Local-Scale Resource Partitioning by Stingrays on an Intertidal Flat

Vol. 533: 205–218, 2015 MARINE ECOLOGY PROGRESS SERIES Published August 6 doi: 10.3354/meps11358 Mar Ecol Prog Ser

Local-scale resource partitioning by stingrays on an intertidal flat

Sebastián A. Pardo1,2,*, Katherine B. Burgess1, Daniella Teixeira1, Michael B. Bennett1

1School of Biomedical Sciences, The University of Queensland, St Lucia, Queensland 4072, Australia 2Present address: Earth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada

ABSTRACT: The partitioning of dietary resources is a potential mechanism by which competing species can coexist. We examined local-scale dietary partitioning among 3 sympatric stingrays, Neotrygon kuhlii, Dasyatis fluviorum and Himantura toshi, from an intertidal flat in Moreton Bay, Australia, and compared their diets to the benthic prey items at the site. Ordination of stomach contents revealed that the species’ diets differed significantly from each other and from the composition of potential prey items in their habitat, suggesting dietary partitioning among these species (ANOSIM, p < 0.001, R-statistic = 0.874). According to the index of relative importance (IRI), polychaetes were the most important prey for N. kuhlii (90.0% IRI), while D. fluviorum preferred brachyuran crabs (52.6% IRI) and H. toshi preferred carid shrimp (65.2% IRI). Size-related shifts in diet were investigated for N. kuhlii, and a weakly significant effect was detected, due to a decrease in importance of polychaetes and increased importance of carid shrimp and teleost fishes with in- creasing body size (ANOSIM, p < 0.001; R-statistic = 0.253). Jaw morphology was compared between D. fluviorum and N. kuhlii; D. fluviorum had a larger gape and a more molariform dentition than N. kuhlii, which may relate to preferences for epifaunal and infaunal prey, respectively. The results of this study suggest that N. kuhlii, D. fluviorum and H. toshi partition food resources at a local-scale within Moreton Bay, which likely facilitates their coexistence in this area.

KEY WORDS: Dasyatidae · Diet · Benthic · Batoid · Stomach contents

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INTRODUCTION et al. 2011, Bornatowski et al. 2014), which are common mesopredators in marine and estuarine environ- Resource partitioning is among the evolutionary ments around the world. For example, in northeast mechanisms that facilitate stable coexistence among Australia, dietary composition differs significantly competing species (Schoener 1974, McPeek 2014). among 3 sympatric stingrays of the genus Neotrygon Limiting resources must be divided among competi- (Family Dasyatidae; Jacobsen & Bennett 2012). Like- tors to the extent that intraspecific competition out- wise, dietary differences have been identified among weighs interspecific competition; that is, a species a number of stingaree species (Family Urolophidae) must be limited more by its own use of a resource from Australia’s coastal and offshore habitats (Platell than by another species’ use of it (Chesson 2000). et al. 1998, Marshall et al. 2008). These findings sup- Among marine fishes, resource partitioning com- port the view that dietary partitioning can facilitate monly involves dietary divergences, whereby func- coexistence among rays. tionally similar species evolve dissimilar diets (Ross Resource partitioning among batoids contrasts 1986). This is the case among many sympatric batoid starkly with the historical view that these species species (rays and skates, Superorder Batoidea; Yick feed opportunistically and occupy functionally equiva-

*Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 206 Mar Ecol Prog Ser 533: 205–218, 2015

lent roles (Hess 1961, Gilliam & Sullivan 1993). The objective of this study was to investigate Instead, their specialised diets suggest that they are dietary partitioning among 3 sympatric stingray spe- able to actively feed on their preferred prey. Dietary cies, N. kuhlii, D. fluviorum and H. toshi, which feed differences are known to correlate with feeding mor- concurrently on intertidal flats in Moreton Bay, Aus- phology in teleosts (Linke et al. 2001, Platell & Potter tralia. Specifically, we aimed to quantitatively com- 2001) and sharks (Simpfendorfer et al. 2001, Powter pare the diets of these species via stomach content et al. 2010). Stingrays vary in their sensory capabili- analysis, and contrast these to the composition of ties with which feeding is facilitated, such as elec- benthic prey species in their common intertidal habi- troreception and olfaction (Jordan et al. 2009a,b), tat. An important distinction of this study is that we and it is likely that dietary differences among sym- aimed to investigate partitioning at a local scale patric species will correlate with differences in jaw (~1 km2), so as to effectively mitigate other variables morphologies as well. that might cause dietary differences among these Even though many sympatric batoid species differ species (e.g. differences in habitat use patterns). in their dietary resource use, it is difficult to deter- Additionally, we compared the jaw morphologies mine whether this is due to selective feeding or to dif- and dentition between D. fluviorum and N. kuhlii ferences in habitat preferences within sampling with respect to their relative diets. Importantly, we scales. Most dietary comparisons between sympatric did not aim to describe the complete diet of these elasmobranchs have been made in studies that col- species, but rather to investigate dietary differences lected individuals over broad spatial scales, obscur- among co-existing species that feed at a single site. ing the effects of habitat partitioning (Braccini et al. 2005, Jacobsen & Bennett 2012, Bornatowski et al. 2014). Habitat differences may even be occurring at MATERIALS AND METHODS smaller spatial scales; for example, O’Shea et al. (2013) suggested that sympatric stingrays that have Sampling similar diets might be partitioning their habitat at scales of metres, such as between the reef lagoon and Specimens of Neotrygon kuhlii, Dasyatis fluviorum the outer reef. and Himantura toshi were collected as bycatch from The high diversity of sympatric stingrays in More- commercial tunnel-netting operations at Wynnum ton Bay, Australia, provides an ideal opportunity to Banks in Moreton Bay, Queensland, Australia (27° investigate dietary partitioning (Johnson 1999, Last & 25’ 38’’ S, 153° 10’ 33’’E, Fig. 1) during February and Stevens 2009). Moreton Bay is a large semi-enclosed March 2006 and January to April 2012 (see Table S1 embayment, covering an area of 1523 km2. Stingrays in the Supplement at www.int-res.com/ articles/ are known to feed actively in the bay’s intertidal suppl/m533p205_ supp.pdf ). The site is composed of areas during high tide (S. Pardo pers. obs.), creating intertidal and shallow subtidal mudflats covered by prominent sand pits that become exposed after the patchy seagrass beds of Zostera capricorni and tide recedes. The most common stingray species in Halophila ovalis. Stingrays were captured in a 784 m these areas are the blue-spotted maskray Neotrygon monofilament nylon net (7.5 cm mesh, 2 m drop) fit- kuhlii (Müller & Henle, 1841), the estuary stingray ted with a tubular mesh bag at its deeper end (10 m Dasyatis fluviorum (Ogilby, 1908) and the brown long, 5 cm mesh) that was set at high tide before whipray Himantura toshi (Whitley, 1939) (Pierce et dawn. The sex of each stingray was recorded, and al. 2011). N. kuhlii has a widespread tropical to sub- disc width (DW) was measured as the straight-line tropical distribution throughout the Indian and West- distance (± 1 mm) between the lateral margins of the ern Pacific Oceans, while H. toshi and D. fluviorum pectoral fins. Stomachs were excised and fixed in are thought to be endemic to Australian inshore and 10% neutral buffered formalin solution, except for estuarine environments (Last & Stevens 2009). D. flu- stingrays whose buccal cavities indicated prior stom- viorum has the most restricted range, spanning only ach eversion. To assess potential prey in the feeding the sub-tropical to temperate central eastern waters habitat, sediment core samples (13 cm diameter, (Last & Stevens 2009). Studies have found N. kuhlii to 20 cm depth) were collected at the site during feed primarily on polychaetes (Kulbicki et al. 2005, stingray collection on 4 occasions in 2006. Samples Jacobsen & Bennett 2012, O’Shea et al. 2013), but were taken at 5 m intervals along a single 50 m tran- the diets of D. fluviorum and H. toshi and the degree sect laid perpendicular to the shoreline, and benthic of dietary overlap among these species remain fauna were extracted by passing the cores through a unknown. 2 mm sieve. Pardo et al.: Resource partitioning among intertidal stingrays 207

