Marine Biology (2019) 166:160 https://doi.org/10.1007/s00227-019-3599-9

ORIGINAL PAPER

Fish stable isotope community structure of a Bahamian

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 bifasciatum being close to the planktivore guild, while the piscivore 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. Highly mobile transient individuals (e.g. sharks and jacks) were excluded since they had large home range and All dried samples were imported to Newcastle Univer- were not necessarily reef associated, and also large schools sity, freeze dried and then manually ground with mortar of fshes were excluded since they were sighted only sporadi- and pestle. Fish samples were weighed to 1.0 ± 0.1 mg cally (Ferreira et al. 2001). in tin capsules with a Mettler MT5 microbalance. The prepared samples were analysed by Iso-Analytical Ltd Sampling for stable isotope analysis (Crewe, UK) by Elemental Analysis-Isotope Ratio Mass Spectrometry (EA-IRMS). The 15N/14N ratio (δ15N) was expressed relative to ­N2 in air for nitrogen, while that of Abundant species were selected by their contribution to the 13 12 13 total biomass (B). From UVC data, individual body mass C/ C (δ C) was relative to Pee Dee Belemnite (PDB) values (M, g) were calculated from L (cm) using: of ­CO2. Reference material used for this analysis was IA-R042 (δ13C = − 21.6 ± 0.1‰, δ15N = 7.6 ± 0.1‰), b M = a × L (1) with quality control check samples IA-R042, IA-R038 with published length to weight conversion factors a and b (δ13C = − 25.0 ± 0.1‰, δ15N = − 0.4 ± 0.1‰), a mix- (“Appendix A” in supplementary materials) from fshbase. ture of IA-R006 (δ13C = − 11.7 ± 0.0‰) and IA-R046 org (Froese and Pauly 2017). Where conversion factors (δ15N = 21.9 ± 0.2‰). IAR042 and IA-R038 were calibrated were linked with standard or fork length rather than L, or against and traceable to IAEA-CH-6 (δ13C = − 10.4‰) and L was in units other than centimetres, length was converted IAEA-N-1 (δ15N = 0.4‰), IA-R006 to IAEA-CH-6 and into appropriate units or length types using the equations in IA-R046 to IAEA-N-1. External standards (fsh white mus- 13 15 fshbase.org. All body mass data were log­ 2 transformed to cle tissue, δ C = − 18.9 ± 0.0‰, δ N = 12.9 ± 0.1‰) were remove any efects of relationship between body size and also used for future reference. The precision of analysis for phylogeny (Freckleton 2000). For each M class (2–512 g), δ13C, δ15N, %C and %N was ± 0.1‰, ± 0.2‰, ± 4% and B was calculated by summing individual M values. Species ± 1%, respectively. For individual samples, no lipid extrac- were ranked in order of their contribution to the B of each tion was needed because their C/N ratios were less than 3.7 ­log2M interval, and those making up 80% of the B were (Fry et al. 2003; Sweeting et al. 2006). selected for the community trophic structure analysis. Samples of selected species (Table 1) were collected Data analysis through the length range recorded in the UVC to adequately 15 describe species δ N–log2M relationships (Galván et al. All data were tested for normality and homogeneity of vari- 2010). The size range cover ratio (rL = LSIA sample range/LUVC ance prior to analysis and analysed in R 3.24 (R Core Team range) was used to check whether the sampling objective 2016) using the package siar (Parnell and Jackson 2013) was met. Fish were collected using a variety of techniques between δ13C and δ15N data, linear regression (Wilkinson 15 depending on their behaviour towards divers, feeding and Rogers 1973; Bates et al. 1992) between δ N and ­log2

