Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-12T19:42:42.317Z Has data issue: false hasContentIssue false
  • English
  • Français

Zeros as a result in diet studies, is this really bad? Rhinoptera steindachneri as a case study

Published online by Cambridge University Press:  20 June 2019

N. R. Ehemann Open the ORCID record for N. R. Ehemann [Opens in a new window] ,
L. A. Abitia-Cardenas Open the ORCID record for L. A. Abitia-Cardenas [Opens in a new window] ,
A. F. Navia ,
P. A. Mejía-Falla  and
V. H. Cruz-Escalona
N. R. Ehemann
Affiliation:
Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Avenida Instituto Politécnico Nacional, s/n, Apartado Postal 592, La Paz, Baja California Sur, 23096, México
L. A. Abitia-Cardenas*
Affiliation:
Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Avenida Instituto Politécnico Nacional, s/n, Apartado Postal 592, La Paz, Baja California Sur, 23096, México
A. F. Navia
Affiliation:
Fundación colombiana para la investigación y conservación de tiburones y rayas, SQUALUS, Cali, Colombia
P. A. Mejía-Falla
Affiliation:
Fundación colombiana para la investigación y conservación de tiburones y rayas, SQUALUS, Cali, Colombia
V. H. Cruz-Escalona
Affiliation:
Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Avenida Instituto Politécnico Nacional, s/n, Apartado Postal 592, La Paz, Baja California Sur, 23096, México
*
Author for correspondence: L. A. Abitia-Cardenas, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Rhinoptera steindachneri is a commercially important, medium-sized, pelagic migratory batoid fish with benthic feeding habits. It has been considered a specialized predator that feeds on molluscs as well as benthic ophiurids and arthropods off the Mexican Pacific coast. Most biological aspects of this species in La Paz Bay are unknown, despite its being a commercially important species of conservation interest. Therefore, the aim of this study was to characterize the feeding habits of R. steindachneri based on specimens caught in artisanal fisheries. The stomach contents of 310 specimens (146 females and 164 males) were analysed, all captured from 2013 to 2015. The vacuity index was 97.1%, and the most important prey species were Mysidium spp. and Cylichna spp. Because of the high frequency of empty stomachs recorded, it was not possible to describe with precision the general diet of the species. Three hypotheses were developed to try to explain why this characteristic occurred in this species, ranging from eating habits to physiology and prey digestion and geographic location of the study. However, considering the mechanical process of prey handling of R. steindachneri, several hypotheses were formulated, with the hour of capture, chemical processes and physiology and prey digestion being the most probable to explain this high vacuity index reported in this study.

Keywords

Batoideielasmobranchsfeedingstomach contentsvacuity index
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 7 , November 2019 , pp. 1661 - 1666
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ajemian, MJ and Powers, SP (2012) Habitat-specific feeding by cownose rays (Rhinoptera bonasus) of the northern Gulf of Mexico. Environmental Biology of Fishes 95, 79–97.Google Scholar
Ajemian, MJ and Powers, SP (2013) Foraging effects of cownose rays (Rhinoptera bonasus) along barrier islands of the northern Gulf of Mexico. Journal of Experimental Marine Biology and Ecology 439, 119–128.Google Scholar
Amariles, DF, Navia, AF and Giraldo, A (2017) Food resource partitioning of the Mustelus lunulatus and Mustelus henlei (Elasmobranchii: Carcharhiniformes). Environmental Biology of Fishes 100, 717–732.Google Scholar