careous shell because stingrays are thought to discard these when feeding (S. Pardo pers. obs.). The % IRI was calculated from the contribution of each faunal category to the total IRI (Cortés 1997). Species and

cores were compared for % IRI, % Fo, % Mc and % Nc. Differences in stomach contents and sediment cores were analysed via non-metric multi-dimen- sional scaling (nMDS) ordinations and analyses of similarity (ANOSIM) using PRIMER v5.2.9 (Clarke & Gorley 2001). Similarity matrices were constructed using Bray-Curtis dissimilarity coefficients on Hellinger-transformed mass values of each major prey category. To compare within and between species, core samples and years, analyses were performed in 2 ways. First, the mean mass values of 4 randomly pooled stomachs were analysed due to the low number of prey categories per stomach, an approach previously described for studies of this nature (Platell & Potter 2001, White et al. 2004). Sec- Fig. 1. Netting location in Moreton Bay, Queensland, Aus- tralia. Dark grey areas represent locations of intertidal flats ond, analyses were performed at the level of the indi- and mangroves, while the approximate net placement is vidual without pooling. Similarly, to investigate onto- marked with the dotted line genetic shifts in N. kuhlii, data were compared among individuals and by pooling them into 3 size classes: 150−249 mm, 250−349 mm and 350−449 mm DW. These size classes were selected as they allowed Stomach content and sediment core analyses for a similar number of samples in each group. The small sample sizes of D. fluviorum and H. toshi did Fauna from the stomach contents and sediment not allow for such analyses. In all cases, preliminary cores were examined under a dissecting microscope analyses revealed no differences between sexes (Wild Type M3Z or Olympus SZ11) and identified to (ANOSIM, p > 0.05), thus data of both sexes were the lowest possible taxonomic level. For analyses, pooled. fauna were categorised into higher taxonomic groups (e.g. polychaetes, brachyurans, bivalves; see Platell et al. 1998, White et al. 2004), since some items Jaw morphology were unidentifiable to lower taxonomic levels. The importance of each faunla category to the diet of Excised stingray jaws were measured for the fol- each species and in the sediment cores was analysed lowing parameters: gape width with jaws closed using the index of relative importance (IRI) (Pinkas et (GWCLOSED) (Fig. 2a); dental set length for both the al. 1971) on data pooled for species and for sediment upper (DSLUPPER) and lower jaws (DSLLOWER) with the cores. IRI is given by the function: jaws in a near occlusal position (Fig. 2c); jaw depth along the dorso-ventral axis (JD and JD ; IRI = (N + M )F (1) UPPER LOWER c c o Fig. 2b,d) and jaw height along the antero-posterior where Fo (frequency of occurrence) is the percentage axis (JHUPPER and JHLOWER), both measured at the jaw of stomachs or cores that contained a specific faunal symphysis (Fig. 2a). Jaw robustness was approxi- category, Nc (numerical composition) is the number of mated by multiplying both the upper (JDUPPER × JHUP- items of a specific faunal category expressed as a per- PER) and lower (JDLOWER × JHLOWER) jaw depths and centage of the total number of items, and Mc (mass heights. All measurements were ± 0.01 mm. Principal contribution) is the mass of a specific faunal category component analysis (PCA) was used to compare all expressed as a percentage of the total mass of all morphometric measurements among species, as a items (± 1 mg). Mass (Mc) was chosen over volumetric proportion of disc width, using normalised Euclidean contribution because many items were too small for distances (for rationale refer to Clarke & Warwick accurate volumetric measurements. Unlike bivalve 2001). The morphology of each species’ dentition was mass, gastropod mass was measured without the cal- also qualitatively examined. 208 Mar Ecol Prog Ser 533: 205–218, 2015