1 3 160 Page 4 of 14 Marine Biology (2019) 166:160 ), size SIA C 13 (L δ − 12.4 ± 0.3 − 12.0 ± 0.9 − 10.6 ± 0.9 − 12.4 − 13.6 ± 0.2 − 11.9 ± 0.4 − 11.0 ± 0.6 − 16.5 ± 0.8 − 12.0 ± 0.6 − 14.4 ± 0.6 − 13.2 ± 0.5 − 13.6 ± 0.5 − 9.5 − 12.2 ± 0.4 − 13.9 ± 0.4 − 14.9 ± 0.2 − 13.9 ± 0.2 − 17.0 ± 0.1 − 17.2 ± 0.1 − 10.9 − 16.5 ± 0.4 − 12.6 ± 1.3 − 11.7 ± 0.3 − 11.9 ± 0.2 − 17.0 ± 0.2 − 10.1 ± 0.3 − 10.9 ± 0.3 − 12.2 ± 0.1 − 14.0 − 10.6 ± 0.2 − 13.7 ± 0.3 − 13.7 − 17.4 ± 0.2 − 14.8 ± 0.4 N 15 δ 7.7 ± 0.1 8.4 ± 0.2 7.8 ± 0.5 5.6 7.2 ± 0.2 8.4 ± 0.1 8.2 ± 0.3 4.7 ± 0.3 8.6 ± 0.1 6.3 ± 0.2 7.9 ± 0.1 5.1 ± 0.2 8.7 8.1 ± 0.1 8.4 ± 0.2 5.9 ± 0.6 4.2 ± 0.1 5.2 ± 0.1 5.4 ± 0.2 3.9 4.0 ± 0.1 8.9 ± 0.8 7.9 ± 0.2 8.7 ± 0.2 4.6 ± 0.1 7.5 ± 0.2 7.0 ± 0.2 8.1 ± 0.2 7.5 6.1 ± 0.1 6.2 ± 0.3 6.7 4.5 ± 0.1 5.8 ± 0.2 ), maximum total lengthtotal maximum 2017 ), L NA NA NA r 0% 68% 30% NA 25% 13% 31% 46% 100% 0% NA 73% 100% 18% 28% 18% NA 80% 23% 34% 18% 19% 0% 65% 35% 0% 0% 55% 0% 16% 0% (mm) SIA 320–419 273–308 200–300 280 L 135–275 260–378 278–300 81–168 202–246 210–260 273–392 84–280 377 155–400 103–295 145–530 62–130 54–87 71–113 34 14–34 25–32 212–336 361–423 22–35 321–419 96–233 231–300 275 120–133 36–135 117 16–30 195–325 4 2 5 1 6 9 4 3 3 7 5 9 1 8 2 7 8 1 3 2 5 6 4 5 9 4 1 2 5 1 4 5 11 10 n 3.8 ± 0.1 3.5 ± 0.4 3.8 ± 0.2 2.1 ± 0.1 3.6 ± 0.4 4.0 ± 0.3 3.7 ± 0.2 2.0 ± 0.0 4.3 ± 0.4 3.2 ± 0.1 4.3 ± 0.1 2.0 ± 0.0 4.2 ± 0.3 4.4 ± 0.4 4.3 ± 0.6 4.3 ± 0.6 2.0 ± 0.0 3.7 ± 0.4 3.4 ± 0.2 2.7 ± 0.4 2.9 ± 0.4 3.4 ± 0.3 3.8 ± 0.3 4.1 ± 0.0 3.3 ± 0.4 3.1 ± 0.1 3.5 ± 0.1 3.8 ± 0.0 3.5 ± 0.2 3.8 ± 0.1 3.7 ± 0.2 3.3 ± 0.2 3.5 ± 0.4 3.0 ± 0.0 Trophic position Trophic ), SIA sample total length range ­ total lengthn ), SIA sample size ( 2017 ), SIA sample range and Pauly 1 SE (Froese ± (mm) UVC L 40–100 70–270 160–550 30–380 120–460 200–360 190–450 90–210 200–370 60 60–220 240–430 10–380 10–130 10–250 10–30 10–40 100–270 250–600 10–80 200–320 50–180 150–350 210–350 30–100 10–190 50–140 10–100 140 (mm) 64 38 44 76 76 max 610 406 381 381 381 318 762 381 610 610 610 381 610 381 305 914 254 127 305 610 762 305 457 457 229 203 165 457 1219 L ), mean trophic position ), mean trophic UVC (L Benthivore Benthivore Benthivore Herbivore Trophic guild Trophic Benthivore Benthivore Piscivore Herbivore Piscivore Herbivore Piscivore Herbivore Piscivore Piscivore Piscivore Piscivore Herbivore Planktivore Planktivore Herbivore Herbivore Parasitivore Benthivore Piscivore Planktivore Benthivore Benthivore Benthivore Benthivore Benthivore Omnivore Benthivore Benthivore Herbivore C ± 1 SE 13 BAVE HOAD LUSY ACCH Code CAPE HORU OCCH ACCO LUAP POAR ​ CARU ​ ACTR ​ LUGR PTVO CECR AUMA SCIS CHCY CLPA COGL COPE ELGE EPGU EPST GRLO HAAL HAFL HAPL HASC HABI ​ HAGA HAMA HAPI HOCI N and δ 15 a , mean δ L a a List of sampled species of reef fsh at Cape Eleuthera (the Bahamas), with scientifc name, common name, species code, trophic guild (Froese and Pauly EleutheraCape at fsh Pauly and reef of species (the sampled of (Froese guild withBahamas), trophic code, List species name, common name, scientifc ), UVC total length range ­ length total range 1989 ), UVC ) (Humann and DeLoach max ( L range cover ratio r ratio cover range Acanthurus chirurgus Acanthurus 1 Table Scientifc name Calamus pennatula Holocentrus rufus Ocyurus chrysurus Acanthurus coeruleusAcanthurus Lutjanus apodus arcuatus Pomacanthus Caranx ruber Caranx Acanthurus tractus Acanthurus Lutjanus griseus volitans Pterois Cephalopholis cruentata Aulostomus maculatus Aulostomus Lutjanus synagris Scarus iserti Chromis cyanea Chromis Balistes vetula Balistes Clepticus parrae Clepticus Coryphopterus glaucofraenum Coryphopterus personatus Elacatinus genie Epinephelus guttatus Epinephelus striatus Gramma loreto Gramma Haemulon album Haemulon favolineatum Haemulon plumierii Haemulon sciurus Halichoeres bivittatus Halichoeres Halichoeres garnoti Halichoeres Halichoeres maculipinna Halichoeres Halichoeres pictus Halichoeres Holacanthus ciliarisHolacanthus Holocentrus adscensionis