Bade, LM, Balakrishnan, CN, Pilgrim, EM, McRae, SB and Luczkovich, JJ (2014) A genetic technique to identify the diet of cownose rays, Rhinoptera bonasus: analysis of shellfish prey items from North Carolina and Virginia. Environmental Biology of Fishes 97, 999–1012.Google Scholar
Bizzarro, JJ, Robinson, HJ, Rinewalt, CS and Ebert, DA (2007) Comparative feeding ecology of four sympatric skate species off central California, USA. Environmental Biology of Fishes 80, 197–220.Google Scholar
Bizzarro, JJ, Smith, WD, Hueter, RE and Villavicencio-Garayzar, CJ (2009) Activities and catch composition of artisanal elasmobranchs fishing sites on the Eastern Coast of Baja California Sur, Mexico. Bulletin of the Southern California Academy of Sciences 108, 137–151.Google Scholar
Blanco-Parra, MP, Galván-Magaña, F, Márquez-Farías, JF and Niño-Torres, CA (2012) Feeding ecology and trophic level of the banded guitarfish, Zapteryx exasperata, inferred from stable isotopes and stomach contents analysis. Environmental Biology of Fishes 95, 65–77.Google Scholar
Bornatowski, H, De Castro Robert, M and Costa, L (2010) Feeding of guitarfish Rhinobatos percellens (Walbaum, 1972) (Elasmobranchii, Rhinobatidae), the target of artisanal fishery in southern Brazil. Brazilian Journal of Oceanography 58, 45–52.Google Scholar
Bornatowski, H, Wosnick, N, do Carmo, WPD, Corrêa, MFM and Abilhoa, V (2014) Feeding comparisons of four batoids (Elasmobranchii) in coastal waters of southern Brazil. Journal of the Marine Biological Association of the United Kingdom 94, 1491–1499.Google Scholar
Brown, SC, Bizzarro, JJ, Cailliet, GM and Ebert, DA (2012) Breaking with tradition: redefining measures for diet description with a case study of the Aleutian skate Bathyraja aleutica (Gilbert, 1896). Environmental Biology of Fishes 95, 3–20.Google Scholar
Bucking, C (2015) Feeding and digestion in elasmobranchs: tying diet and physiology together. In Shadwick, RE, Farrell, AP and Brauner, CJ (eds), Physiology of Elasmobranch Fishes: Structure and Interaction with Environment. London: Elsevier, pp. 347–394.Google Scholar
Cervantes, HP and Egremy, VA (2013) Variación de la captura del recurso camarón, en relación con la disposición geográfica de los sedimentos en la zona 90 de pesca, Golfo de Tehuantepec, Oaxaca, México. Hidrobiológica 23, 111–123.Google Scholar
Collins, AB, Heupel, MR and Motta, PJ (2007) Residence and movement patterns of cownose rays Rhinoptera bonasus within a south-west Florida estuary. Journal of Fish Biology 71, 1159–1178.Google Scholar
Colwell, RK (2005). EstimateS: Statistical Estimation of Species Richness and Shared Species From Samples. Version 7.5. User's Guide. Storrs University of Connecticut, CT. http://viceroy.eeb.uconn.edu/estimates.Google Scholar
Cortés, E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726–738.Google Scholar
Cortés, E (1999) Standardized diet compositions and trophic levels of sharks. ICESI Journal of Marine Science 56, 707–717.Google Scholar
Cortés, E, Papastamatiou, Y, Carlson, J, Ferry, GL and Wetherbee, B (2008) An overview of the feeding ecology and physiology of elasmobranch fishes. In Cyrino, JEP, Bureau, DP and Kapoor, BG (eds), Feeding and Digestive Functions of Fish. Enfield, NH: Science Publishers, pp. 393–443.Google Scholar
Csilla, A (2011) Encephalization and brain organization of mobulid rays (Myliobatiformes, Elasmobranchii) with ecological perspectives. The Open Anatomy Journal 3, 1–13.Google Scholar
Díaz-Carballido, PL (2011) Hábitos alimenticios de juveniles de la raya tecolote Rhinoptera steindachneri (Evermann y Jenkins, 1892) en el Golfo de Tehuantepec. Bachelor thesis, Universidad del Mar, Puerto Ángel, Oaxaca, México.Google Scholar
