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Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.47 no.5 Valparaíso nov. 2019

http://dx.doi.org/10.3856/vol47-issue5-fulltext-10 

Research Article

Dietary composition and trophic level of Hypanus marianae (Myliobatiformes: Dasyatidae), captured off Pernambuco coast, Brazil

Aristóteles P.N. Queiroz1  2 

Maria L.G. Araújo3 

Rosângela P.T. Lessa1  2 

1Universidade Federal de Pernambuco, Programa de Pós-graduação em Biologia Animal, Recife, Brasil

2Laboratório de Dinâmica de Populações Marinhas-DIMAR, Departamento de Pesca e Aquicultura Universidade Federal Rural de Pernambuco, Recife, Brazil

3Departamento de Pesca e Aquicultura, Universidade Federal de Sergipe, São Cristóvão Sergipe, Brasil

ABSTRACT

Hypanus marianae, a stingray endemic to Brazil, inhabits coastal coral reef areas occurring in the landings of artisanal fisheries. The present study aimed to characterize the diet of this species captured off Pernambuco. We obtained 77 stomachs with contents: 52.27% female, 47.72% male. DW ranged from 15 to 37.80 cm mean of 26.53 ± 4.82 cm. Four higher taxonomic prey categories were identified: Arthropoda, Annelida, Chordata and Sipuncula. The most important item in the diet was Polychaeta (40.65% IRI), followed by Leptochela serratorbita (30.35% IRI), suborder Dendrobranchiata (10.18% IRI), order Isopoda (4.19% IRI), and Meiosquilla schmitti (3.56% IRI). H. marianae displays specialized predatory habit (BA = 0.06) primarily based on shrimps (42.36% IRI) and polychaetes (40.65% IRI). There was no significant difference in the diet by sex or in sexual development stages. However, neonates fed on decapods crustaceans (70.68%) and polychaetes (17.09%). For immatures, decapod crustaceans (69.5%) and polychaetes (25.86%) made up most of their diet. The adults feed mainly on polychaetes (62.79%) and crustacean decapods (30.47%), with a slight increase of fish (5.46%). The trophic level (TL) estimated was based on stomach content analysis was 3.66 and estimated on the analysis of stable isotopes being 3.29, which classified the species as a mesopredator.

Keywords: Dasyatis marianae; elasmobranchs; endemic ray; trophic ecology; South America

INTRODUCTION

In tropical regions, the most numerous groups of Batoidea are the Myliobatiformes (Ebert & Compagno, 2007; Aschliman et al., 2012). The rays of the Myliobatiformes order account for 43% of all batoids and for more than 22% of all known species of Chondrichthyes (Ebert & Compagno, 2007; Weigmann, 2016).

In Brazil, out of 26 species of the Myliobatiformes order (Rosa & Gadig, 2014), seven species of the Dasyatidae family occupy coastal and estuarine environments (Bigelow & Schroeder, 1953; McEachran & Carvalho, 2002; Santos & Carvalho, 2007). Hypanus marianae (Gomes, Rosa & Gadig, 2000) is endemic to coastal areas of northeastern Brazil (Bender et al., 2013; Costa et al., 2017), occurring in artisanal fisheries (Yokota & Lessa, 2007) where it is locally named “big-eye-stingray” or “coã-stingray”.

Adult specimens of big-eye-stingray occupy coral reef areas, with seagrass beds as the preferred habitat of females, while immature stingrays concentrate on sandy bottoms, near the beach and on sandbanks (Gomes et al., 2000; Costa et al., 2015). Coastal sandbanks are likely the primary nursery areas for this species (Yokota & Lessa, 2006).

The feeding biology of elasmobranchs have been investigated in the last decade in order to describe the diet of the species (Wetherbee & Cortés, 2004; Navia et al., 2007; Albo-Puigserver et al., 2015; López et al., 2016; Wilga et al., 2016); to understand the role of given species in marine ecosystems (Wetherbee & Cortés, 2004; Navia et al., 2007; Albo-Puigserver et al., 2015; Madigan et al., 2015; López et al., 2016); to estimate predation impacts on economically valuable or threatened species (Myers et al., 2007) as well as to elucidate the biomechanic processes involved in predation strategies (Dean et al., 2005; Wilga et al., 2016). However, studies on the feeding biology of elasmobranchs are more frequently focused on shark species.