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body mass and mvtnorm to simulate values from a bivariate normal distribution. Results were visualised using ggplot2

C (Wickham and Chang 2016). The assumptions of the ordi- 13 δ − 12.5 ± 0.8 − 11.9 − 11.8 ± 1.5 − 14.0 ± 0.7 − 14.5 − 14.1 ± 0.3 − 16.3 ± 0.2 nary least squares linear regression analyses were assessed with QQ plots, histograms of standardised residuals and plots of standardised residuals versus ftted values. Pearson’s

N correlation coefcient was used to test correlations between 15 δ 3.9 ± 0.2 4.6 9.9 ± 0.4 6.4 ± 0.5 5.4 6.1 ± 0.4 5.4 ± 0.1 variables. Signifcance was set at p = 0.05 in all cases. All errors are reported as ± 1SE unless otherwise stated. L r 80% 0% 35% 25% 0% 6% 35% Species and trophic guild stable isotope analyses

The bulk δ13C and δ15N data were used to interpret δ15N–δ13C relationships in each species and trophic guild (mm)

SIA (Froese and Pauly 2017). Isotopic niches of fve trophic 67–400 L 460 853–1100 57–85 26 67–70 45–90 guilds (four benthic: benthivore, herbivore, omnivore and piscivore and one pelagic: planktivore) were investigated 6 1 4 7 1 2 9

n using SIBER in the siar package. This was achieved by investigating standard ellipse parameters: eccentricity (E) and the angle in degrees (θ, 0°–180°) between semi-major axis and the x axis, the sample size corrected standard ellipse areas ­(SEAC) and Bayesian standard ellipse areas (SEA­ B) (Jackson et al. 2011). θ and E values potentially 2.0 ± 0.1 2.0 ± 0.0 4.5 ± 0.6 2.0 ± 0.0 3.1 ± 0.2 2.0 ± 0.0 3.3 ± 0.1

Trophic position Trophic distinguish among isotopic niches where diferent trophic guilds have similar sized ­SEAC but diferent relationships between δ13C and δ15N (Reid et al. 2016). θ values close to 0° or 90° suggest dispersion in only one axis: θ values close (mm) to 0° represent relative dispersion along the x axis (δ13C), UVC L 10–300 10–550 440–1150 40–150 10–80 20–70 10–140 indicating multiple production sources, while θ values close to 90° highlight relative dispersion along the y axis (δ15N), indicating feeding across multiple trophic positions from a uniform basal source. E explains the variance on the x and (mm) y E

max axes: low refers to similar variance on both axes with a 279 610 152 102 102 152 1829 L more circular shape, while high E indicates that the isotopic niche is stretched along either x or y axis. The overlap of the standard ellipses between guilds was calculated using “sea. overlap” using SIBER. In order to compare isotopic niche areas among trophic guilds, a Bayesian approach was used Herbivore Trophic guild Trophic Herbivore Piscivore Herbivore Herbivore Herbivore Omnivore that calculated 20,000 posterior estimates of ­SEAB based on the data set. The mode and 95% credible intervals (CI) were reported. A signifcant diference among ­SEAB was interpreted graphically whereby if the 95% CI did not over- SPAU Code SPVI SPBA STDI STLE STPA THBI lap, then the SEA­ B were deemed to be signifcantly diferent (Parnell and Jackson 2013).