Fig. 2. Measurements taken from stingray jaws: (a) Ventral (labial) view of jaw showing closed gape width (GWCLOSED), and upper and lower jaw heights (JHUPPER and JHLOWER, respectively); (b) anterior view of the jaw showing upper jaw depth (JDUPPER); (c) dorsal (lingual) view of the jaw showing upper and lower dental set length (DSLUPPER and DSLLOWER, respectively); and (d) posterior view of the jaw showing lower jaw depth (JDLOWER)

RESULTS chaetes were absent from H. toshi stomachs, whose

diet was dominated by carid shrimp (77.8% Fo; 52.4% Stomach content analysis Nc; 62.5% Mc; 65.2% IRI), followed by penaeid prawns (50.0% Fo; 28.94% Nc; 23.0% Mc; 19.0% IRI). A total of 78 Neotrygon kuhlii, 20 Dasyatis fluvio- Brachyurans contributed moderately to the diet of H. rum and 18 Himantura toshi were investigated for toshi (66.7% Fo; 18.3% Nc; 14.3% Mc; 15.9% IRI), but their stomach contents: 66 N. kuhlii (154−440 mm were not important in N. kuhlii (28.2% Fo; 0.9% Nc; DW), 16 D. fluviorum (333−598 mm DW) and 14 H. 2.3% Mc; 0.5% IRI). Carids contributed moderately to toshi (235−692 mm DW) from 2006, and 12 N. kuhlii the diets of N. kuhlii and D. fluviorum (46.2% Fo; (277−390 mm DW), 4 D. fluviorum (313−440 mm DW) 1.74% Nc; 16.1% Mc; 4.6% IRI and 55.0% Fo; 10.1% and 4 H. toshi (202−295 mm DW) from 2012 (Fig. 3). Nc; 26.0% Mc; 12.5% IRI, respectively), whilst teleost A further 8 N. kuhlii showed signs of stomach ever- fishes, although consumed relatively frequently, were sion and 5 had empty stomachs, all of which were of little importance (Fo = 20.5%; Nc = 0.6%; Mc = removed from analyses. For cumulative prey curves 6.1%; 0.8% IRI and Fo =35.0%; Nc = 3.3%; Mc = 5.4%; ses Fig. S1 in the Supplement. 1.9% IRI, respectively). Similarly, bivalves were fre-

The relative importance of the various prey cate- quently consumed by N. kuhlii (70.5% Fo) but had lit- gories differed among the 3 stingray species (Table 1, tle importance (2.5% Nc; 7.3% Mc; 3.9% IRI). Other Fig. 4). The diet of N. kuhlii was dominated by poly- prey items were found infrequently and were of neg- chaete worms (90.0% IRI); they were found in all ligible importance in the diets of any species (% IRI < stomachs (100% Fo) and had the greatest contribution 0.01). For example, anomurans (hermit crabs) and by number and mass (93.2% Nc; 66.5% Mc). In D. flu- amphipods were found only in N. kuhlii (2.6% Fo and viorum, polychaetes had the greatest contribution by 1.3% Fo, respectively), thalassinids (mud shrimps) number (46.6% Nc), but brachyuran crabs were the were found only in D. fluviorum (5.0% Fo), and most important prey category overall (95.0% Fo; tanaids were found in N. kuhlii (15.4% Fo) and D. flu- 38.7% Nc; 50.1% Mc; 52.6% IRI). In contrast, poly- viorum (5.0% Fo). Pardo et al.: Resource partitioning among intertidal stingrays 209

15 a Neotrygon kuhlii effect was detected when data were pooled into 13 13 n = 78 the 3 size classes, viz. small (150−249 mm DW; n = 9), medium (250−349 mm DW; n = 46) and large 11 (350−449 mm DW; n = 23) (ANOSIM, p < 0.001; R- 10 10 9 statistic = 0.253; see also Fig. S2 in the Supple- ment). Polychaetes were the dominant prey cate- 7 gory in all size classes, but their importance by mass decreased as body size increased: 85.5% M 5 c 5 for the small class, 68.2% Mc for the medium class 3 3 Y ear and 64.1% Mc for the large class (Fig. 5). Similarly, 2 2006 the importance of bivalves decreased with increas- 1 1 2012 ing size: 11.9%, 9.16% and 5.4% Mc for the small, 0 medium and large class, respectively. Carids and teleosts became more important with size, con- 15 b Himantura toshi tributing 13.0% and 3.7% Mc, respectively, in the n = 18 medium class, and 19.8% and 8.7% Mc, respectively, in the largest class. Carids, teleosts and brachyurans were absent from the smallest class, 10 whilst penaeids were absent from the largest class.

Count Sediment core analyses 5 In total, we collected 39 sediment core samples 22 2 2 2 2 1 1 1 11 1 from the study site in 2006, of which 1 lacked benthic macrofauna and was therefore removed from 0 analyses. Large clams (>8 cm total length) were 15 c Dasyatis ﬂuviorum also removed, as they were deemed too large to be n = 20 prey for the stingray species in this study. In total, 239 animals with a combined mass of 22.3 g were sieved from the sediment cores for analyses. Poly- 10 chaetes had the greatest relative importance of any faunal category (58.6% IRI), were very frequent