Quantitative studies on Dasyatidae stingrays' diet and trophic ecology being scarce (Aguiar & Valentin, 2010; Shibuya & Rosa, 2011) though, this researches may contribute to a better understanding of the mesopredators' role and can help in the development of ecosystem-based management approaches (Heithaus et al., 2008; Rocchi et al., 2017), as this information increases the understanding of the fishing impacts on mesopredator species (Grubbs et al., 2016).

The combination of traits such as endemism, small body and feeding of invertebrates, may drive H. marianae to a high-risk probability of extinction (Bender et al., 2013) since its preferred habitats are highly sensitive to environmental changes. In IUCN assessments, H. marianae is classified as DD (Data Deficient) due to the lack of information necessary to adequately assess its extinction risk (Rosa & Furtado, 2016). Thus, the objective of the current study is to analyze the diet and to verify the occurrence, or not, of sexual and ontogenetic changes in H. marianae, landed along the Pernambuco coast. Furthermore, the trophic level of the species will be inferred through the stomach contents and stable isotope analysis.

MATERIALS AND METHODS

Sample collection

The specimens of Hypanus marianae were obtained from artisanal fisheries off Pernambuco coast, Brazil (7°37′33.6″S, 34°48′52.4″W to 8°53′19.0″S, 35°08′59.8″W). The sample sites were Ponta de Pedras (PP), Itamaracá (IT), Sirinhaém (SI) and São José da Coroa Grande (SJ), where the individuals are captured as bycatch in fish-weirs, in beach seine, shrimp trawl and longline, respectively (Fig. 1).

Figure 1 Locations of landings of Hypanus marianae in Pernambuco, Brazil, in Ponta de Pedras (PP), Itamaracá (IT), Sirinhaém (SI) and São José da Coroa Grande (SJ) from July 2013 to October 2016. 

After sampling, the specimens were sexed, photographed and weighed (in g). The disc width (DW) was measured (in cm), and the sexual development stages were determined by macroscopic analysis of the reproductive organs, according to the criteria established by ICES (2012).

The stomachs were removed and then stored in 4% formalin solution. After 48 h, the stomachs were excised, washed with tap water and the food contents were retained in a sieve mesh of 0.1 cm and preserved in 70°GL ethanol. The material was analyzed under a stereoscopic microscope, and food components were identified to the lowest possible taxonomic level. After, the items were separated, counted, and individually weighed to the nearest 0.0001 g (Cortés, 1997). The excess ethanol was removed with a paper towel (Magnusson et al., 2003; Aguiar, 2010).

Algae and sediment were considered accidental ingestions and thus were excluded from the analysis (as well as all unrecognized materials). Stomachs showing only unidentifiable material were treated as empty stomachs and were excluded from the analysis.

Quantitative analysis of diet

A prey accumulation curve (Cortés, 1997) was built using EstimateS© version 7.5.1 to verify whether the number of analyzed stomachs was sufficient to represent the species diet, based on the reduction of standard deviations. Thus, the percentage frequency of occurrence (O%), the numerical occurrence or number percentage (N%) and weight (W%) were calculated. The index of relative importance (IRI) was determined according to Pinkas et al. (1971), and also calculated as a percentage (%IRI) (Cortés, 1997): %IRI = (IRI / ΣIRI) × 100.

The diet niche breadth was estimated using Levin's index Bi (Krebs, 1999): Bi=1/Pj2 , where Pj is the fraction by IRI of each food j in the diet. The values were standardized for BA (Krebs, 1999): BA = (Bi-1) / (N-1), where N is the number of classes, and BA ranges from 0 to 1. Low values of BA indicate diets dominated by few prey items (specialist predators), while higher values indicate generalist diets.