δ15N–body size relationship

Cross-species relationships between stable isotope data and M were analysed using linear regression between mean bulk δ13C and δ15N of each species and their maximum body mass (continued) (Mmax) recorded by Humann and DeLoach (1989). Comparing fshes at a fxed proportion of maximum size (here ≥ 55% of Species sampled to represent other uncollected species on the represent to list Species sampled

Sparisoma aurofrenatum 1 Table Scientifc name a Sparisoma viride Sphyraena barracuda Sphyraena Stegastes diencaeus Stegastes Stegastes Stegastes partitus Stegastes Thalassoma bifasciatum

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Table 2 List of fshing method and targeting species Fishing method Targeting species Examples of species

Hand net Slow, approachable, small, cryptic, territorial Gobies, damselfsh, PTVO, AUMA 1 cm× 1 cm gill net Fast, alert, non-thread shaped, schooling J. Scarinae, A. labrids, J. haemulids, pomacentrids BINCKE net Fast swimming, close to substrate, schooling J. Scarinae, labrids Underwater fshing Large bodied, fast swimming, cryptic, smart and alert A. haemulids, HORU, some Scarinae, lutjanids, grouper Line and hook Pelagic, fast, alert Carangids, lutjanids Spearfshing Fast, aggressive A. Scarinae, acanthurids, PTVO Surface troll Pelagic, fast swimming individuals Carangids, SPBA

J juvenile, A adult, for codes see Table 1

L max) reduced the risk of comparing diferent life stages (Char- δ15N −δ15N TP = TP + fish base nov 1993; Jennings et al. 2001; Galván et al. 2010). base 15 (2) 15 Δδ N For each species, the δ N–log2M relationship was gen- erated using linear regression, the slope and intercept val- where the Δδ15N is assumed constant and equal to 3.4‰ 15 ues being used to calculate δ N values of individuals of (DeNiro and Epstein 1981; Minagawa and Wada 1984). the same species with other body mass values. To derive ­TPbase was indicated by the striped parrotfsh (S. iserti, 15 B 15 the community relationship between δ N and ­log2B ( δ Nbase = 4.2 ± 0.1‰; ­TPbase = 2.0) due to its low isotopic was used instead of M to diferentiate the community-level variation across sizes, time integration of seasonality from analysis from the species-level analysis), the mean weighted producers and adequate sample size (n = 10). The slope (b) 15 δ N value of each log­ 2B class was derived by calculating of TP–log2B relationship was obtained from the slope (s) of r i 15 b = s∕3.4 (1) the mass ratio ( ) of each individual ( ) in each ­log2B δ N–log2B relationship where . Thus, the PPMR r = M ∕ n M class, using i i ∑i=1 i , where n is the total number is calculated as of individuals in the log­ 2B class; and (2) mean weighted 3.4∕s 15 PPMR = 2 . (3) δ N for each log­ 2B class j of the whole community as 15 n 15 15 δ Nj = ∑i=1 δ Ni × ri (Al-Habsi et al. 2008). The δ N The uncertainty of PPMR was estimated by (1) simulat- 15 s of each individual (δ Ni) was either calculated using the ing 10,000 times of independent variables (the mean and 15 species-level linear δ N–log2M relationship if it is signif- standard deviation from the linear regression statistics) and 15 cant or equivalent to the mean δ15N of the species if not. Δδ N values (mean and standard deviation of 3.4 ± 1.0‰; Because of the species richness of these reefs and limita- Post 2002) from a bivariate normal distribution (ρ = 0) and tion of fshing techniques, not all species could be sampled. (2) calculating PPMR estimates using Eq. 3. The median, To obtain δ15N values of such species, several methods were 25th and 75th quantiles were reported. The same method used (full details in “Appendix B” supplementary materi- was applied to existing studies for comparison. als): (1) using samples from similar species within the same genus if possible (order of priority: same genus, family, site, trophic position, diet and feeding habit from fshbase.org) by Results comparing 3 criteria: (a) length to weight conversion factors, (b) dietary similarities and (c) their feeding behaviours in Isotopic niches at species and trophic guild levels this area; and (2) using existing data in the literature from nearby locations or elsewhere in the with baseline In total 9055 individuals (L from 1 to 120 cm, M from 0.01 to adjustment (D. cavernosa to D. cavernosa if possible, oth- 2742 g) were recorded in 32 UVCs over 4800 m2 of reef. Of erwise D. cavernosa to turf algae) to reduce temporal and/ 41 fsh species collected and analysed for δ15N, 11 had sample or spatial baseline variations (Cabana and Rasmussen 1996). sizes under three, and three (Coryphopterus glaucofraenum, Balistes vetula, Holocentrus adscensionis) were sampled to Predator–prey mass ratio represent certain uncollected species. The size range cover ratio (rL) ranged from 0 to 100% (mean = 31.0 ± 5.0%). Mean The mean PPMR was calculated using the slope (b) species δ13C ranged from − 17.4 ± 0.2‰ (Halichoeres pictus) 15 of the regression line of the TP–log2B relationship as to − 9.5 ± 0.0‰ (Lutjanus griseus), while mean δ N ranged 1∕b PPMR = 2 . TP was calculated using the additive frame- from 3.9 ± 0.8‰ (S. aurofrenatum) to 9.9 ± 1.5‰ (Sphyraena work as barracuda). δ15N values were signifcantly but weakly cor- 13 2 related with δ C (p < 0.05, radjusted = 0.29 ) at the species level

