Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-20T02:28:52.669Z Has data issue: false hasContentIssue false

Feeding habits and trophic level of the shovelnose guitarfish (Pseudobatos productus) in the upper Gulf of California

Published online by Cambridge University Press:  10 July 2017

Fausto Valenzuela-Quiñonez
Affiliation:
CONACYT-Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Calle Av. IPN #195, La Paz, B.C.S. 23060, México
Felipe Galván-Magaña*
Affiliation:
Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas-IPN, Av. IPN s/n, La Paz, B.C.S. 23060, México
David A. Ebert
Affiliation:
Pacific Shark Research Center, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA 95039, USA
E. Alberto Aragón-Noriega
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, Unidad Sonora, Km 2.35 Camino al Tular, Guaymas, Sonora, 85454, México
*
Correspondence should be addressed to: F. Galván-Magaña, Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas-IPN, Av. IPN s/n, La Paz, B.C.S. 23060, México email: fgalvan@ipn.mx

Abstract

The shovelnose guitarfish (Pseudobatos productus) is the most abundant and economically important batoid in Gulf of California fisheries. Despite the importance of the guitarfish in the demersal ecosystem, its trophic relationships are poorly understood. Results from stomach content and stable isotope analysis indicate P. productus is a specialist predator that feeds on coastal benthic organisms, mainly crustaceans, followed by fishes and cephalopods in the Upper Gulf of California. Males and females did not differ in dietary composition and isotopic values. Pseudobatos productus displayed ontogenetic changes in the diet, with smaller, immature individuals having a more specialized diet and mature individuals becoming generalist predators. Size classes I (<570 mm) and II (>570 mm) fed almost exclusively on crustaceans (99.78% and 82.37 %IRI, respectively). Size class III (>832 mm) increased consumption of fishes (22.11 %IRI) and squid (6.54 %IRI). Ontogenetic diet shifts were strongly supported by the SIAR mixing model. Stomach content and stable isotope analyses classify P. productus as a second-order predator.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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