The trophic level (TL) of the species, based on stomach contents, was also calculated (Cortés, 1999): TLk=1+(j=1nPj×TLJ) , where TLk is the trophic level of the species (k), Pj is the proportion of the prey category (j) in predator diet (k); n is the total number of prey categories, and TLj is the trophic level of the prey group (j). We used the trophic level values of the prey categories suggested by Ebert & Bizzarro (2007) for trophic level analysis in batoids.

The weight data of the food items were grouped into five categories of prey, suggested by Ebert & Bizzarro (2007): decapods (crustacean decapods); fishes (fish teleost); amphipods (amphipods and isopods); polychaetes (polychaetes worms) and other crustaceans (crustaceans not included in the decapod order).

Based on the weight of each prey category, the data of food items were transformed in square-root, and a Bray-Curtis similarity coefficient was used to construct a similarity matrix (Jacobsen & Bennet, 2012).

The one-way similarity analysis (ANOSIM) using the similarity matrix, was conducted considering individuals as samples and sex and sexual development stages as factors. The R-value resulted by the ANOSIM analysis (the strength of the factors on the samples) and the significance level (P) was evaluated using a random permutation test with 999 permutations (Clarke & Gorley, 2006). When R = 0, there are no differences among the groups (sex and sexual development stages) or the samples (stomach) in each group. When R = 1, the samples of the groups are similar, but the groups are different. Statistical significance was set at P <0.05. Diet similarity was also analyzed by non-metric multidimensional scaling analysis (nMDS).

Finally, the percentage of similarity (SIMPER) was used to estimate the contribution of each prey category to the diet of each factor (sex or sexual development stages). The analyses were performed using the software Primer v.6 (Clarke & Gorley, 2006).

Muscle tissue collection

Muscle samples of H. marianae were obtained from eight individuals, taken from the lower portion of the pectoral fin and stored frozen. As stipulated by Post (2002), muscle tissue samples from an herbivorous species were obtained (n = 2) to be used as a baseline. The species chosen were the teleost fish Sparisoma axillare (Steindachner, 1878), an herbivore (Rosa & Moura, 1997) that occurs in the same coral reef environment as H. marianae, which reflects the δ15N and δ13C value of the base of the food chain (Post, 2002).

Stable isotope analysis

The collected material was cut in 1 cm² cubes and placed in test tubes, following the methodology suggested by Kim & Koch (2012) for extraction of lipids from the tissue by the addition of 10 mL of petroleum ether. The test tubes were then shaken in Ultrasonic Washer (Ultracleaner 700 - Unique) for 15 min. The petroleum ether solution was discarded, and the procedure repeated. After, 10 mL of deionized water was added to extract the urea accumulated in the tissue; the test tube was stirred for 15 min, and then the deionized water solution was discarded and the process repeated twice.

After the extraction of lipids and urea, H. marianae muscle tissue samples were lyophilized. Finally, the material was macerated and subjected to stable isotope analysis on a mass spectrometer.

The values of δ were calculated from the reference standards of carbon (Pee Dee Belemnite) and nitrogen (atmospheric air), according to equation (Peterson & Fry, 1987):

δsample=[(RsampleRstandard)1×1,000],

where R represents the ratio of the heaviest to the lightest isotope (15N:14N; 13C:12C).

Trophic level estimate

The trophic level of the species was calculated using the formula described by Post (2002):

TLδ15N=TLbaseline+(δ15Npredatorδ15Nbaseline)1.5,

where TLδ15N is the trophic position of the predator, TLbaseline is the trophic position of the baseline (TLbaseline = 2), δ15Npredator is the δ15N value of the consumer, δ15Nbaseline is the δ15N value of the baseline and 1.5‰ is the expected enrichment in δ15N per trophic level.

The enrichment constant of δ15N used was based on a study by Galván et al. (2016), which estimated the trophic discrimination factors (TDF) and turnover rates in blood and muscle of the small nose fanskate Sympterygia bonapartii (Müller & Henle, 1841) through controlled feeding. The results found by Galván et al. (2016) led to an estimated TDF value for S. bonapartii of 1.5‰. Since the enrichment constant may vary according to the species studied (Post, 2002; Hussey et al., 2014), the estimated value for S. bonapartii was used because it lives in a benthic habitat similar that of H. marianae.