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Fig. 2 Plot of bulk δ15N against δ13C (mean ± SE) of all sampled fsh species (for codes see Table 1) and standard ellipses (solid line-ellipses) for fve trophic guilds (and one species of parasitivore, ELGE) of fsh at Cape Eleuthera (the Bahamas)

(Fig. 2). Some species had large SE values in δ13C (≥ 1‰) Table 3 Isotopic niche area (‰2) estimates and parameters [eccen- (e.g. S. barracuda) or δ15N (≥ 0.5‰) (e.g. Aulostomus macu- tricity (E), the angle in degree between the semi-major axis of the x θ latus), or both δ13C and δ15N (e.g. Elacatinus genie). Mean standard ellipse and the axis ( ) for fve trophic guilds (benthivore, 13 15 herbivore, omnivore, piscivore and planktivore) of coral reef fsh at δ C and δ N values of strict pelagic planktivores (e.g. Cape Eleuthera (the Bahamas)] Chromis cyanea 13 , TP = 3.7, δ C = − 17.0 ± 0.1‰, 2 2 15 Trophic SEAC (‰ ) E θ (°) SEAB (‰ ) SEAB 95% CI δ N = 5.2 ± 0.1‰) and strict benthivores of similar TP (e.g. guild B. vetula, TP = 3.8, δ13C = − 12.4 ± 0.3‰, δ15N = 7.7 ± 0.1‰) were signifcantly diferent. Benthivore 5.30 0.94 20.96 5.19 3.96–6.93 The herbivore and benthivore guilds had the largest iso- Herbivore 5.90 0.77 6.29 5.73 4.32–7.53 topic niches, followed by the piscivore guild, and then the Omnivore 1.83 0.98 19.17 1.77 1.05–3.14 omnivore guild; the planktivore guild had an isotopic niche Piscivore 3.91 0.89 14.36 3.81 2.88–4.04 signifcantly smaller than others (Table 3). The plankti- Planktivore 0.46 0.79 75.69 0.41 0.26–0.66 vore guild had a lower δ13C than others and was separated Estimates of isotopic niche areas are given as ­(SEAC) and the mode from the herbivore, benthivore and piscivore trophic guilds of the Bayesian standard ellipse area (SEA­ B) estimates. Upper and (Fig. 2, Table 4). The isotopic niche of the omnivores over- lower 95% credible intervals (CI) indicate the uncertainty in the lapped with those of the herbivores and planktivores as ­SEAB estimates did those of the benthivore and piscivore (Table 4). The isotopic niche of the herbivores was vertically separated Table 4 Standard ellipse overlap (‰2) among the fve trophic guilds E θ from those of the benthivores and piscivores. and val- Trophic guild Benthivore Herbivore Omnivore Piscivore ues difered among trophic guilds (Table 3); the herbivore guild had the lowest E (0.77), while the omnivores had Herbivore 0.00 the highest (0.98). The benthivore (0.94) and planktivore Omnivore 0.00 0.77 (0.79) trophic guilds had E values very similar to those of Piscivore 0.57 0.00 0.00 the omnivore and herbivore trophic guilds, respectively. Planktivore 0.00 0.00 0.03 0.00

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The θ values of the δ15N versus δ13C relationships of all an isotopic coordinate within the standard ellipse of the the trophic guilds were positive; the herbivores had the herbivore trophic guild. lowest θ (6°), while the planktivores had the highest (76°). 15 Among the benthivore, omnivore, piscivore and herbivore δ N–body mass relationships at species trophic guilds, the isotopic niche was spread along the x and community levels and PPMR axis (θ < 45°), while that of the planktivores was more vertically spread (θ > 45°). Some species (the benthivore There were signifcant but weak relationships across spe- H. pictus, herbivores Acanthurus coeruleus and Coryphop- cies between ­log2Mmax (maximum body mass) and both 15 2 13 terus personatus and omnivore Thalassoma bifasciatum) δ N ( radjusted = 0.12 , p < 0.05; Fig. 3a) and δ C data 2 15 had isotopic coordinates close to the ellipse of the plank- ( radjusted = 0.17 , p < 0.05; Fig. 3b). The δ N values of sev- tivore trophic guild, and one piscivore (A. maculatus) had eral species did not scale positively with log­ 2Mmax (e.g. E.

