Abstract
Describing the trophic structure and interactions of demersal elasmobranch assemblages is fundamental to understanding food web dynamics and developing ecosystem-based management approaches. Stomach content analysis (SCA) and stable isotope ratios (SIA) of carbon (δ13C) and nitrogen (δ15N) from muscle were used to examine the dietary habits and intra- and interspecific trophic ecology of three sympatric batoid species (Dasyatis pastinaca, Raja clavata, and Raja maderensis) from the Azores, Northeast Atlantic. Data were analyzed with respect to sex and maturity stages. SCA showed that D. pastinaca feeds mostly on crustaceans, whereas R. clavata and R. maderensis prey almost exclusively on teleosts, but not on the same species. Dasyatis pastinaca displayed higher δ13C and lower δ15N values compared to R. clavata and R. maderensis. Trophic niche breadth was variable, D. pastinaca and R. clavata had the broadest and the narrowest trophic breadth, respectively. Relative trophic position categorized D. pastinaca as a mesopredator, while R. clavata and R. maderensis occupied higher trophic positions. With size, R. clavata and R. maderensis shifted from small prey such as crustaceans to larger prey such as teleosts, and they also exhibited significant increases in δ15N with size. Dietary and isotopic overlap was overall low among species, but it was higher between R. clavata and R. maderensis, suggesting more similarity in diet and habitat use between them than with D. pastinaca. This study depicts trophic interactions and functional roles of three co-existing batoid species in the Azorean food webs. In addition to presenting new information on the trophic ecology of D. pastinaca and R. clavata, the present study provides, to our knowledge, the first description of the diet composition and trophic level of the Macaronesian endemic batoid R. maderensis.




Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Afonso AS, Hazin FH (2015) Vertical movement patterns and ontogenetic niche expansion in the tiger shark, Galeocerdo cuvier. Plos One 10:e0116720
Afonso P, Fontes J, Giacomello E, Magalhães MC, Martins HR, Morato T, Neves V, Prieto R, Santos RS, Silva MA (2020) The Azores: a mid-Atlantic hotspot for marine megafauna research and conservation. Front Mar Sci 6:826
Ajemian MJ, Powers SP (2014) Towed-float satellite telemetry tracks large-scale movement and habitat connectivity of myliobatid stingrays. Environ Biol Fish 97:1067–1081
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253
Ball RE, Serra-Pereira B, Ellis J, Genner MJ, Iglésias S, Johnson AF, Jones CS, Leslie R, Lewis J, Mariani S (2016) Resolving taxonomic uncertainty in vulnerable elasmobranchs: are the Madeira skate (Raja maderensis) and the thornback ray (Raja clavata) distinct species? Conserv Genet 17:565–576
Barreiros JP, Gadig OB (2011) Catálogo ilustrado dos tubarões e raias dos Açores. Instituto Açoriano de Cultura, Angra do Heroismo
Barrios-O’Neill D, Bertolini C, Collins PC (2017) Trophic cascades and the transient keystone concept. Biol Conserv 212:191–195
Bascompte J, Melian CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Natl Acad Sci USA 102:5443–5447
Bizzarro JJ, Robinson HJ, Rinewalt CS, Ebert DA (2007) Comparative feeding ecology of four sympatric skate species off central California. Environ Biol Fish 80:197–220
Bowen SH (1996) Quantitative description of the diet. In: Murphy BR, Willis DW (eds) Fisheries techniques. American Fisheries Society, Bethesda, pp 513–522
Brown SC, Bizzarro JJ, Cailliet GM, Ebert DA (2012) Breaking with tradition: redefining measures for diet description with a case study of the Aleutian skate Bathyraja aleutica (Gilbert 1896). Environ Biol Fish 95:3–20
Cailliet GM, Love MS, Ebeling AW (1996) Fishes: a field and laboratory manual on their structure, identification and natural history. Waveland, Long Grove
Carvalho N, Edwards-Jones G, Isidro E (2011) Defining scale in fisheries: Small versus large-scale fishing operations in the Azores. Fish Res 109:360–369
Coll-Calvo E, Barría C, Recasens L, Navarro J (2020) Feeding ecology of a Mediterranean endemic mesopredator living in highly exploited ecosystems. Mar Environ Res 157:104932
Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717