RESULTS

Out of 89 of Hypanus marianae specimens, 77 had a disc width (DW) of 15 to 37.80 cm (mean 26.53 ± 4.82 cm) and had identifiable stomach contents. Females represented 52.27% (15 to 37.80 cm DW) and males 47.72% (15.10 to 30.7 cm DW) of the total sample. The prey accumulation curve tends to an asymptote in the last five points of the curve (Fig. 2), meaning that the sample size was sufficient to represent the diet of the species.

Figure 2 Cumulative average and standard deviation of the Shannon-Wiener diversity index of food items in the stomachs of Hypanus marianae off Pernambuco coast, Brazil from July 2013 to October 2016. 

The four most frequent prey categories identified in this study were Arthropoda (Amphipoda, Decapoda, Isopoda and Stomatopoda); Annelida (Polychaeta); Chordata (Teleostei) and Sipuncula (Table 1).

Table 1 Occurrence (O), frequency of occurrence (FO%), number (n), numerical frequency (N%), weight in grams (W), weight frequency (W%) relative importance index (IRI), relative importance index in percentage (IRI%) and order of importance (OI-IRI) of the food items in diet of Hypanus marianae off Pernambuco coast, from July 2013 to October 2016. 

Prey's item O %FO n %N W %W IRI %IRI OI-IRI
Phylum Sipuncula 8 10.39 13 1.41 3.79 3.32 49.19 0.87 11
Phylum Annelida
Class Polychaeta 49 63.64 85 9.25 30.69 26.88 2299.30 40.65 1
Phylum Arthropoda
Class Crustacea
Order Decapoda
Suborder Pleocyemata
Family Palinuridae 2 2.60 2 0.22 0.06 0.05 0.69 0.01 19
Family Scillaridae
Scyllarides sp. 1 1.30 3 0.33 0.27 0.24 0.73 0.01 19
Suborder Dendrobranchiata 29 37.66 113 12.30 3.43 3.00 576.09 10.18 3
Family Penaeidae
Rimapenaeus constrictus 7 9.09 23 2.50 3.73 3.27 52.48 0.93 10
Sicyonia parri 2 2.60 4 0.44 0.12 0.11 1.41 0.02 18
Pleoticus muelleri 3 3.90 4 0.44 1.78 1.56 7.75 0.14 15
Family Caridae
Leptochaela serratorbita 30 38.96 340 37.00 8.08 7.07 1717.00 30.35 2
Family Sergestoidae 3 3.90 95 10.34 0.54 0.47 42.12 0.74 13
Acetes americanus 1 1.30 1 0.11 0.01 0.01 0.16 <0.01 20
Suborder Brachyura 8 10.39 10 1.09 5.79 5.07 63.97 1.13 9
Family Portunidae
Callinectes sp. 14 18.18 20 2.18 9.45 8.27 190.01 3.36 6
Callinectes exasperatus 2 2.60 5 0.54 2.96 2.60 8.16 0.14 15
Microphrys bicornutus 1 1.30 1 0.11 1.47 1.29 1.82 0.03 17
Family Upogebiidae
Upogebia sp. 6 7.79 7 0.76 0.98 0.86 12.63 0.22 14
Order Amphipoda 3 3.90 10 1.09 0.10 0.09 4.58 0.08 16
Order Isopoda 16 20.78 96 10.45 1.09 0.95 236.82 4.19 4
Class Cephalocarida 1 1.30 1 0.11 0.01 0.01 0.15 <0.01 20
Order Stomatopoda 11 14.29 24 2.61 2.45 2.15 67.98 1.20 8
Family Squillidae
Meiosquilla schmitti 12 15.58 50 5.44 8.53 7.47 201.19 3.56 5
Phylum Chordata
Class Actinopterygii
Teleost 7 9.09 7 0.76 8.48 7.42 74.40 1.32 7
Family Holocentridae
Holocentrus adscensionis 2 2.60 5 0.54 20.38 17.85 47.77 0.84 12
Total 77 100 919 100 114.18 100 5656.40 100