Fig. 3 Plots of bulk δ15N (a) and bulk δ13C (b) (mean ± SE) versus ­log2 maximum body mass for all collected fsh species (for codes see Table 1) at Cape Eleuthera with mean isotope values of individuals bigger than 55% of their Lmax. Solid line: linear regression line (p < 0.05)

1 3 Marine Biology (2019) 166:160 Page 9 of 14 160 genie, Sparisoma viride, Scarus iserti and S. aurofrena- whereas this was not the case for others (e.g. Clepticus tum). The SE values of δ13C were generally higher than parrae, Calamus pennatula, Halichoeres garnoti). At the 15 15 those of δ N regardless of Mmax. δ N tended to vary with community level, the combined isotope data demonstrated 15 ­log2M for 29 species (Fig. 4) with n ≥ 3; of these 24 rela- a strong positive linear relationship between mean δ N 15 tionships were positive (signifcantly so, e.g. C. cyanea), and ­log2B, the regression equation being δ N = 0.34 ± 0. r2 = 0.64 while fve were negative (signifcantly so, e.g. Pomacan- 04log2B + 4.03 ± 0.24 ( adjusted , p < 0.05, Fig. 5). thus arcuatus r2 = 0.80 , “Appendix C” supplementary materials). The slope value of TP–log2B was b = 0.10 ( adjusted , There was considerable variability around the regression p 2 < < 0.05), and the PPMR estimates were 1047:1 (Table 5). line for nine species ( radjusted 0.5 , e.g. S. barracuda),

15 Fig. 4 Plot of δ N versus ­log2 body mass (linear regression) of all sampled species at Cape Eleuthera (the Bahamas). Solid line: signifcant relationship (p < 0.05), dashed line: non- signifcant relationship. For codes see Table 1

Fig. 5 Plot of combined relationship (linear regression) 15 between δ N and log­ 2 body mass at Cape Eleuthera (the Bahamas). Solid line: linear regression line (p < 0.05), long dashed line: 95% CI

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Table 5 Mean PPMR values Community PPMR estimates Reference of diferent communities from the literature using the additive Median 25th and 75th quantiles framework Central North Sea 104:1 42 to 75:1 Jennings et al. (2002a, b) Northern North Sea 1037:1 239 to 4503 Jennings et al. (2001) Cape Eleuthera 1047:1 250 to 4833:1 Present study Puget Sound 4320:1 779 to 2.71 × 104:1 Reum et al. (2015) North Sea 8349:1 1235 to 6.73 × 104:1 Jennings and Warr (2003) Western Arabian 8935:1 1287 to 6.60 × 104:1 Al-Habsi et al. (2008) Iberian Peninsula 2.02 × 107:1 2.27 × 105 to 1.61 × 1010:1 Bode et al. (2006)