Espinoza, M, Clarke, TM, Villalobos-Rojas, F and Wehrtmann, IS (2012) Diet composition and diel feeding behaviour of the banded guitarfish Zapteryx xyster along the Pacific coast of Costa Rica, Central America. Journal of Fish Biology 82, 286–305.Google Scholar
Espinoza, M, Munroe, SEM, Clarke, T, Fisk, AT and Wehrtmann, IS (2015) Feeding ecology of common demersal elasmobranch species in the Pacific coast of Costa Rica inferred from stable isotope and stomach content analyses. Journal of Experimental Marine Biology and Ecology 470, 12–25.Google Scholar
Euzen, O (1987) Food habits and diet composition of some fish of Kuwait. Kuwait Bulletin Science 9, 65–86.Google Scholar
Evermann, BW and Jenkins, OP (1891) Report upon a collection of fishes made at Guaymas, Sonora, Mexico, with descriptions of new species. Proceedings of the United States National Museum 14, 121–164.Google Scholar
Ferry, LA and Cailliet, GM (1996) Sample size sufficiency and data analysis: are we characterizing and comparing diet properly. In MacKinlay, D and Shearer, K (eds) Feeding Ecology and Nutrition in Fish: Proceedings of the Symposium on the Feeding Ecology and Nutrition in Fish. San Francisco, CA: International Congress on the Biology of Fishes, pp. 71–80.Google Scholar
Fisher, RA (2012) Life History, Trophic Ecology and Prey Handling by Cownose Ray, Rhinoptera bonasus, from Chesapeake Bay. Gloucester Point, VA: Virginia Institute of Marine Science-Virginia Sea Grant Report 2010-20, VSG-10-25.Google Scholar
Fisher, RA, Call, GC and Grubbs, RD (2011) Cownose ray (Rhinoptera bonasus) predation relative to bivalve ontogeny. Journal of Shellfish Research 30, 187–196.Google Scholar
Flores-Martínez, IA, Torres-Rojas, YE, Galván-Magaña, F and Ramos-Miranda, J (2016) Diet comparison between silky sharks (Carcharhinus falciformis) and scalloped hammerhead sharks (Sphyrna lewini) off the south-west coast of Mexico. Journal of the Marine Biological Association of the United Kingdom 97, 337–345.Google Scholar
Gilliam, D and Sullivan, KM (1993) Diet and feeding habits of the southern stingray Dasyatis americana in the Central Bahamas. Bulletin of Marine Science 52, 1007–1013.Google Scholar
González-Medina, FJ, Holguín-Quiñones, OE and De la Cruz-Agüero, G (2006) Variación espaciotemporal de algunos macroinvertebrados (Gastropoda, Bivalvia y Echinodermata) de fondos someros del Archipiélago Espíritu Santo, Baja California Sur, México. Ciencias Marinas 32, 33–44.Google Scholar
Guevara-Guillén, C, Shirasago-Germán, B and Pérez-Lezama, EL (2015) The influence of large-scale phenomena on La Paz Bay hydrographic variability. Open Journal of Marine Science 5, 146–157.Google Scholar
Guzmán-Méndez, IA (2009) Estructura de las asociaciones de algunos invertebrados del Archipiélago Espíritu Santo, Baja California Sur, México. Master's thesis, Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, La Paz, Baja California Sur, México.Google Scholar
Heithaus, MR and Vaudo, JJ (2012) Predator–prey interactions. In Carrier, JC, Musick, JA and Heithaus, MR (eds) Biology of Sharks and their Relatives, 2nd Edn. Boca Raton, FL: CRC Press.Google Scholar
Hurtubia, J (1973) Trophic diversity measurement in sympatric predatory species. Ecology 54, 885–890.Google Scholar
Jacobsen, IA and Bennet, MB (2013) A comparative analysis of feeding and trophic level ecology in stingrays (Rajiformes; Myliobatoidei) and electric rays (Rajiformes: Torpedinoidei). PLoS ONE 8, e7148.Google Scholar
James, PS (1962) Observation on shoals of the Javerine cownose ray Rhinoptera javanica Müller and Henle from the Gulf of Mannar, with additional notes on the species. Journal of the Marine Biological Association of India 4, 217–223.Google Scholar