REFERENCES

Abdel-Aziz, S.H., Khalil, A.N. and Abdel-Maguid, S.A. (1993) Reproductive cycle of the common guitarfish, Rhinobatos rhinobatos (Linnaeus, 1758), in Alexandria waters, Mediterranean Sea. Australian Journal of Marine and Freshwater Research 44, 507517.Google Scholar
Altabet, M.A., Pilskaln, C., Thunnell, R., Pride, C., Sigman, D., Chavez, F. and Francois, R. (1999) The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern North Pacific. Deep-Sea Research 46, 655679.Google Scholar
Bizzarro, J.J., Smith, W.D., Hueter, R.E., Tyminski, J., Marquez-Farias, J.F., Castillo-Geniz, J.L., Cailliet, G.M. and Villavicencio-Garayzar, C.J. (2007) The status of shark and ray fishery resources in the Gulf of California: applied research to improve management and conservation. Report to the David and Lucile Packard Foundation. Moss Landing, CA: Moss Landing Marine Laboratories, 237.Google Scholar
Blanco-Parra, M.-d.-P., Galván-Magaña, F., Márquez-Farías, J. and Niño-Torres, C. (2011) Feeding ecology and trophic level of the banded guitarfish, Zapteryx exasperata, inferred from stable isotopes and stomach contents analysis. Environmental Biology of Fishes 95, 6577. doi: 10.1007/s10641-011-9862-7.Google Scholar
Borrell, A., Cardona, L., Kumarran, R.P. and Aguilar, A. (2011) Trophic ecology of elasmobranchs caught off Gujarat, India, as inferred from stable isotopes. ICES Journal of Marine Science: Journal du Conseil 68, 547554. doi: 10.1093/icesjms/fsq170.Google Scholar
Box, A., Deudero, S., Blanco, A., Grau, A.M. and Riera, F. (2010) Differences in δ13C and δ15N stable isotopes in the pearly razorfish Xyrichtys novacula related to the sex, location and spawning period. Journal of Fish Biology 76, 23702381. doi: 10.1111/j.1095-8649.2010.02627.x.Google Scholar
Boyle, M.D., Ebert, D.A. and Cailliet, G.M. (2012) Stable-isotope analysis of a deep-sea benthic-fish assemblage: evidence of an enriched benthic food web. Journal of Fish Biology 80, 14851507. doi: 10.1111/j.1095-8649.2012.03243.x.Google Scholar
Burton, R.K. and Koch, P.L. (1999) Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia 119, 578585.Google Scholar
Capapé, C. and Zaouali, J. (1979) Etude du régime alimentaire de deux sélaciens communs dans le golfe de Gabès (Tunisie): Rhinobatos rhinobatos (Linne, 1758) et Rhinobatos cemiculus (Geoffroy Saint-Hilaire, 1817). Archives de l’ Institut Pasteur de Tunis 56, 285306.Google Scholar
Caut, S., Angulo, E. and Courchamp, F. (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443453.Google Scholar
Colwell, R.K. (2009) EstimateS: Statistical estimation of species richness and shared species from samples. Version 8.2. Available at 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, 726738.Google Scholar
Cortés, E. (1999) Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707717.Google Scholar
Deehr, R.A., Luczkovich, J.J., Hart, K.J., Clough, L.M., Johnson, B.J. and Johnson, J.C. (2014) Using stable isotope analysis to validate effective trophic levels from Ecopath models of areas closed and open to shrimp trawling in Core Sound, NC, USA. Ecological Modelling 282, 117. doi: http://dx.doi.org/10.1016/j.ecolmodel.2014.03.005.Google Scholar
DeNiro, M.J. and Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495506.Google Scholar
DeNiro, M.J. and Epstein, S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341351.Google Scholar
Diaz-Gamboa, R. (2003) Diferenciación entre tursiones Tursiops truncatus costeros y oceánicos en el Golfo de California por medio de isótopos estables de Carbono y Nitrógeno. Tesis Maestría (MSc thesis). Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, 62 pp.Google Scholar
Dodge, K., Logan, J. and Lutcavage, M. (2011) Foraging ecology of leatherback sea turtles in the Western North Atlantic determined through multi-tissue stable isotope analyses. Marine Biology 158, 28132824. doi: 10.1007/s00227-011-1780-x.Google Scholar
Dowton-Hoffman, C. (2007) Biología del pez guitarra Rhinobatos productus (Ayres, 1856), en Baja California Sur, México. PhD thesis, Instituto Politécnico Nacional, Centro Interdiciplinario de Ciencias Marinas, 180 pp.Google Scholar