Da Silva HM, Pinho MR (2007) Small-scale fishing on seamounts. In: Pitcher TJ, Morato T, Hart PJB, Clark MR, Haggan N, Santos RS (eds) Seamounts: ecology fisheries and conservation, fisheries and aquatic resource series, vol 12. Blackwell, Oxford, pp 333–360
Daban IB, Cabbar K, Yiğin CÇ (2022) Feeding ecology of Thornback Ray, Raja clavata (Linnaeus 1758) in Gökçeada Island, Northern Aegean Sea, Turkey. Thalassas 38:197–211
Das D, Afonso P (2017) Review of the diversity, ecology, and conservation of elasmobranchs in the Azores region, mid-north Atlantic. Front Mar Sci 4:354
Das D, Gonzalez-Irusta JM, Morato T, Fauconnet L, Catarino D, Afonso P, Viegas C, Rodrigues L, Menezes G, Rosa A (2022) Distribution models of deep-sea elasmobranchs in the Azores, Mid-Atlantic Ridge, to inform spatial planning. Deep Sea Res I 182:103707
Debelius H (1997) Mediterranean and Atlantic fish guide. IKAN-Unterwasserarchiv, Frankfurt
Demirhan SA, Engin S, Seyhan K, Akamca E (2005) Some biological aspects of thornback ray (Raja clavata L., 1758) in the southeastern Black Sea. Turk J Fish Aquat Sci 5:75–83
Diggles B, Cooke S, Rose J, Sawynok W (2011) Ecology and welfare of aquatic animals in wild capture fisheries. Rev Fish Biol Fish 21:739–765
Diogo H, Pereira JG, Higgins RM, Canha Â, Reis D (2015) History, effort distribution and landings in an artisanal bottom longline fishery: an empirical study from the North Atlantic Ocean. Mar Policy 51:75–85
Dolgov A (2005) Feeding and food consumption by the Barents Sea skates. J Northwest Atl Fish Sci 35:495–503
Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LN, Fordham SV, Francis MP (2014) Extinction risk and conservation of the world’s sharks and rays. eLife 3:e00590
Dulvy NK, Walls R, Buscher E, Stehmann M (2015) Raja maderensis. In: IUCN 2023. IUCN red list of threatened species. Version 2023.2. www.iucnredlist.org. Accessed 17 Apr 2023
Ebert DA, Bizzarro JJ (2007) Standardized diet composition and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei). Environ Biol Fish 80:221–237
Ellis J, Dulvy N, Serena F (2016) Raja clavata. In: IUCN 2023. IUCN red list of threatened species. Version 2022.2. www.iucnredlist.org. Accessed 17 Apr 2023
Eronat EGT, Özaydın O (2015) Diet composition of the thornback ray, Raja clavata Linnaeus, 1758 (Elasmobranchii: Rajidae) in the Turkish Aegean Sea. Zool Middle East 61:38–44
Flowers KI, Heithaus MR, Papastamatiou YP (2021) Buried in the sand: uncovering the ecological roles and importance of rays. Fish Fish 22:105–127
Frisch AJ, Cole AJ, Hobbs J-PA, Rizzari JR, Munkres KP (2012) Effects of spearfishing on reef fish populations in a multi-use conservation area. PLoS One 7:e51938
Gardener M (2014) Community ecology: analytical methods using R and Excel. Pelagic Publishing, Exeter
Gomes FV, Pinto FT (2004) Azores Islands (Portugal). EUROSION Case Study Instituto de Hidráulica e Recursos Hídricos, Lisboa
Grubbs RD, Carlson JK, Romine JG, Curtis TH, McElroy WD, McCandless CT, Cotton CF, Musick JA (2016) Critical assessment and ramifications of a purported marine trophic cascade. Sci Rep 6:1–12
Gül G, Demirel N (2020) Trophic interactions of uncommon batoid species in the sea of Marmara. J Black Sea/Medit Environ 26:294–309
Gül G, Demirel N (2022) Ontogenetic shift in diet and trophic role of Raja clavata inferred by stable isotopes and stomach content analysis in the Sea of Marmara. J Fish Biol 101:560–572
Hayward PJ, Ryland JS (1990b) The marine fauna of the British Isles and north-western Europe. Vol. 2. Molluscs to chordates. Clarendon Press, Oxford
Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK (2014) Sizing up the ecological role of sharks as predators. Mar Ecol Prog Ser 495:291–298
Hussey NE, Dudley SF, McCarthy ID, Cliff G, Fisk AT (2011) Stable isotope profiles of large marine predators: viable indicators of trophic position, diet, and movement in sharks? Can J Fish Aquat Sci 68:2029–2045
Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SF, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17:239–250
Hyslop E (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429
Ismen A (2003) Age, growth, reproduction and food of common stingray (Dasyatis pastinaca L., 1758) in Iskenderun Bay, the eastern Mediterranean. Fish Res 60:169–176
Jabado R, Chartrain E, De Bruyne G, Derrick D, Dia M, Diop M, Doherty P, Leurs G, Metcalfe K, Pacoureau N, Pires J, Ratão S, Seidu I, Serena F, Soares A, Tamo A, Vander Wright W, Williams A (2021) Dasyatis pastinaca. In: IUCN 2013. IUCN red list of threatened species. Version 2022.2.www.iucnredlist.org. Accessed 17 Apr 2023