Jiménez-Illescas, ÁR, Obeso Nieblas, M and Salas de León, DA (1997) Oceanografía física de la Bahía de La Paz, B.C.S. In Urbán-Ramírez, J and Ramírez-Rodríguez, M (eds) La Bahía de La Paz, investigación y conservación. La Paz, Baja California Sur, México: Universidad Autónoma de Baja California Sur, Centro Interdisciplinario de Ciencias Marinas and Scripps Institution of Oceanography, pp. 31–41.Google Scholar
Jiménez, PM, Narváez, M, Fernández, J, Allen, T and Villafranca, S (2016) Cambios estacionales y espaciales en la abundancia y composición de moluscos asociados a fondos arenosos de la costa oriental del estado Sucre, Venezuela. Boletín del Instituto Oceanográfico de Venezuela 55, 39–50.Google Scholar
Jones, BC and Geen, GH (1977) Food and feeding of spiny dogfish (Squalus acanthias) in British Columbia waters. Journal of the Fisheries Research Board of Canada 34, 2056–2066.Google Scholar
Kemper, JM, Bizzarro, JJ and Ebert, DA (2017) Dietary variability in two common Alaskan skates (Bathyraja interrupta and Raja rhina). Marine Biology 164, 52.Google Scholar
Kobelkowsky, A (2010) Anatomía comparada del sistema digestivo de las rayas Urotrygon chilensis y Dasyatis sabina (Myliobatiformes). Revista Chilena de Historia Natural 83, 387–394.Google Scholar
Last, P, White, W, Séret, B, de Carvalho, M, Stehmann, M and Naylor, G (2016) Rays of the World. Ithaca, NY: Cornell University Press, 790 pp.Google Scholar
Leigh, SC, Papastamatiou, Y and German, DP (2017) The nutritional physiology of sharks. Reviews in Fish Biology and Fisheries 27, 561–585.Google Scholar
López-García, J, Navia-Lopez, AF and Mejía-Falla, PA (2012) Feeding habits and trophic ecology of Dasyatis longa (Elasmobranchii: Myliobatiformes): sexual, temporal and ontogenetic effects. Journal of Fish Biology 80, 1563–1579.Google Scholar
Macpherson, E, Lleonart, J and Sanchez, P (1989) Gastric emptying in Scyliorhinus canicula (L.): a comparison of surface-dependent and non-surface dependent models. Journal of Fish Biology 35, 37–48.Google Scholar
Marinsek, GP, Viliod, MCDL and Mari, RB (2017) Ecomorphology of the digestive tract of the Brazilian electric ray Narcine brasiliensis (Olfers, 1831) (Torpediniformes: Narcinidae). Acta Zoologica 98, 229–236.Google Scholar
Martínez-Flores, G, Cervantes-Duarte, R and González-Rodríguez, E (2006) Análisis de temperatura superficial del mar en la Bahía de La Paz, Baja California Sur. Naturaleza y Desarrollo 4, 26–34.Google Scholar
Medved, RJ (1985) Gastric evacuation in the sandbar shark, Carcharhinus plumbeus. Journal of Fish Biology 26, 239–253.Google Scholar
Myers, RA, Baum, JK, Shepherd, TD, Powers, SP and Peterson, CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846.Google Scholar
Navarro-González, JA, Bohórquez-Herrera, J, Navia-Lopez, AF and Cruz-Escalona, VH (2012) Diet composition of batoids on the continental shelf off Nayarit and Sinaloa, Mexico. Ciencias Marinas 38, 347–362.Google Scholar
Navia, AF, Mejía, FPA and Giraldo, A (2007) Feeding ecology of elasmobranch fishes in coastal waters of the Colombian Eastern Tropical Pacific. BMC Ecology 7, 8.Google Scholar
Navia, AF, Torres, A, Mejía, FPA and Giraldo, A (2011) Sexual, ontogenetic, temporal and spatial effects on the diet of Urotrygon rogersi (Elasmobranchii: Myliobatiformes). Journal of Fish Biology 78, 1213–1224.Google Scholar
Nelson, GA and Ross, MR (1995) Gastric evacuation in little skate. Journal of Fish Biology 46, 977–986.Google Scholar
Notarbartolo di Sciara, G (1988) Natural history of the rays of the genus Mobula in the Gulf of California. Fishery Bulletin 86, 45–66.Google Scholar
Orth, RJ (1975) Destruction of eelgrass, Zostera marina, by the cownose ray, Rhinoptera bonasus, in the Chesapeake Bay. Chesapeake Science 16, 205–208.Google Scholar