(92.3% Fo) and had the greatest contribution by number (51.9% Nc; Table 1, Fig. 4). Bivalves and gastropods were also important, with similar rela- 5 44 3 tive importance (15.4% and 15.0% IRI, respectively) 22 and contributions by mass (24.4% and 26.9% Mc, 11 11 1 respectively). Bivalves were more common than 0 gastropods (48.7% vs. 38.5% Fo), but gastropods were more numerous (17.6% vs. 11.72% N ). 100 200 300 400 500 600 70 0 c Brachyurans were as common as gastropods (38.5% Disc width (mm) Fo) and had moderate mass contributions (18.94% Mc), but overall were of little importance (8.9% Fig. 3. Size distributions of (a) Neotrygon kuhlii, (b) Himan- IRI). Similarly, anomurans were moderately com- tura toshi and (c) Dasyatis fluviorum caught in Wynnum Banks in 2006 (light grey bars) and 2012 (dark grey bars) mon (17.9% Fo), but had little numerical and mass contributions (3.4% Nc; 5.1% Mc) and were not important overall (1.3% IRI). Teleosts and isopods

Size-related dietary shifts in N. kuhlii were uncommon (both 5.1% Fo) and had very little relative importance (both 0.1% IRI). All other major The diet of N. kuhlii did not differ among size faunal categories were either absent from the sam- classes when analysed at the level of the individual ples or so infrequent that their contributions were (ANOSIM, p > 0.05); however, a weakly significant negligible. 210 Mar Ecol Prog Ser 533: 205–218, 2015 ) c N % IRI % c ows) % M c % N o Sediment samples % IRI% % F c ) and overall percentage(% overall numeric and ) o F % M c % N o % IRI% % F c % M c , and faunal composition of sediment samples collected at Wynnum Banks, More- Banks, Wynnum at collected samples sediment of composition faunal and , % N o Himantura toshi % IRI% % F c and % M c % N 0.16 0.01 0.00 10.0 0.70 0.05 0.05 0.0 0.00 0.00 0.00 5.1 1.26 0.41 0.07 1.74 16.08 4.64 55.0 10.07 26.03 12.45 77.8 52.38 62.49 65.16 2.6 0.42 1.63 0.05 Neotrygon kuhlii Dasuatis fluviorum Himantura toshi o F 9.0 0.19 0.88 5.0 0.23 0.13 33.3 18.32 17.34 0.0 0.00 0.00 Dasyatis fluviorum 10.3 0.45 0.91 75.0 12.18 14.37 5.6 1.10 0.15 10.3 1.67 1.24 sp. 5.1 0.13 0.95 60.0 15.93 24.08 0.0 0.00 0.00 12.8 2.09 16.48 Neotrygon kuhlii , ) contributions are for %IRI were also compared. only calculated for the prey Values categories chosen for comparison (shaded r c sp. 1.3 0.03 0.20 0.0 0.00 0.00 0.0 0.00 0.00 0.0 0.00 0.00 M sp. 0.0 0.00 0.00 5.0 0.23 0.08 0.0 0.00 0.00 0.0 0.00 0.00 0.0 0.00 0.00 0.00 5.0 0.70 3.22 0.12 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 sp. 19.2 0.61 7.56 0.0 0.00 0.00 33.3 20.88 26.91 0.0 0.00 0.00 10.3 0.29 1.21 0.09 5.0 0.23 0.13 0.01 50.0 28.94 23.04 18.95 0.0 0.00 0.00 0.00 1.3 0.03 0.00 0.00 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 2.6 0.84 0.12 0.02 15.4 0.56 0.09 0.06 5.0 0.23 0.01 0.01 0.0 0.00 0.00 0.00 5.1 0.84 0.07 0.04 28.2 0.88 2.26 0.50 95.0 38.17 50.08 52.57 66.7 18.32 14.31 15.86 38.5 7.53 18.94 8.91 2.6 0.05 0.05 0.00 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 17.9 3.35 5.05 1.32 3.8 66.7 2.96 19.61 100.0 49.18 79.45 100.0 99.63 99.84 38.5 11.30 25.62 46.2 Mictyris Macrophthalmus Unidentified Macrophthalminae 69.2 3.71 19.71 100.0 50.12 79.51 100.0 99.63 99.84 41.0 14.23 26.22 Unidentified Alpheidae 24.4 0.59 5.04 0.0 0.00 0.00 11.1 0.73 0.71Alpheus 0.0 0.00 0.00 Unidentified ocypodid 2.6 0.05 0.10 0.0Macrophthalminae 0.00 0.00 16.7 3.66 6.96 0.0 0.00 0.00 Unidentified penaeid 3.8 0.08 0.14 0.0Metapenaeus 0.00 0.00 16.7 10.62 5.70 0.0 0.00 0.00 Metapenaeus bennettae and mass (% mass and Unidentified isopod 3.8 0.16 0.01 5.0Flabellifera 0.23 0.02 0.0 0.0 0.00 0.00 0.00 0.00 0.0Epicaridea 0.0 0.0 0.00 0.00 0.00 0.00 0.00 0.00 0.0 5.0 0.00 0.00 0.47 0.02 5.1 0.0 0.00 0.00 0.00 0.00 0.0Unidentified tanaid 0.00 15.4 0.00 0.56 0.09 5.0 0.23 0.01 0.0 0.00 0.00 5.1 0.84 0.07 Majidae 1.3 0.03 0.01 5.0Grapsidae 0.70 0.04 0.0 0.0 0.00 0.00 0.00 0.00 0.0 2.6Portunidae 0.0 0.00 0.00 0.42 22.2 0.05 6.96 2.63 0.00 0.00 0.0 0.0 0.00 0.00 0.00 0.00 11.1 1.83 0.49 0.0 0.00 0.00 Unidentified amphipod 1.3 0.03 0.00 