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602
Jacobsen IP, Bennett MB (2013) A comparative analysis of feeding and trophic level ecology in stingrays (Rajiformes; Myliobatoidei) and electric rays (Rajiformes: Torpedinoidei). PLoS One 8:e71348
Jargowsky MB, Cooper PT, Ajemian MJ, Colvin ME, Drymon JM (2020) Discerning the dietary habits of the smooth butterfly ray Gymnura lessae using two distinct methods, otolith identification and metagenetics. J Fish Biol 96:434–443
Kabasakal H (2002) Cephalopods in the stomach contents of four Elasmobranch species from the northern Aegean Sea. Acta Adriat 43:17–24
Kadri H, Marouani S, Bradai MN, Bouaïn A (2014) Diet and feeding strategy of thornback ray, Raja clavata (Chondrichthyes: Rajidae) from the Gulf of Gabes (Tunisia—Central Mediterranean Sea). J Mar Biol Assoc UK 94:1509–1516
Kinney MJ, Hussey NE, Fisk AT, Tobin AJ, Simpfendorfer CA (2011) Communal or competitive? Stable isotope analysis provides evidence of resource partitioning within a communal shark nursery. Mar Ecol Prog Ser 439:263–276
Kolmann MA, Huber DR, Motta PJ, Grubbs RD (2015) Feeding biomechanics of the cownose ray, Rhinoptera bonasus, over ontogeny. Janat 227:341–351
Krebs CJ (1999) Ecological Methodology, 2nd edn. Benjamin Cummings, California
Last PR, White WT, de Carvalho MR, Séret B, Stehmann MF, Naylor GJP (2016) Rays of the world. CSIRO Publishing, Clayton
Laverock B, Gilbert JA, Tait K, Osborn AM, Widdicombe S (2011) Bioturbation: impact on the marine nitrogen cycle. Biochem Soc Trans 39:315–320
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48
Li Y, Zhang Y, Hussey NE, Dai X (2016) Urea and lipid extraction treatment effects on δ15N and δ13C values in pelagic sharks. Rapid Commun Mass Spectrom 30:1–8
Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77:838–846
Lucifora LO, García VB, Menni RC, Escalante AH, Hozbor NM (2009) Effects of body size, age and maturity stage on diet in a large shark: ecological and applied implications. Ecol Res 24:109–118
MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302:199–206
Marshall A, Kyne P, Bennett M (2008) Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller & Henle and Urolophus kapalensis Yearsley & Last): evidence of ontogenetic shifts and possible resource partitioning. J Fish Biol 72:883–898
Morato T, Solà E, Grós MP (2003) Diets of thornback ray (Raja clavata) and tope shark (Galeorhinus galeus) in the bottom longline fishery of the Azores, Northeastern Atlantic. Fish Bull 101:590–602
Mulas A, Bellodi A, Cannas R, Carbonara P, Cau A, Marongiu MF, Pesci P, Porcu C, Follesa MC (2019) Resource partitioning among sympatric elasmobranchs in the central-western Mediterranean continental shelf. Mar Biol 166:1–16
Navia AF, Mejía-Falla PA, López-García J, Giraldo A, Cruz-Escalona VH (2017) How many trophic roles can elasmobranchs play in a marine tropical network? Mar Freshw Res 68:1342–1353
Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin P, O’hara R, Simpson G, Solymos P, Stevens M, Wagner H (2013) Package ‘vegan’. Community ecology pack‐ age, version, 2. Retrieved from https://cran.ism.ac.jp/web/packages/vegan/vegan.pdf
Olin JA, Hussey NE, Grgicak-Mannion A, Fritts MW, Wintner SP, Fisk AT (2013) Variable δ15N diet-tissue discrimination factors among sharks: implications for trophic position, diet and food web models. PLoS One 8:e77567
Ponte DDS, Barcelos LMD, Santos CS, Medeiros J, Barreiros JP (2016) Diet of Dasyatis pastinaca and Myliobatis aquila (Myliobatiformes) from the Azores, NE Atlantic. Cybium 40:209–214
R Core Team (2022) R: A language and environment for statistical computing. Austria, Vienna
Rigby CL, Daley RK, Simpfendorfer CA (2015) Comparison of life histories of two deep-water sharks from eastern Australia: the piked spurdog and the Philippine spurdog. Mar Freshw Res 67:1546–1561
Saglam H, Bascinar NS (2008) Feeding ecology of thornback ray (Raja clavata Linnaeus, 1758) on the Turkish coast of the south-eastern Black Sea. Mar Biol Res 4:451–457
Saglam H, Kutlu S, Aydin I (2010) Diet and feeding strategy of the common stingray Dasyatis pastinaca (Linnaeus, 1758) on the Turkish coast of southeastern Black Sea. Cah Biol Mar 51:37–44