Drymon, J., Powers, S. and Carmichael, R. (2011) Trophic plasticity in the Atlantic sharpnose shark (Rhizoprionodon terraenovae) from the north central Gulf of Mexico. Environmental Biology of Fishes 95, 2135. doi: 10.1007/s10641-011-9922-z.Google Scholar
Ebert, D.A. and Bizzarro, J.J. (2007) Standardized diet compositions and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei). Environmental Biology of Fishes 80, 221237.Google Scholar
Fischer, W., Krupp, F., Schneider, W., Sommer, C., Carpenter, K.E. and Niem, V.H. (1995) Guía FAO para la Identificación de Especies para los Fines de la Pesca Pacífico Centro-Oriental, 1st edition. Volume 2. Rome: Food and Agriculture Organization.Google Scholar
France, R.L. (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Marine Ecology Progress Series 124, 307312.Google Scholar
Gendron, D., Aguiñiga, S. and Carriquirry, J.D. (2001) δ15N and δ13C in skin biopsy samples: a note of their applicability for examining the relative trophic level in three rorcual species. Journal of Cetacean Research and Management 3, 4144.Google Scholar
Grey, J., Thackeray, S.J., Jones, R.I. and Shine, A. (2002) Ferox trout (Salmo trutta) as “Russian dolls”: complementary gut content and stable isotope analyses of the Loch Ness foodweb. Freshwater Biology 47, 12351243.Google Scholar
Heithaus, M.R., Frid, A., Wirsing, A.J. and Worm, B. (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology and Evolution 23, 202210.Google Scholar
Hussey, N.E., Brush, J., McCarthy, I.D. and Fisk, A.T. (2010) δ15N and δ13C diet–tissue discrimination factors for large sharks under semi-controlled conditions. Comparative Biochemistry and Physiology – Part A: Molecular and Integrative Physiology 155, 445453.Google Scholar
Hussey, N.E., MacNeil, M.A., McMeans, B.C., Olin, J.A., Dudley, S.F.J., Cliff, G., Wintner, S.P., Fennessy, S.T. and Fisk, A.T. (2014) Rescaling the trophic structure of marine food webs. Ecology Letters 17, 239250. doi: 10.1111/ele.12226.Google Scholar
Hussey, N.E., MacNeil, M.A., Olin, J.A., McMeans, B.C., Kinney, M.J., Chapman, D.D. and Fisk, A.T. (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. Journal of Fish Biology 80, 14491484. doi: 10.1111/j.1095-8649.2012.03251.x.Google Scholar
Hyslop, E.J. (1980) Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17, 411429.Google Scholar
Ismen, A., Yigin, C. and Ismen, P. (2007) Age, growth, reproductive biology and feed of the common guitarfish (Rhinobatos rhinobatos Linnaeus, 1758) in Iskenderun Bay, the eastern Mediterranean Sea. Fisheries Research 84, 263269.Google Scholar
Jennings, S., Reñonez, O., Morales-Nin, B., Polunin, N.V.C., Moranta, J. and Coll, J. (1997) Spatial variation in the 15N, and 13C stable isotope composition of plants, invertebrates and fishes on Mediterranean reefs: implications for the study of trophic pathways. Marine Ecology Progress Series 146, 109116.Google Scholar
Kim, S., Casper, D., Galván-Magaña, F., Ochoa-Díaz, R., Hernández-Aguilar, S. and Koch, P. (2011) Carbon and nitrogen discrimination factors for elasmobranch soft tissues based on a long-term controlled feeding study. Environmental Biology Fishes 95, 3752. doi: 10.1007/s10641-011-9919-7.Google Scholar
Labropoulou, M. and Eleftheriou, A. (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. Journal of Fish Biology 50, 324340.Google Scholar
Lucifora, L., García, V., Menni, R., Escalante, A. and Hozbor, N. (2009) Effects of body size, age and maturity stage on diet in a large shark: ecological and applied implications. Ecological Research 24, 109118. doi: 10.1007/s11284-008-0487-z.Google Scholar
Márquez-Farías, F. (2007) Demografía del pez guitarra Rhinobatos productus (Ayres, 1854) del Golfo de California. Tesis Doctorado, Centro de Investigaciones Biológicas del Noroeste, 147 pp.Google Scholar
Márquez-Farías, F.J. (2002) The artisanal ray fishery in the Gulf of California: development, fisheries research, and management issues. IUCN Shark Specialist Group. Shark News, 15.Google Scholar
Minagawa, M. and Wada, E. (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between 15N and animal age. Geochimica et Cosmochimica Acta 45, 341351.Google Scholar
Motta, P.J. and Wilga, C.D. (2001) Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environmental Biology of Fishes 20, 131156.Google Scholar