Papastamatiou, YP, Purkis, SJ and Holland, KN (2007) The response of gastric pH and motility to fasting and feeding in free swimming blacktip reef sharks, Carcharhinus melanopterus. Journal of Experimental Marine Biology and Ecology 345, 129–140.Google Scholar
Pollerspöck, J and Straube, N (2018) Bibliography Database of Living/Fossil Sharks, Rays and Chimaeras (Chondrichthyes: Elasmobranchii, Holocephali), Version 01/2018. https://www.shark-references.com.Google Scholar
Poulakis, GR, Urakawa, H, Stevens, PW, DeAngelo, JA, Timmers, AA, Grubbs, RD, Fisk, AT and Olin, JA (2017) Sympatric elasmobranchs and fecal samples provide insight into the trophic ecology of the smalltooth sawfish. Endangered Species Research 32, 491–506.Google Scholar
Ramírez-Rodríguez, M (2014) Hábitos alimenticios de juveniles de la raya Rhinoptera steindachneri (Evermann y Jenkins, 1892), en Nayarit y sur de Sinaloa, México. Bachelor thesis, Universidad Veracruzana, Veracruz, México.Google Scholar
Reguero, M and García, CA (1989) Moluscos de la plataforma continental de Nayarit: Sistemática y ecología (cuatro campañas oceanográficas). Anales del Instituto de Ciencias del Mar y Limnología 54, 1–55.Google Scholar
Sasko, DE, Dean, MN, Motta, PJ and Hueter, RE (2006) Prey capture behavior and kinematics of the Atlantic cownose ray, Rhinoptera bonasus. Zoology (Jena) 109, 171–181.Google Scholar
Schluessel, V, Bennet, MB and Collin, SP (2010) Diet and reproduction in the white-spotted eagle ray Aetobatus narinari from Queensland, Australia and the Penghu Islands, Taiwan. Marine and Freshwater Research 61, 1278–1289.Google Scholar
Simental-Anguiano, MR (2011) Dieta de Rhinoptera steindachneri (Evermann y Jenkins, 1892) y Dasyatis brevis (Garman, 1879) en el Alto Golfo De California. Bachelor thesis, Universidad Autónoma de Baja Califronia Sur, La Paz, Baja California Sur, México.Google Scholar
Smith, JW and Merriner, JV (1985) Food habits and feeding behavior of the cownose ray, Rhinoptera bonasus, in lower Chesapeake Bay. Estuaries 8, 305–310.Google Scholar
Urcádiz-Cázares, FJ, Cruz-Escalona, VH, Nava-Sánchez, EH and Ortega-Rubio, A (2017) Clasificación de unidades del fondo marino a partir de la distribución espacial de los sedimentos superficiales de la Bahía de La Paz, Golfo de California. Hidrobiológica 27, 399–409.Google Scholar
Valinassab, T, Jalali, S, Hafezieh, M and Zarshenas, GA (2011) Evaluation of some feeding indices of Pomadasys kaakan in the Northern Persian Gulf. Iranian Journal of Fisheries Sciences 10, 497–504.Google Scholar
Viana, AF, Valentin, JL and Vianna, M (2017) Feeding ecology of elasmobranch species in southeastern Brazil. Neotropical Ichthyology 15, e160176.Google Scholar
Weigmann, S (2016). Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. Journal of Fish Biology 88, 837–1037.Google Scholar
Weiner, J (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends in Ecology and Evolution 7, 384–388.Google Scholar
Wetherbee, BM, Gruber, SH and Ramsey, AL (1987) X-radiographic observations of food passage through digestive tracts of lemon sharks. Transactions of the American Fisheries Society 116, 763–767.Google Scholar
Wetherbee, BM, Cortés, E and Bizarro, JJ (2012) Food consumption and feeding habits. In Carrier, JF, Musick, JA and Heithaus, M (eds) Biology of Sharks and their Relatives. Boca Raton, FL: CRC Press, pp. 239–264.Google Scholar
Windell, JT (1967) Rates of digestion in fishes. In Gerking, SD (ed.) The Biological Basis of Freshwater Fish Production. New York, NY: John Wiley and Sons, pp. 151–173.Google Scholar
Yemışken, E, Forero, MG, Megalofonou, P, Eryilmaz, L and Navarro, J (2018) Feeding habits of three batoids in the Levantine Sea (north-eastern Mediterranean Sea) based on stomach content and isotopic data. Journal of the Marine Biological Association of the United Kingdom 98, 89–96.Google Scholar