The most important item in H. marianae diet was the class Polychaeta (40.65% IRI), followed by Leptochela serratorbita (Spen Bate, 1888) (30.35% IRI), suborder Dendrobranchiata (10.18% IRI), order Isopoda (4.19% IRI), and Meiosquilla schmitti (Schmitt, 1940) (3.56% IRI) (Table 1).

The similarity analysis (ANOSIM) indicated no significant differences in feeding between the sexes (Global R = 0.04; P = 0.09) or in relation to sexual development stages (Global R = 0.02; P = 0.23). Results were also corroborated using non-metric multidimensional scaling analysis (nMDS), which revealed overlap in diet between the sexes and among the sexual development stages (Fig. 3).

Figure 3 Non-metric multidimensional scaling analysis (nMDS) of Hypanus marianae based on the weight of the diet items: females distribution polygon (dashed line), males distribution polygon (solid line), young of the year (square), immature (circle) mature (triangle). AMPH: Amphipoda; DECA: Decapoda; OCRUS: Other Crustacea; POLLY: Polychaete; INVERT: Invertebrates; FISH: fishes; YOY: young of the year. 

H. marianae showed low value in diet breadth based on Levin's index (BA = 0.06). Data showed a specialist feeding strategy, with a diet primarily based on shrimps (suborder Dendrobranchiata, family Sergestoidea, Rimapenaeus constrictus (Stimpson, 1871), Leptochela serratorbita (Spence Bate, 1888), Sicyonia parri (Burkenroad, 1934) and Pleoticus muelleri (Spence Bate, 1888)) with 42.36%, of IRI and polychaetes (40.65% IRI) (Table 1). Results corroborate with the similarity percentage analysis (SIMPER), which showed prey categories that most contributed to the diet of all groups (Table 2).

Table 2 Items contributing to the diet differentiation between sexes and among the sexual development stages of Hypanus marianae according to Similarity Percentage analysis (SIMPER). 

Sample number Sex Sexual development stages
Female (%) Male (%) YOY (%) Immature (%) Mature (%)
39 38 7 42 28
Decapods 73.01 37.98 70.68 69.5 30.47
Polychaetes 21.36 57.01 17.09 25.86 62.79
Fishes 3.93 0.02 - 0.01 5.46
Amphipods 0.62 0.83 12.23 0.95 -
Other crustaceans 0.59 3.53 - 2.66 0.99
Sipuncula 0.49 0.62 - 1.02 0.29

YOY: young of the year.

Neonates (young of the year) of H. marianae displayed a diet based on decapod crustaceans, polychaetes, and amphipods, whereas immature individuals displayed a diet mostly of decapod crustaceans and polychaetes. Similarly, the adults fed mainly on polychaetes, decapod crustaceans and fish (Table 2). Teleostei fish were found in seven examined stomachs, two adult males and five adult females; one was pregnant.

The trophic level (TL) estimated for H. marianae based on stomach content analysis was 3.66. The mean δ15N value was 11.68 ± 0.92, and the estimated TL was 3.29 ± 0.61 (Table 3).

Table 3 Mean values for δ13C and δ15N ± SD (standard deviation) and estimated trophic level through stomach content analysis (TL SCA) and stable isotope analysis (TL δ15N) for Hypanus marianae

Sample number Mean δ13C SD Mean δ15N SD TL SCA TL δ15N
Sparisoma axillari 2 -17.11 1.80 9.75 0.16 2.0* -
Hypanus marianae 8 -14.06 0.87 11.68 0.92 3.66 3.29

* Rosa & Moura (1997).