Salazar G (2015) EcolUtils: utilities for community ecology analysis. R package version 0.1. https://github.com/GuillemSalazar/EcolUtils
Saldanha L (2003) Fauna submarina Atlântica: Portugal continental, Açores. Publicações Europa-América, Madeira
Šantić M, Rađa B, Pallaoro A (2012) Diet and feeding strategy of thornback ray Raja clavata. J Fish Biol 81:1070–1084
Santos R, Medeiros-Leal W, Novoa-Pabon A, Crespo O, Pinho M (2021) Biological knowledge of thornback ray (Raja clavata) from the Azores: improving scientific information for the effectiveness of species-specific management measures. Biology 10:676
Santos R, Novoa-Pabon A, Silva H, Pinho M (2020) Elasmobranch species richness, fisheries, abundance and size composition in the Azores archipelago (NE Atlantic). Mar Biol Res 16:103–116
Santos RS, Porteiro FM, Barreiros JP (1997) Marine fishes of the Azores. Annotated checklist and bibliography. A catalogue of the Azorean marine ichthyodiversity. Arquipel Suppl 1:1–242
Serra-Pereira B, Moura T, Griffiths AM, Serrano Gordo L, Figueiredo I (2011) Molecular barcoding of skates (Chondrichthyes: Rajidae) from the southern Northeast Atlantic. Zool Scr 40:76–84
Serrano-Flores F, Torres-Rojas YE, Ajemian MJ, Mendoza-Carranza M, Pérez-Jiménez JC (2021) Advances in the study of the trophic niche of batoids with distribution in Mexican waters. Mar Ecol 42:e12687
Shiffman D, Gallagher A, Boyle M, Hammerschlag-Peyer C, Hammerschlag N (2012) Stable isotope analysis as a tool for elasmobranch conservation research: a primer for non-specialists. Mar Freshw Res 63:635–643
Shipley ON, Matich P (2020) Studying animal niches using bulk stable isotope ratios: an updated synthesis. Oecologia 193:27–51
Shipley ON, Polunin NV, Newman SP, Sweeting CJ, Barker S, Witt MJ, Brooks EJ (2017) Stable isotopes reveal food web dynamics of a data-poor deep-sea island slope community. Food Webs 10:22–25
Stehmann M (2002) Proposal of a maturity stages scale for oviparous and viviparous cartilaginous fishes (Pisces, Chondrichthyes). Arch Fish Mar Res 50:23–40
Stevens J, Bonfil R, Dulvy NK, Walker P (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494
Takeuchi S, Tamaki A (2014) Assessment of benthic disturbance associated with stingray foraging for ghost shrimp by aerial survey over an intertidal sandflat. Cont Shelf Res 84:139–157
Tiralongo F, Messina G, Lombardo BM (2020) Biological Aspects of Juveniles of the Common Stingray, Dasyatis pastinaca (Linnaeus, 1758) (Elasmobranchii, Dasyatidae), from the Central Mediterranean Sea. J Mar Sci Eng 8:269
Torres P, da Cunha RT, Micaelo C, dos Santos RA (2016a) Bioaccumulation of metals and PCBs in Raja clavata. Sci Total Environ 573:1021–1030
Torres P, da Cunha RT, dos Santos RA (2016b) The elasmobranch fisheries of the Azores. Mar Policy 73:108–118
Treloar MA, Laurenson LJ, Stevens JD (2009) Dietary comparisons of six skate species (Rajidae) in south-eastern Australian waters. Environ Biol Fish 80:181–196
Vaudo JJ, Heithaus MR (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Mar Ecol Prog Ser 425:247–260
Wetherbee BM, Cortés E, Bizzarro JJ (2004) Food consumption and feeding habits. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 225–246
White J, Simpfendorfer C, Tobin A, Heupel M (2014) Spatial ecology of shark-like batoids in a large coastal embayment. Environ Biol Fish 97:773–786
White W, Platell M, Potter I (2004) Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for resource partitioning. Mar Biol 144:439–448
Yeldan H, Avsar D, Manasırlı M (2009) Age, growth and feeding of the common stingray (Dasyatis pastinaca, L., 1758) in the Cilician coastal basin, northeastern Mediterranean Sea. J Appl Ichthyol 25:98–102
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All authors contributed to the study conception and design. Material preparation, data collection, and analyses were per Paco Fontaine, João Pedro Barreiros, and Sébastien Jaquemet. The first draft of the manuscript was written by Paco Fontaine and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Fontaine, P., Barreiros, J.P. & Jaquemet, S. Trophic ecology of three sympatric batoid species (Dasyatis pastinaca, Raja clavata, and Raja maderensis) from the Azores, NE Atlantic. Environ Biol Fish 106, 1477–1492 (2023). https://doi.org/10.1007/s10641-023-01412-2
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DOI: https://doi.org/10.1007/s10641-023-01412-2