0.0 0.00 0.00 0.0 0.00 0.00 2.6 0.84 0.12 Mictyridae Diogenidae 2.6 0.05 0.05 0.0Unidentified anomuran 0.00 0.00 0.0 0.0 0.00 0.00 0.00 0.00 15.4 2.93 4.16 0.0 0.00 0.00 0.0 0.00 0.00Calianassidae 2.6 0.0 0.42 0.89 0.00 0.00 5.0 0.70 3.22 0.0 0.00 0.00 0.0 0.00 0.00 Unknown carid 20.5 0.53 3.48 30.0 2.58 3.81 22.2 18.68Alpheidae 32.1 1.20 3.19 12.60 0.0 25.0 6.56 0.00 0.00 22.04 50.0 32.97 59.06 2.6 0.42 1.63 Paleomonidae 0.0 0.00 0.00 0.0 0.00 0.00 5.6 0.73 0.25 0.0 0.00 0.00 Unidentified brachyuran 10.3 0.21 0.28 45.0 9.13 11.51 38.9 4.76 4.07 20.5 3.35 1.18Ocypodidae Penaeidae Tanaidacea Amphipoda Isopoda Thalassinidea Brachyura Anomura Penaeoidea Caridea Decapoda % Prey categories Crustacea Table 1. Dietary composition of composition Dietary 1. Table ton Bay, Australia. Importance is displayed by the percentage index of relativepercentageof the Frequencyimportanceindex by ImportanceoccurrenceIRI). displayed Australia. of (% is (% Bay, ton Pardo et al.: Resource partitioning among intertidal stingrays 211 % IRI % c % M c % N o Sediment samples % IRI% % F c % M c % N o 0.0 0.00 0.00 2.6 0.84 0.15 % IRI% % F c % M c % N o Table 1 (continued) Table % IRI% % F c % M c % N 0.08 0.29 0.01 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 2.6 0.42 0.04 0.02 Neotrygon kuhlii Dasuatis fluviorum Himantura toshi o F 0.0 0.00 0.00 0.0 0.00 0.00 0.0 0.00 0.00 2.6 0.42 0.04 0.0 0.00 0.00 0.0 0.00 0.00 0.0 0.00 0.00 17.9 2.93 0.27 1.3 0.03 0.01 0.0 0.00 0.00 0.0 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 0.00 0.00 0.0 0.0 0.00 0.00 0.00 0.00 0.00 17.9 2.93 0.27 0.50 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 38.5 17.57 26.85 14.96 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 2.6 0.42 0.04 0.02 70.5 2.46 7.32 3.89 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 48.7 11.72 24.43 15.41 1.3 0.03 0.01 0.00 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 0.0 0.00 0.00 0.00 100.0 93.16 66.53 90.04 85.0 46.60 15.09 32.88 0.0 0.00 0.00 0.00 92.3 51.88 20.60 58.57 70.5 2.46 7.32 0.0 0.00 0.00 0.0 0.00 0.00 71.8 29.29 51.28 20.5 0.56 6.13 0.77 35.0 3.28 5.40 1.91 5.6 0.37 0.16 0.02 5.1 0.84 1.55 0.11 3.8 Unidentified worm 3.8 0.08 0.29 0.0 0.00 0.00 0.0 0.00 0.00 2.6 0.42 0.01 Unidentified bivalve 70.5 2.46 7.32 0.0 0.00 0.00Veneridae 0.0 0.0 0.00 0.00 0.00 0.00 17.9 2.93 0.0 16.02Cardiidae 0.00 0.00 0.0 0.0 0.00 0.00 0.00 0.00 30.8 7.11 5.05Lucinidae 0.0 0.0 0.00 0.00 0.00 0.00 0.0 0.0 0.00 0.00 0.00 0.00Arcidae 0.0 5.1 0.0 0.00 0.00 0.84 1.03 0.00 0.00 2.6 0.0 0.84 2.33 0.00 0.00 0.0 0.00 0.00 0.0 0.00 0.00 Unidentified teleost 17.9 0.48 3.52 35.0 3.04 4.37 0.0 0.00 0.00Gobiidae 0.0 3.8 0.00 0.00 0.08 2.62 5.0Syngnathidae 0.23 1.04 0.0 0.0 0.00 0.00 0.00 0.00 0.0 5.1 0.00 0.00 0.84 1.55 5.6 0.37 0.16 0.0 0.00 0.00 Muricidae 0.0 0.00 0.00 0.0Nassariidae 0.00 0.0 0.00 0.00 0.00 0.0 0.00 0.0 0.00Trochidae 0.00 0.00 5.1 0.84 0.0 0.0 0.17 0.00 0.00 0.00 0.00 12.8 4.60 0.79 0.0Batillaridae 0.00 0.00 0.0 0.00 0.0 0.00 0.00 0.00 0.0 0.00 5.1 0.00 0.84 0.23 0.0 0.00 0.00 20.5 11.30 25.65 Nereididae 0.0 0.00 0.00Phyllodocidae 0.0 0.0 0.00 0.00 0.00 0.00 0.0 0.0 0.00 0.00Cirratulidae 0.00 0.0 0.00 7.7 0.00 0.00 0.0 1.26 0.13 0.00 0.0 0.00 0.00 0.00Nephtyidae 7.7 0.0 1.26 0.0 0.54 0.00 0.00 0.00 0.00 0.0 5.1Oweniidae 0.0 0.00 0.00 0.84 2.41 0.00 0.00 0.0 0.0 0.00 0.00 17.9 4.18 1.70 0.00 0.00 0.0 0.00 0.00 5.1 0.84 0.07 Unidentified polychaete 88.5 11.48 35.38 85.0Opheliidae 21.08 11.37 0.0 21.8 3.79 0.08 0.00 0.00 43.6 0.0 12.13 0.00 0.00Eunicidae 4.73 0.0 48.7 2.83 0.00 0.00 15.48 5.1 15.0 0.70 1.81Terebellidae 0.84 0.04 0.0 5.1 0.00 0.00 28.2 5.02 7.75 0.32 1.53 0.0 Capitellidae 0.00 0.00 83.3 0.0 73.67 11.20 0.00 0.00 10.0Onuphidae 2.6 19.91 0.84 0.82 0.67 2.6 0.11 0.0 0.15 0.00 0.00 0.0Lumbrineridae/Oeonidae 64.1 20.5 0.96 2.71 0.00 0.00 23.85 25.0 4.92 1.09 2.42 0.0 0.00 0.00 0.0 0.00 0.00 Terebratulida Ophiuroidea Hirudinea Bivalvia Gastropoda % Prey categories Others Brachiopoda Echinodermata Mollusca Teleostei Hirudinea Polychaeta 212 Mar Ecol Prog Ser 533: 205–218, 2015