DISCUSSION

The cumulative prey curve for Hypanus marianae tended to an asymptote in 72 stomachs, more than twice the value found by Costa et al. (2015), in samples from the state of Rio Grande do Norte, whose asymptote was reached at 31 stomachs, probably because in this work almost twice as many food items were identified, compared to Costa et al. (2015). The early stabilization of the curve is justified by the small niche breadth found for H. marianae (BA = 0.06), indicating a reduced diversity of food items in the diet, which is typical of specialized diets, as is the case for Rhinobatos percellens from southern Brazil (Levin's index BA = 0.06) (Carmo et al., 2015).

H. marianae is associated with coral reefs (Gomes et al., 2000; Costa et al., 2015, 2017), reflecting a feeding strategy based on the predation of benthic reef organisms, such as small crustaceans and polychaetes. Similarly, in Australia and the Caribbean, the diets of Pastinachus ater, Himantura uarnak, Neotrygon kuhlii, Taeniura lymma, Urogymnus asperrimus (O'Shea et al., 2013) and Hypanus americanus are predominantly made up of polychaetes and shrimp (Tilley et al., 2013).

Although polychaetes have been a significant item in the diet of H. marianae, accounting for 40.65% of the IRI, shrimp (suborder Dendrobranchiata, family Sergestoidae, Rimapenaeus constrictus, Leptochela serratorbita, Sicyonia parri and Pleoticus muelleri) corresponded to 42.36% of IRI. Some other batoid from the Brazilian coast inhabiting the marine substrate also feeds mainly on polychaetes and crustaceans. The species Hypanus americanus (Aguiar, 2010), Hypanus guttatus (Silva et al., 2001; Carvalho-Neta & de Almeida, 2002; Gianeti, 2011), Urotrygon microphtalmum (Santander-Neto, 2015), Rioraja agassizii, Zapteryx brevirostris and Rhinoptera bonasus (Bornatowski et al., 2014) have shrimp or polychaetes as main groups of prey of the diet, similar to H. marianae.

According to Costa et al. (2015), shrimp of the suborder Dendrobranchiata (29.0% of IRI) and the class of Polychaeta (12.2% of IRI) were the second and the fourth most important items in the diet of H. marianae. However, Shibuya & Rosa (2011) indicated shrimp as the main item, with 70.57% of IRI, whereas polychaetes were only 0.76% of IRI. Overall, the decapod crustaceans tended to be one of the most important prey items for the stingrays (Bornatowski et al., 2010, 2014; Pardo et al., 2015) because shrimp and polychaetes are abundant prey for coralline stingrays (O'Shea et al., 2013).

The specialized diet of H. marianae based on shrimp and polychaetes can be due to the small mouth aperture, which limits prey size (Tilley et al., 2013). This consideration also fits for Zapteryx brevirostris, which feed on the same prey (Bornatowski et al., 2014).

It is known that some batoids capture and process their prey through movements of the oral cavity, allowing strict internal orientation of the water flow (Dean et al., 2005). As observed by Shibuya & Rosa (2011), stomach contents of H. marianae suggest similar foraging behavior due to the presence of many preys from the same group, presenting a similar degree of digestion as well as the occurrence of sediments.

Furthermore, ANOSIM revealed no significant differences in diet between the sexes (Global R = 0.04; P = 0.09), similar to Hypanus longus (López-García et al., 2012); Urotrygon rogersi (Navia et al., 2011); Dasyatis chrysonota (Ebert & Cowley, 2003); Bathyraja brachyurops (Belleggia et al., 2008) and Bathyraja magellanica (Barbini et al., 2010). Nonetheless, nMDS showed an overlap of prey categories used by males and females (Fig. 3). The different contributions of the same food category for male and female diets (Polychaeta and Decapod Crustacea) (Table 2) can reflect sexual segregation for this species (Yokota & Lessa, 2006). Thus, teleostean fish in the adult female diet of H. marianae may be related to the use of different habitats. Thus, corroborating the observation by Yokota & Lessa (2007) and Costa et al. (2015) about ontogenetic and sexual segregation for H. marianae, which is also reinforced by Motta et al. (2009), who reported fishes from Scaridae family in the contents of a pregnant female captured in northern Brazil (Maranhão State).

