising features of the isotopic niches included the benthivore Halichoeres pictus, herbivores Acanthurus coeruleus and Coryphopterus personatus and omnivore Thalassoma bifasciatum being close to the planktivore guild, while the piscivore Aulostomus maculatus came within the omnivore and herbivore ellipses. These characterisations contradicted the simple trophic categories normally assigned to these species. δ15N tended 15 to increase with body mass in most species, and at community level, the linear δ N–log2 body mass relationship pointing to a mean predator–prey mass ratio of 1047:1 and a relatively long food chain compared with studies in other aquatic systems. This frst demonstration of a positive δ15N–body mass relationship in a coral reef fsh community suggested that the Cape Eleuthera coral reef food web was likely supported by one main pathway and bigger reef fshes tended to feed at higher trophic position. Such fnding is similar to other marine ecosystems (e.g. North Sea). Introduction Robertson 1982; Chen 2002) and thus their trophic functions and the overall functioning of the reef (Mouillot et al. 2014). In coral reef food webs, fshes are typically categorised into Inaccurate trophic information jeopardises comprehensive strict trophic guilds (e.g. Hiatt and Strasburg 1960; Jennings understanding of these food webs. Traditional gut contents et al. 1995; Polunin 1996; McClanahan et al. 1999; Hughes analysis gives detailed dietary information; however, this et al. 2003; MacNeil et al. 2015; D’Agata et al. 2016; Gra- typically has high temporal and spatial variability (Jennings ham et al. 2017; Stamoulis et al. 2017; Hadi et al. 2018; et al. 2001) and it might include items accidently ingested Moustaka et al. 2018). Yet this may overlook trophoplastic- (e.g. eDNA in gut contents DNA bar coding; Leal and Fer- ity, where many species feed across trophic boundaries (e.g. rier-Pagès 2016). Stable isotopes provide a time-integrated signal of what has been assimilated from the diet (Jennings 13 12 Responsible Editor: C. Trueman. et al. 2001). The stable isotope ratio of carbon ( C/ C, expressed as δ13C) is commonly used to distinguish produc- Reviewed by undisclosed experts. tion sources such as benthic and pelagic autotrophs (Tieszen Electronic supplementary material et al. 1983; Bearhop et al. 2004), whereas the stable iso- The online version of this 15 14 15 article (https ://doi.org/10.1007/s0022 7-019-3599-9) contains tope ratio of nitrogen ( N/ N, expressed as δ N) is used supplementary material, which is available to authorized users. as a proxy for trophic position (TP) because it has a higher trophic enrichment factor (TEF) (DeNiro and Epstein 1978, * Yiou Zhu 1981; McCutchan et al. 2003; Strieder Philippsen and Ben- [email protected] edito 2013) and shows less variation at the baseline (Hes- 13 1 School of Natural and Environmental Sciences, Newcastle slein et al. 1991) than does carbon. Combining δ C and University, Newcastle upon Tyne NE1 7RU, UK δ15N delineates ‘isotopic niches’ (Leibold 1995; Newsome 2 Banyan Tree Marine Lab, Vabbinfaru, North Malé Atoll, et al. 2007) which inform feeding strategies and trophic Republic of Maldives Vol.:(0123456789)1 3 160 Page 2 of 14 Marine Biology (2019) 166:160 interactions (Post 2002) at species, trophic guild and com- mass ratio (PPMR) can be calculated. This refects con- munity levels (France et al. 1998; Jennings et al. 2001, straints on community structure (Trebilco et al. 2013) and 2002a, b; Al-Habsi et al. 2008). Combining these levels of can be used to evaluate general food web properties such data can explain a species’ trophic ecology including how as food chain length (Jennings and Warr 2003) and food strict it is and what potential source(s) it is utilising with chain transfer efciency (Jennings et al. 2002c; Barnes et al. the latter being very important because trophic interactions 2010) across diferent aquatic systems (Jennings et al. 2001, among omnivorous species within the same community 2002c; Bode et al. 2003, 2006; Al-Habsi et al. 2008). The remain understudied in coral reefs. great diversity of production sources and trophic partitioning Trophodynamics can be size based. In aquatic systems, by consumers on coral reefs suggest that the PPMR may be large individuals generally feed at higher TPs (Jennings et al. smaller and food chains longer than in many other marine 2001, 2002b; Al-Habsi et al. 2008; Romanuk et al. 2011). ecosystems. But to date, the community-level δ15N to body This is a result of ontogenetic dietary shifts, morphometric mass relationship and the PPMR have not been reported for changes including increasing gape size, post-maturity factors a coral reef, so important insights such as measures of food and greater predator ability that infuence foraging (Peters chain length cannot be gained. 