Navia, A.F., Mejía Falla, P.A. and Giraldo, A. (2007) Feeding ecology of elasmobranch fishes in coastal waters of the Colombian Eastern Tropical Pacific. BMC Ecology 7, 8.Google Scholar
Niño-Torres, C.A., Gallo-Reynoso, J.P., Galván-Magaña, F., Escobar-Briones, E. and Macko, S.A. (2006) Isotopic analysis of delta C-13, delta N-15, and delta S-34 “a feeding tale” in teeth of the longbeaked common dolphin, Delphinus capensis. Marine Mammal Science 22, 831846.Google Scholar
Paré, J.R.J., Bélanger, J.M.R. and Stafford, S.S. (1994) Microwave-assisted process (MAP™): a new tool for the analytical laboratory. TrAC Trends in Analytical Chemistry 13, 176184.Google Scholar
Parnell, A.C., Inger, R., Bearhop, S. and Jackson, A.L. (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5, e9672.Google Scholar
Peterson, B.J. and Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293320.Google Scholar
Phillips, D., Newsome, S. and Gregg, J. (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144, 520527. doi: 10.1007/s00442-004-1816-8.Google Scholar
Pielou, E.C. (1975) Ecological diversity. New York, NY: Wiley.Google Scholar
Pinkas, L. Oliphant, S.M. and Iverson, I.L.K. (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bulletin 152, 105 pp.Google Scholar
Pinnegar, M.J. and Polunin, N.V.C. (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122, 399409.Google Scholar
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703718.Google Scholar
R Core Team (2012) R: a language and environment for statistical computing. Available at http://www.R-project.org/.Google Scholar
Renoe, B.W. (1994) Microwave assisted extraction. American Laboratory 26, 3440.Google Scholar
Reñones, O., Polunin, N.V.C. and Goni, R. (2002) Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis. Journal of Fish Biology 61, 122137.Google Scholar
Sharf, S.F., Juanes, F. and Rountree, R.A. (2000) Predator size – prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Marine Ecology Progress Series 208, 229248. doi: 10.3354/meps208229.Google Scholar
Shibuya, A., de Souza Rosa, R. and Costa Soares, M. (2005) Note in the diet of the guitarfish Rhinobatos percellens (Walbaum 1972) (Elasmobrachii Rhinobatidae) from the coast of Paraíba, Brazil. Acta Biologica Leopoldensia 27, 6364.Google Scholar
Stapp, P. and Polis, G.A. (2003) Marine resources subsidize insular rodent populations in the Gulf of California, Mexico. Oecologia 134, 496504.Google Scholar
Stevens, J.D., Bonfil, R., Dulvy, N.K. and Walker, P.A. (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science: Journal du Conseil 57, 476494. doi: 10.1006/jmsc.2000.0724.Google Scholar
Talent, L.G. (1982) Food habits of the gray smoothhound, Mustelus californicus, the brown smoothhound, Mustelus henlei, the shovelnose guitarfish Rhinobatos productus, and the bat ray Myliobatis californica, in Elkhorn Slough California. California Fish and Game 68, 224234.Google Scholar
Vanderklift, M.A. and Ponsard, S. (2003) Sources of variation in consumer-diet delta N-15 enrichment: a meta-analysis. Oecologia 136, 169182.Google Scholar
Vander Zanden, M.J. and Rasmussen, J.B. (2001) Variation in delta N-15 and delta C-13 trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 20612066.Google Scholar
Vaudo, J.J. and Heithaus, M.R. (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology Progress Series 425, 247260. doi: 10.3354/meps08988.Google Scholar
White, W., Platell, M.E. and Potter, I.C. (2004) Comparisons between the diets of four abundant species of elasmobranchs in subtropical embayment: implications for resource partitioning. Marine Biology 144, 439448.Google Scholar
Wilga, C.D. and Motta, P.J. (1998) Feeding mechanism of the Atlantic guitarfish Rhinobatos lentiginosus: modulation of kinematic and motor activity. Journal of Experimental Biology 201, 31673184.Google Scholar
Supplementary material: File

Valenzuela-Quiñonez supplementary material S1

Supplementary Table

Download Valenzuela-Quiñonez supplementary material S1(File)
File 59.4 KB
Supplementary material: File

Valenzuela-Quiñonez supplementary material S2

Supplementary Table

Download Valenzuela-Quiñonez supplementary material S2(File)
File 56.8 KB
Supplementary material: File

Valenzuela-Quiñonez supplementary material S3

Supplementary Table

Download Valenzuela-Quiñonez supplementary material S3(File)
File 102.4 KB