Fig. 4. Contributions in terms of (a) numbers, (b) mass and (c) percentage index of relative importance (% IRI), of major prey items to the diet of Neotrygon kuhlii, Dasyatis fluviorum and Himantura toshi, as well as the faunal composition of the sediment samples collected from Wynnum Banks. The category ‘Others’ includes anomurans, thalassinids, amphipods, isopods, tanaids, hirudineans, echinoderms, brachiopods and unidentified organisms

Dietary partitioning p > 0.05), and thus these were also pooled for analyses. Ordination of mean faunal mass values revealed The diets of N. kuhlii and H. toshi did not differ distinct clustering among species and the sediment between 2006 and 2012 (ANOSIM, p > 0.05), al- cores (Fig. 6a), and these were found to be signifi- though a weakly significant effect was detected for cantly distinct (ANOSIM, p < 0.001, R = 0.874). Fur- D. fluviorum (ANOSIM, p < 0.05, R = 0.365). For ther, all pairwise comparisons of groups were signifi- analyses, data from both years were pooled for each cant (ANOSIM, p < 0.008, R > 0.651), suggesting a species, including D. fluviorum because of the very degree of dietary partitioning. Likewise, when ana- small R-statistic. Faunal composition did not differ lysed at the level of the individual, diets differed sig- significantly among the sediment cores (ANOSIM, nificantly among species (ANOSIM, p < 0.001, R = Pardo et al.: Resource partitioning among intertidal stingrays 213

Fig. 5. Gravimetric contributions of major prey items to the diet of different size classes of Neotrygon kuhlii. The cate- Fig. 6. Non-metric multidimensional scaling ordination of (a) gory ‘Others’ includes anomurans, thalassinids, amphipods, pooled mass contributions and (b) individual mass contribu- isopods, tanaids, hirudineans, echinoderms, brachiopods tions of the major prey categories ingested by Neotrygon and unidentified organisms kuhlii, Dasyatis fluviorum and Himantura toshi, as well as the mean mass contributions of the faunal composition of the sediment samples. Symbols with black dots denote samples 0.557), with ordination revealing clustering among collected in 2012. Similarity matrices were created using Bray-Curtis similarity and Hellinger transformation groups with only slight overlap (Fig. 6b). Pairwise comparisons were also significant (ANOSIM, p < 0.001), although some were moderately weak; for given DW to that of D. fluviorum. PCA revealed that example, R = 0.296 between D. fluviorum and the Axis 1 explained 91.3% of the variation in the data sediment cores. No overlap was found among species and that Axis 2 explained a further 3.8% (Table 2, within each size class, suggesting that body size was Fig. 7d). Each species formed a distinct group on the not responsible for observed dietary differences (see PCA plot, and jaw measurements, standardised as a Fig. S3 in the Supplement). proportion of DW, differed significantly among the 3 species (ANOSIM, p < 0.001, R = 0.990). On PCA Axis 1, all eigenvalues were large, with the largest being

Jaw morphology for DSLUPPER, DSLLOWER and GWCLOSED (Table 2). Since these values were negatives, and points for D. A total of 29 N. kuhlii (154−440 mm DW), 14 D. flu- fluviorum lay to the left of N. kuhlii, the relative viorum (333−598 mm DW) and 2 H. toshi (553−692 lengths of DSLUPPER, DSLLOWER, JHUPPER, GWCLOSED mm DW) were measured for jaw morphometric com- and JDLOWER were greater for D. fluviorum than for parisons. N. kuhlii had numerous small cuspidate N. kuhlii. Eigenvalues for PCA Axis 2 were relatively teeth, whereas D. fluviorum and H. toshi had molari- high for JDUPPER, JHLOWER (negative values) and form teeth. Jaw robustness was similar between N. GWCLOSED (positive value). Since the points for D. flu- kuhlii and D. fluviorum, while the small sample of H. viorum clustered at the top of the plot, while the toshi did not allow for a rigorous assessment points for N. kuhlii are vertically spread, GWCLOSED in (Fig. 7a,b). Gape width (GWCLOSED) increased propor- D. fluviorum overlaps with N. kuhlii, which can have tionally with DW in both N. kuhlii and D. fluviorum, a relatively smaller gape. In contrast, JDUPPER and but for any given DW, gape was about 10 mm larger JHLOWER overlapped between species, with these in D. fluviorum (Fig. 7c). Although limited, data for measurements in D. fluviorum overlapping only with H. toshi suggested a gape width similar in size for a the relatively smaller values in N. kuhlii. 214 Mar Ecol Prog Ser 533: 205–218, 2015

Fig. 7. Analysis of jaw morphology measurements between Dasyatis fluviorum, Neotrygon kuhlii and Himantura toshi. (a) Relationship between upper jaw robustness (JHUPPER × JDUPPER; abbreviations as in Fig. 2) and disc width (DW). (b) Relation- ship between lower jaw robustness (JHLOWER × JDLOWER) and DW. (c) Relationship between closed gape width and DW; dark grey trend line shows linear model fit for D. fluviorum, while light grey indicates fit for N. kuhlii. (d) Plot of principal component analysis Axis 1 vs. Axis 2 of the 7 mouth measurements of N. kuhlii, D. fluviorum, and H. toshi. Measurements were calculated as a proportion of DW