1986; Jennings et al. 2001; Munday 2001; Jennings et al. Here, underwater visual census and stable isotope data 2002b; Al-Habsi et al. 2008; Newman et al. 2012; Robinson were used to explore the role of body size and trophic inter- and Baum 2015; Ríos et al. 2019). However, some large actions among fsh species in structuring a coral reef fsh fshes forage at lower TPs due to dietary shifts (e.g. Chen community at Cape Eleuthera (the Bahamas). Specifcally, 2002; Layman et al. 2005), seasonality efects (Bronk and the study aimed to: (1) defne isotopic niches at species and Glibert 1993; Rolf 2000) and human disturbance (Pastorok trophic guild levels in order to understand the principal and Bilyard 1985). TPs of some species remain relatively energy pathways supporting them; and (2) assess whether unchanged with increasing body size (e.g. herbivores; Plass- there are positive δ15N–body mass relationships at the spe- Johnson et al. 2013; Dromard et al. 2015). Size-based feed- cies and community levels and if so, derive an average pred- ing remains almost unstudied in coral reef ecosystems (Rob- ator–prey biomass ratio (PPMR). inson and Baum 2015) where large herbivores contribute greatly to the biomass. Investigating TP to body mass relationships at commu- Materials and methods nity level can improve understanding of predator to prey relationships and energetic pathways (Romanuk et al. 2011; Study site Robinson and Baum 2015) and of changes in community trophic composition (Graham et al. 2017). Where a positive Four accessible and conservation-protected reef sites (Fig. 1) TP relationship with body mass exists, the predator–prey on the Exuma side of Cape Eleuthera (the Bahamas) with Fig. 1 Map of survey sites at Cape Eleuthera (the Bahamas) 1 3 Marine Biology (2019) 166:160 Page 3 of 14 160 relatively high structural complexity and a diverse fsh com- habits and swimming patterns. Hand net, gill net (mesh size: munity were selected for visual surveys and fsh sampling. 1 cm × 1 cm, net size: 2 m × 1 m), BINCKE net (Anderson These sites were close to each other and to shore and repre- and Carr 1998), underwater fshing hook and line, static sented both bommies and patch reefs. In spite of the conser- hook and line, spearfshing (local fshermen only) and hook vation status of the study sites, the reefs have been subject and line surface trolling were all used in the sampling in the to chronic overfshing and otherwise impacted by cyclones survey sites and adjacent areas (Table 2). Fish were killed by and coral bleaching episodes. spine dislocation and stored in an ice chest on board. Sam- ples were all collected within a 1-month period and from Fish survey nearby sites to reduce spatial and temporal isotopic variation (Bronk and Glibert 1993; Jennings et al. 1997; Rolf 2000; Underwater visual census (UVC) was conducted by two McCutchan et al. 2003). divers using eight single-sweep 30 m × 5 m transects at After landing, approximately 2 g of dorsal white muscle each site to record fsh species, individual total length (L, to tissue near the dorsal fn were dissected, rinsed with water nearest cm) and numbers of individuals. Surveyors’ length and stored in individual whirlpack bags in a − 20 °C freezer, estimation precision was repeatedly measured by conduct- and algal samples were only rinsed and stored in a freezer. ing underwater fsh-shaped object length estimation train- All samples were dried in individual tin trays in an oven ing (Bell et al. 1985) to minimise error (± 5%). Transects at 40 °C for ~ 12 h until fully dried and then in individual ran parallel to each other to avoid intersection. Transects sealed Eppendorf tubes in zip-lock bags. were carried out in the morning (9:30–11:30) or after- noon (14:00–16:00), while swimming at a steady speed for Stable isotope analysis preparation 30 min.
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