Discussion et al. 2016). The benthivore, piscivore and herbivore trophic guilds, which share mostly benthic production sources, had Species and trophic guild trophodynamics similar isotopic niche areas which were much greater than those of the planktivores and omnivores, with their isotopic Stable isotope data at both species and trophic guild levels niches spread along the x axis as indicated by E and θ values, indicated that at the Cape Eleuthera site there were large suggesting source omnivory within the benthic producer cat- diferences in trophic ecology within and among species, egory. Overlapping isotopic niches among the trophic guilds and species utilising a range of production source types were (e.g. piscivore and benthivore) suggested that they might common. share dietary resources to some extent; for example, some High within-species variability in δ13C and δ15N values lutjanids are both piscivorous and feed on zoobenthos (Allen for some species suggested the existence of individual spe- 1985; Kulbicki et al. 2005; Layman and Allgeier 2012). The cialisation (Matthews and Mazumder 2004) in the food web vertical distribution in the isotopic niches for the four ben- where diferent individuals of the same species were consist- thic trophic guilds refected the herbivorous fsh feeding at ently sampling diferent production sources. For example, low trophic positions, while the omnivores, benthivores and similarly sized individuals of the apex predator S. barracuda piscivores utilised a wider range of energy sources from dif- had similar δ15N values but difered greatly in δ13C values. ferent TPs. There were species with stable isotope values The δ13C value of approximately − 16‰ was close to that outside the isotopic niches of their assumed trophic guilds, within the planktivore trophic guild, while the δ13C value of which suggested feeding on diferent food sources than pre- − 10‰ was more consistent with the piscivore trophic guild. viously known or those derived from snapshot diet studies. Trophic position omnivory indicated by diferences in δ15N For example, the four benthic feeders (H. pictus, A. coer- also occurs, for example, in the parasitivore E. genie which uleus, C. personatus and T. bifasciatum) were likely relying feeds on parasites from fsh at diferent trophic positions. on plankton sources, and the piscivore A. maculatus might The SIBER analysis indicated at least two types of pro- be predating on smaller herbivores. Some herbivores came duction sources, namely benthic (e.g. algae) and pelagic partly within the isotopic niches of other trophic guilds, indi- (e.g. plankton), and mixed-feeding patterns for some species cating feeding on food sources in addition to algae such as that are typically regarded as relying solely on single types invertebrates or planktivore faeces (Robertson 1982; Wulf of source materials (e.g. herbivorous fsh; Plass-Johnson 1997; Dunlap and Pawlik 1998; Chen 2002; Plass-Johnson et al. 2013; Dromard et al. 2015). In this study, isotopic et al. 2013). This can only be confrmed with detailed die- niche areas of the planktivores were signifcantly smaller tary analysis including baseline variation (i.e. during the than other guilds even though plankton can have highly vari- 3–6 months isotopic turn over period). able isotopic signatures (McClelland and Montoya 2002; 15 Kürten et al. 2013), which indicated a level of dietary strict- δ N–body mass relationship ness or consistency. High θ, low E and low SEA values of the planktivore guild nevertheless suggested TP omnivory, The majority of species had a positive trend between δ15N with these fsh feeding at diferent TPs albeit from the same and ­log2M indicating that they tend to feed at higher TPs as type of pelagic source (e.g. phytoplankton and zooplank- size increases. This could be a result of increasing gape size, ton). The omnivore guild had high E, low θ and SEA values, predatory skill and ftness level allowing individuals to feed the δ13C data indicating that the two species are supported on higher TP prey as they grow (Peters 1986; Munday 2001; by plankton and benthic algae with similar δ15N baselines. Newman et al. 2012). Those with negative or highly vari- Although based on only two species, the omnivores may be able stable isotope-size relationships potentially have dietary connecting these two pathways to some extent (McMeans shifts from isotopically high value production sources to