DISCUSSION (Kulbicki et al. 2005, Jacobsen & Bennett 2012, O’Shea et al. 2013). Polychaetes were the most Dietary partitioning important faunal category in the sediment cores (58.6% IRI), which implies an abundance of food for Our study provides evidence of dietary partitioning N. kuhlii in this habitat. Brachyurans, the preferred among the sympatric stingrays Neotrygon kuhlii, prey of D. fluviorum (52.6% IRI), were not important Dasyatis fluviorum and Himantura toshi at Wynnum in the sediment cores (8.9% IRI), but were moder-

Banks, Moreton Bay, Australia. Ordination of stom- ately frequent (38.5% Fo). Polychaetes were the spe- ach contents revealed that the species’ diets differed cies’ next most important prey, which suggests that significantly from each other and from the observed overall the habitat provides good feeding opportuni- composition of potential prey items in their intertidal ties for D. fluviorum. Conversely, carid shrimp, the feeding habitat. Polychaete worms were by far the preferred prey of H. toshi (65.2% IRI), were limited in most important prey category for N. kuhlii (90.0% the sediment cores (0.05% IRI, 2.6% Fo), and penaeid IRI), consistent with previous studies on this species prawns, the next most important prey, were absent. Pardo et al.: Resource partitioning among intertidal stingrays 215

Table 2. Eigenvalues and percentage cumulative variation explained by 5 reported to feed primarily on crus- principal component axes using proportional mouth measurements of 29 taceans (Jacobsen & Bennett 2012); Neotrygon kuhlii,14 Dasyatis fluviorum, and 2 Himantura toshi. Eigenvectors however, in our study polychaetes for the 7 measurements in relation to these axes are also provided. GW: gape width, DSL: dental set length, JH: jaw height, JD: jaw depth. See Fig. 2 for were the dominant prey item. Differ- measurements ences within and among species might exist simply because of differ- Principal component axis ences in habitat or prey availability, 1 2 3 4 5 although it is likely that, at least in some cases, localised dietary parti- Eigenvalue 0.000311 0.000013 7.46 × 10−6 6.07 × 10−6 2.16 × 10−6 tioning is an important factor in driv- Variation (%) 91.3 3.8 2.2 1.8 0.6 ing these divergences. Cumulative 91.3 95.1 97.3 99.1 99.7 variation (%) Eigenvectors GWCLOSED −0.618 0.387 0.641 0.236 0.042 Dietary or habitat partitioning? DSLUPPER −0.605 −0.103 −0.239 −0.727 −0.178 DSLLOWER −0.474 −0.080 −0.633 0.602 0.065 A challenge in investigating dietary JH −0.059 −0.149 0.016 0.032 −0.237 UPPER partitioning is that often it cannot be JDUPPER −0.071 −0.684 0.309 0.207 −0.480 JHLOWER −0.029 −0.170 0.057 0.067 −0.261 unambiguously disentangled from JDLOWER −0.137 −0.561 0.177 −0.070 0.779 habitat partitioning, usually because studies are conducted at scales larger than the species’ common feeding habitat (Braccini et al. 2005). For this Although brachyurans were moderately important reason, conclusions about dietary partitioning must for this species (15.9% IRI), this habitat overall be taken cautiously, because habitat partitioning can appears limited in its food resources for H. toshi. Our be an important mechanism by which elasmobranchs findings thus suggest that H. toshi is the most selec- mitigate competition. A recent study on 5 sympatric tive feeder in this habitat, possibly expending more stingray species at Ningaloo Reef, Western Australia, energy when hunting its prey. found that only 1 species, H. uarnak, had a signifi- Diets of Dasyatis and Himantura tend to be charac- cantly distinct diet (O’Shea et al. 2013). In the terised by crustacean specialisation, although some absence of dietary partitioning, habitat partitioning species in these genera differ markedly (Jacobsen & was postulated as a potentially important coexistence Bennett 2013). For example, D. marmorata has a mechanism for the other 4 species, which were broad diet of molluscs, teleosts, crustaceans and observed to occupy different microhabitats (parti- polychaetes (Capapé & Zaouali 1992), while D. tioning within metres). Similarly, Vaudo & Heithaus chrysonota specialises on polychaetes (Ebert & Cow- (2011) showed habitat separation among nearshore ley 2003), and D. tortonesei feeds mostly on teleosts elasmobranchs in Shark Bay, Western Australia; and molluscs (Capapé 1978). Similarly, crustaceans adults tended to be caught adjacent to rocky sub- are the most common prey of many Himantura spe- strates, and juveniles were commonly caught over cies, but H. uarnak and H. alcockii prefer teleosts open sand−seagrass habitats. Thus, observed differ- (Jacobsen & Bennett 2011, 2013). The diets of ences in diet within and among species may be a maskrays (genus Neotrygon) vary considerably in the consequence of habitat partitioning depending on relative importance of crustaceans and polychaetes; the scale at which organisms are sampled. To N. kuhlii and N. annotata are polychaete specialists address this issue, we sampled at a single intertidal (Kulbicki et al. 2005, Jacobsen & Bennett 2012, flat (~ 1 km2) where prey availability is constrained. O’Shea et al. 2013, this study), while N. picta feeds However, it is possible that even within this spatial mostly on crustaceans (Jacobsen & Bennett 2012). scale species might segregate between microhabitats Moreover, differences might occur within species, (within metres, e.g. seagrass beds and bare mud- such as among populations (Powter et al. 2010, Som- flats), which differ in their benthic faunal composi- merville et al. 2011), age classes (Bizzarro et al. 2007, tions. Further insights into the mechanisms enabling Marshall et al. 2008, Taylor & Bennett 2008, Vaudo & coexistence can be gained by investigating spatial Heithaus 2011) and seasons (Talent 1976, Som- segregation and microhabitat use using radio merville et al. 2011). For ex ample, smaller individu- telemetry or, in areas with low water turbidity, visual als (DW ≤ 220 mm) of N. kuhlii have been previously surveys. 216 Mar Ecol Prog Ser 533: 205–218, 2015