Teleost fish are bigger and faster than shrimp, which explains the presence of this item almost exclusively in the adult diet - something that is related to their higher predation capacity (Sisneros & Tricas, 2002a) and their larger mouth width enabling the catch of larger prey. Size-related shifts in the diet for N. kuhlii (Pardo et al., 2015) were reported with decreasing importance of polychaetes and the increased importance of carid shrimp and teleost fishes. Although there are no significant differences in the diet among the sexual development stages for H. marianae (Global R = 0.02; P = 0.23; Fig. 3), the SIMPER showed an ontogenetic change in the contribution of each item in the diet of the stingray (Table 2). Also, a diet shift in batoids during ontogeny is widely known (Sisneros & Tricas, 2002b; Kyne et al., 2008; Jacobsen & Bennett, 2011; Vaudo & Heithaus, 2011; Yick et al., 2011; López-García et al., 2012; Ruocco & Lucifora, 2016).

Some factors related to diet shift are habitat change, an increase in the size of prey relative to an increase in the size of the predator, differences in movement patterns and an improvement in the ability to capture prey (Wetherbee & Cortés, 2004; Aguiar & Valentim, 2010; Grubbs, 2010).

Costa et al. (2015) suggest that the use of diverse habitats may result in different prey availability in each area, and this may explain the SIMPER results. In this study, neonates are found on the beaches, whereas larger individuals are found at greater depths, similar to reports on the species in other areas (Yokota & Lessa, 2007).

The trophic level estimated for H. marianae based on stomach content analysis (3.66) and δ15N value (3.29) places the species at an intermediate level of the food chain, as a mesopredator (Cortés, 1997; Ebert & Bizarro, 2007). Both the trophic levels (obtained through SCA and SIA) presented values expected for the Dasyatidae family, ranging between 3.16 and 4.08 (Jacobsen & Bennett, 2013).

Hypanus marianae in Brazil occupies a trophic level (TL = 3.6) similar to H. americanus (TL = 3.52) in the Caribbean (Tilley et al., 2013), Urotrygon aspidura (TL = 3.7) and U. rogersi (TL = 3.5) in Colombia (Navia et al., 2016), N. kuhlii (TL = 3.58), Neotrygon annotata (TL = 3.57), and Neotrygon picta (TL = 3.55) in Australia (Jacobsen & Bennett, 2012), Rhinoptera bonasus (TL = 3.4) in Brazil (Bornatowski et al., 2014) and Myliobatis goodei (TL = 3.2) in Patagonia (Molina & Cazorla, 2015), because their diet is based mainly on invertebrates.

Similarly, to other Myliobatiformes mesopredators (O'Gorman & Emmerson, 2009), H. marianae can play an important ecological role in the environment, controlling the populations of reef invertebrates used as prey, and being food source of other species (Vaudo & Heithaus, 2011) such as reef sharks (Costa et al., 2015) and other stingrays such as H. americanus (Branco-Nunes et al., 2016). Linking top predators to lower trophic levels, this species can promote the energy flow of the ecosystems it inhabits.

ACKNOWLEDGMENTS

We thank Dr. Luiz Martinelli (Universidade de São Paulo - CENA-ESALQ) and Dr. Nigel Hussey (University of Windsor-GLIER) for the stable isotope analyses. Thanks also to Esteban Vidal and Aldenise Oliveira (Centro de Tecnologias Estratégicas do Nordeste - CETENE) for lyophilizing the samples. This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq through APQ 483224/2013-8 and supplied a Productivity Research Grant to R.L. (PQ 306672/2015). Fundação de Amparo à Ciência e Tecnologia de Pernambuco-FACEPE supplied Scholarships to A.P. (IBPG-0658-2.04/14) and M.L. (Post Doctoral DCR 0086-5.06/12).

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Recibido: 13 de Diciembre de 2018; Aprobado: 01 de Agosto de 2019

Corresponding author: Aristóteles P.N. Queiroz (queirozapn@gmail.com)

Corresponding editor: Gustavo Macchi

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