1 3 Marine Biology (2019) 166:160 Page 11 of 14 160 low or multi-pathway (e.g. exploitation of short food chain) within the same genus or family having ontogenetic and/or feeding patterns in their sampled size ranges, or otherwise dietary diferences; some not meeting all three criteria and assimilating signifcantly diferent isotopic baselines across using published data from the same species could be subject the population (Jennings et al. 2002a; Layman et al. 2005). to feeding strategies varying ontogenetically (Plass-Johnson 15 Unlike Robinson and Baum (2015) where δ N–log2M rela- et al. 2013) or spatially (Jennings et al. 1997; Matthews and tionships of all individuals in two separate trophic pathways Mazumder 2004). Unlike studies using combined baselines (herbivore and carnivore) were investigated, species-level (Mill et al. 2007), here the benthic alga D. cavernosa was and whole-community-level analyses were conducted in the sole baseline and this might not adequately represent this study. The variation among species is attributable to the whole benthic assemblage, which includes turf algae, diferences in the trophic pathways supporting them, but to cyanobacteria and other potential production sources. understand better how trophic pathways afect such relation- ships, more data are clearly needed. At community level, a Predator–prey mass ratio 15 positive linear relationship between δ N and ­log2B across the combined sites was found, indicating that TP tended to The mean PPMR at Cape Eleuthera indicates a relatively increase with body mass regardless of and larger long food chain in this coral reef system compared with coral reef fsh in this Cape Eleuthera community on average other aquatic systems (Table 5), suggesting potentially fed at higher TPs. greater ecosystem size and stability (Jennings and Warr The weak cross-species relationship between isotopic 2003). However, surveys at adjacent non-protected sites signatures and ­log2Mmax suggested that maximum body failed to show the presence of large predators there; thus, mass could scarcely constrain species’ trophic capabilities the PPMR data we report seem to be specifc to the protected in this food web in which there were small-bodied benthi- sites. vores and planktivores and large-bodied herbivores. The body-size structuring is similar to that of North Sea and Western Arabian Sea community data (Jennings et al. 2001; Conclusions Al-Habsi et al. 2008). Here, the small size class biomass data were dominated by herbivores rather than higher TP Stable isotope data indicate more than one production source omnivores such as Labridae (Graham et al. 2017), while the and mixed reliance on them by some coral reef fshes sug- large size classes were dominated by piscivores and omni- gesting evidence of reef fsh crossing trophic boundaries vores rather than large-bodied herbivores such as Scarinae described by their trophic guilds and that current catego- (Hughes et al. 2007; Zhu 2019). Although the surveyed risations are often simplistic. Combining visual census and Cape Eleuthera sites are now legally protected, they were stable isotope data indicated that the Cape Eleuthera coral previously fshed and are structurally degraded. The linear- reef fsh community was size structured. The relationship 15 ity of the δ N–log2B relationship at Cape Eleuthera may at this site points to body size as a driver of predator–prey not be generic; it could be infuenced by the loss of habitat relationships and trophic pathways at community level, with structural complexity and aspects of past overfshing (e.g. the isotope data suggesting that trophic position plasticity removal of large herbivores). is common at species level. This is the frst indication of a The present study also had limitations. All individu- 15 positive linear δ N–log2 body mass relationship in a coral als were treated as if they had the same isotopic baseline, reef system, but this may not pertain to all coral reefs. yet signifcant isotopic diferences between benthic and pelagic sources are expected (McConnaughey and McRoy Acknowledgements We thank Cape Eleuthera Institute (CEI) for pro- 1979; Polunin and Pinnegar 2002), whereas other baselines viding logistic support, Jordan Atherton for underwater visual surveys, would have been taken into consideration when estimating CEI interns involved in fsh sampling, and local fshermen for providing fsh samples. the trophic positions of consumers with signifcantly mixed diets. Also, for some species, sample sizes failed to ade- Author contributions This study was designed by YZ and NVCP, the quately fulfl requirements for confdently describing stable feld work was carried out by YZ, the data analysis was conducted isotope changes as a function of body mass (Galván et al. by YZ, SPN and WDKR, and the paper was written by YZ, NVCP, 2010), yet linear regression was still applied to these spe- WDKR and SPN. cies to explore their δ15N–log M relationships. Low sample 2 Funding No external funding. sizes and/or size ranges (rL) meant that for some species, stable isotope data could not be derived across whole UVC Compliance with ethical standards size ranges; for these stable isotope data were assumed to be size invariant. For missing species, the methods used to Conflict of interest The authors declare that they have no conficts of infer stable isotope values had limitations including species interest.

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Ethic approval All applicable international, national and/or institu- DeNiro MJ, Epstein S (1978) Influence of diet on the distribu- tional guidelines for the care and use of were followed. The tion of carbon isotopes in animals. Geochim Cosmochim Acta research was approved by the Newcastle University Ethics Committee 42:495–506 and the Bahamian Department of Marine Resources under permits DeNiro MJ, Epstein S (1981) Infuence of diet on the distribution MAMR/FIS/17 and MAMR/FIS/34A. No coral habitat was disturbed of nitrogen isotopes in animals. Geochim Cosmochim Acta during this research. All fsh were killed in accordance with the UK 45:341–351 Home Ofce Scientifc Procedures () Act. All samples were Dromard CR, Bouchon-Navaro Y, Harmelin-Vivien M, Bouchon C imported to UK under DEFRA permit TARP/2015/210. (2015) Diversity of trophic niches among herbivorous fshes on a Caribbean reef (Guadeloupe, Lesser Antilles), evidenced by stable isotope and gut content analyses. J Sea Res 95:124–131 Open Access This article is distributed under the terms of the Crea- Dunlap M, Pawlik JR (1998) Spongivory by parrotfsh in Florida tive Commons Attribution 4.0 International License (http://creat​iveco​ mangrove and reef habitats. Mar Ecol 19:325–337 mmons.org/licen​ ses/by/4.0/​ ), which permits unrestricted use, distribu- Ferreira CEL, Goncçalves JEA, Coutinho R (2001) Community tion, and reproduction in any medium, provided you give appropriate structure of fshes and habitat complexity on a tropical rocky credit to the original author(s) and the source, provide a link to the shore. Environ Biol Fishes 61:353–369 Creative Commons license, and indicate if changes were made. France R, Chandler M, Peters R (1998) Mapping trophic continua of benthic food-webs: body size–δ15N relationships. Mar Ecol Prog Ser 174:301–306 Freckleton RP (2000) Phylogenetic tests of ecological and evolution- ary hypotheses: checking for phylogenetic independence. 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