Caveats evolved with dietary partitioning among these species. D. fluviorum has a proportionately larger, but Two central assumptions of our study were that similarly robust, gape in comparison to N. kuhlii, stingrays were feeding at the study site prior to cap- suggesting that it can ingest larger prey relative to ture, and that the benthic faunal samples are repre- its body size. However, the smaller gape of N. kuh- sentative of the prey items available to the stingrays. lii may be an advantage, as it likely allows for a For most specimens, stomachs were full with prey in proportionately stronger pressure gradient force, the early stages of digestion, suggesting that feed- which is the strongest force used by suction- ing had occurred shortly before capture. Further, feeding aquatic predators (Wainwright & Day stingrays are known to have daily activity spaces of 2007). This may allow N. kuhlii to extract prey that about 1 km2 (Cartamil et al. 2003, Tilley et al. 2013), is deeper in the sediment, which agrees with their and mark−recapture data on H. toshi and N. kuhlii in preference for infaunal polychaete prey. Moreover, Moreton Bay indicate that these species have high tooth morphology differed between the species, site fidelity (Pierce et al. 2011). For these reasons, we with D. fluviorum and H. toshi having a more believe it is sensible to assume that feeding had molariform dentition, while N. kuhlii had numerous occurred within, or nearby, the study site prior to small cuspidate teeth (see Fig. S4 in the Supple- capture. Whether benthic samples are representative ment). These may relate to their prey preferences, of available prey is more ambiguous. A study on cap- since molariform teeth are suited for crushing hard- tive N. kuhlii showed that they can hunt prey hidden bodied prey, while cuspidate teeth are suited to at depths of 5 cm with the same efficiency as with gripping soft-bodied worms. In addition to mouth shallower prey (Tillett et al. 2008). Furthermore, morphology, feeding in stingrays is influenced by O’Shea et al. (2012) reported 5.6 cm to be the mean their electrosensory capabilities (Jordan et al. depth of stingray pits at intertidal flats in Ningaloo 2009b). D. fluviorum has shorter and smaller elec- Reef (Pikitch et al. 2005), while D’Andrea et al. (2004) troreceptive pores than N. kuhlii (Camilieri-Asch et reported stingray pits reaching 15 cm in depth. Since al. 2013), which may relate to its preference for epi- we sampled to 20 cm, it is possible that we collected fauna. Warranting further study, it seems likely that fauna unavailable to stingrays in this habitat. Sam- many batoids have evolved divergent feeding and pling may have been further biased by the vertical sensory morphologies alongside the partitioning of movements of organisms with the tides (since their diets. stingrays feed at high tide, but we could sample only at low tide) and by escape behaviours in benthic fauna from collection-related disturbance. Another Conclusion confounding factor is that we only sampled on a short transect adjacent to the net, thus masking the spatial Our study provides evidence of localised dietary heterogeneity of benthic fauna across the feeding partitioning among the sympatric stingrays N. kuhlii, area and biasing our assessment of available benthic D. fluviorum and H. toshi in Moreton Bay, Australia. prey. An ideal sampling regime would require sedi- These species forage at the same spatiotemporal ment samples taken randomly throughout the whole scale, yet vary significantly in their diets and in the mudflat. Moreover, sediment sampling was not con- prey items available in their intertidal feeding habi- ducted in 2012, and benthic assemblages may have tat. Moreover, N. kuhlii and D. fluviorum differed changed since 2006. However, because the diets of 2 considerably in their mouth morphologies, which stingray species did not vary significantly between likely relates to their dietary preferences. Given the collection years, it is likely that benthic faunal assem- diversity of mesopredatory batoids in Moreton Bay, blages remained relatively unchanged between our results suggest that their stable coexistence is at these events. While taken with caution, we believe least partly due to dietary partitioning. The differ- that the sediment samples are likely representative ences in functional diversity among stingrays could of the prey available to the stingrays at the study site. potentially increase resilience and enhance ecosystem functioning (Cardinale et al. 2002, Finke & Sny- der 2008). Future studies exploring the differential Jaw morphology use of resources by these species, such as microhabitat preferences, will shed light on the role that Feeding morphology was found to differ between these mesopredators play in maintaining healthy N. kuhlii and D. fluviorum, which may have co - eco systems. Pardo et al.: Resource partitioning among intertidal stingrays 217

Acknowledgements. We are extremely grateful to John nota (Smith, 1828) in South African waters. Mar Freshw Page for allowing us to participate in his commercial fishing Res 54:957−965 operation and making this study possible. We also thank Finke DL, Snyder WE (2008) Niche partitioning increases Scott Cutmore for help in the collection of specimens; mem- resource exploitation by diverse communities. Science bers of the Shark and Ray Research Group at the University 321: 1488−1490 of Queensland for their assistance throughout collection, Gilliam D, Sullivan KM (1993) Diet and feeding habits of the analysis and writing; and Carla Evangelista and Ricky Glee- southern stingray Dasyatis americana in the central son for assistance with dissections. We are also grateful to Bahamas. Bull Mar Sci 52: 1007−1013 Maria José Juan Jordá and Jennifer Bigman for comments Hess PW (1961) Food habits of two dasyatid rays in on the manuscript, and to Lindsay Davidson for help with Delaware Bay. 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Editorial responsibility: Janet Ley, Submitted: June 25, 2014; Accepted: May 14, 2015 St. Petersburg, Florida, USA Proofs received from author(s): July 24, 2015