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Environmental Biology of Fishes

, Volume 100, Issue 6, pp 717–732 | Cite as

Food resource partitioning of the Mustelus lunulatus and Mustelus henlei (Elasmobranchii: Carcharhiniformes)

  • Diego F. Amariles
  • Andrés F. NaviaEmail author
  • Alan Giraldo
Article

Abstract

The feeding habits and trophic ecology of Mustelus lunulatus and Mustelus henlei in the central coast of the Colombian Pacific were evaluated and compared to determine whether there was trophic niche overlap or resource partitioning between these two sympatric shark species. A total of 59 prey items were identified and grouped into 10 taxonomic categories. Mustelus lunulatus fed in large proportion on Stomatopoda and Brachyura, whereas M. henlei fed almost exclusively on Teleostei. Dendrobranchiata, Cephalopoda, Anomura and Polychaeta complemented the diets of both species. There were significant differences in diet between the two species, and there was an ontogenetic diet shift in Mustelus lunulatus, with Stomatopoda being the main prey item of juveniles and Brachyura the main prey item of adults. Dietary overlap (by sex and size) was low between species, but it was high for each species, with significant overlap between juveniles and adults of M. lunulatus and M. henlei, and between males and females of M. henlei. There were differences in the trophic levels of the species, sexes and sizes. This study suggests there is food resource partitioning, and differing ecological function of the two Mustelus species in the food web of the study area.

Keywords

Diet Trophic niche Dietary overlap Resource partitioning Coexistence 

Notes

Acknowledgements

To biologist J. López, M.A. Orozco and E. Galindo for their assistance conducting field and laboratory work. To fishermens of Pueblo Nuevo in Buenaventura city, for their help in obtaining samples. This study was partially funded by Conservación Internacional and Colciencias-Universidad del Valle (code: 1106-452-21080, contract: 429 RC-258-2008).

References

  1. Amundsen PA, Gabler HM, Staldvik FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data modification of the Costello (1990) method. J Fish Biol 48:607–614. doi: 10.1111/j.1095-8649.1996.tb01455.x Google Scholar
  2. Bellegia M, Figueroa D, Sanchez F, Bremec C (2012) The feeding ecology of Mustelus schmitti in the southwestern Atlantic: geographic variations and dietary shifts. Environ Biol Fish 95:99–114. doi: 10.1007/s10641-0119874-3 CrossRefGoogle Scholar
  3. Bethea DM, Buckel JA, Carlson JK (2004) Foraging ecology of the early life stages of four sympatric shark species. Mar Ecol Prog Ser 268:245–264. doi: 10.3354/meps268245 CrossRefGoogle Scholar
  4. Bethea DM, Hale L, Carlson JK, Cortés E, Manire CA, Gelsleichter J (2007) Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Mar Biol 152:1009. doi: 10.1007/s00227-007-0728-7 CrossRefGoogle Scholar
  5. Bizarro JJ, Robinson HJ, Rinewalt CS, Ebert DA (2007) Comparative feeding ecology of four sympatric skate species off central California USA. Environ Biol Fish 80:197–220. doi: 10.1007/s10641-007-9241-6 CrossRefGoogle Scholar
  6. Brown SC, Bizarro 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. doi: 10.1007/s10641-011-9959-z Google Scholar
  7. Browning NE, Cockcroft VG, Worthy GAJ (2014) Resource partitioning among South African delphinids. J Exp Mar Biol Ecol 457:15–21. doi: 10.1016/j.jembe.2014.03.016 CrossRefGoogle Scholar
  8. Chiaramonte GE, Pettovello AD (2000) The biology of Mustelus schmitti in southern Patagonia, Argentina. J Fish Biol 57:930–942. doi: 10.1111/j.1095-8649.2000.tb02202.x CrossRefGoogle Scholar
  9. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
  10. Clarke KR, Gorley RN (2006) PRIMER v6: user manual ⁄ tutorial. Primer-E Ltd, PlymouthGoogle Scholar
  11. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E Ltd, PlymouthGoogle Scholar
  12. Clarke M, Clarke D, Martins H, Silva H (1996) The diet of the blue shark (Prionace glauca L.) in Azorean waters. Arquipel Life Mar Sci 14A:41–56Google Scholar
  13. Cortés E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can J Fish Aquat Sci 54:726–738. doi: 10.1139/f96-316 CrossRefGoogle Scholar
  14. Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717. doi: 10.1006/jmsc.1999.0489 CrossRefGoogle Scholar
  15. Costello MJ (1990) Predator feeding strategy and prey importance: a new graphical analysis. J Fish Biol 36:261–263CrossRefGoogle Scholar
  16. Doherty PJ, Williams DMB (1988) The replenishment of coral reef fish populations. Oceanogr Mar Biol 26:487–551Google Scholar
  17. Espinoza M, Clarke TM, Villalobos-Rojas F, Wehrtmann IS (2012) Ontogenetic dietary shifts and feeding ecology of the rasptail skate Raja velezi and the brown smoothhound shark Mustelus henlei, along the Pacific coast of Costa Rica, central America. J Fish Biol 82:286–305Google Scholar
  18. Filiz H (2009) Diet composition of smooth-hound, Mustelus mustelus (Linnaeus, 1758), in Aegean Sea, Turkey. Bel J Zool 139:81–84Google Scholar
  19. Gelsleichter J, Musick JA, Nichols S (1999) Food habits of the smooth dogfish, Mustelus canis, dusky shark, Carcharhinus obscurus, Atlantic sharpnose shark, Rhizoprionodon terraenovae, and the sand tiger, Carcharias taurus, from the northwest Atlantic Ocean. Environ Biol Fish S4:205–217CrossRefGoogle Scholar
  20. Gill T (1863) On the classification of the families and genera of the Squali of California. Proc Acad Natl Sci Phila 14:483–501Google Scholar
  21. Gómez G, Zapata L, Franke R, Ramos GE (2003) Hábitos Alimentarios de Mustelus lunulatus y M. henlei (Pisces: Triakidae) colectados en el parque nacional natural Gorgona, Pacífico colombiano. Bol Invest Mar Cost 32:219–229Google Scholar
  22. Gotelli NJ, Entsminger GL (2004) EcoSim. Null model software for ecology Version 7.0. Acquid Intelligence Inc. and Kesey Bear. Jericho, VT 05465 Available at http://garyentsminger.com/ecosim/index.htm
  23. Gotelli NJ, Graves GR (1996) Null models in ecology. Smithsonian Institution Press, Washington D.CGoogle Scholar
  24. Guzmán-Alvis A, Solano OD (2002) Estado de los fondos blandos de la plataforma continental. In: Ospina-Salazar GH, Acero A (eds) Informe del estado de los ambientes marinos y costeros en Colombia: 2001. INVEMAR, Santa Marta, pp 71–75Google Scholar
  25. Haeseker SL, Cech JJ Jr (1993) Food habits of the brown smoothhound shark (Mustelus henlei) from two sites in Tomales Bay. Calif Fish Game 79:89–95Google Scholar
  26. Hori M (1987) Mutualism and commensalism in a fish community in Lake Tanganyika. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in the biotic communities. University of Tokyo Press, Tokio, pp 219–239Google Scholar
  27. Hyslop EJ (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429. doi: 10.1111/j.1095-8649.1980.tb02775.x CrossRefGoogle Scholar
  28. Jacobsen IP, Bennett MB (2011) Feeding ecology and dietary comparisons among three sympatric Neotrygon (Myliobatoidei: Dasyatidae) species. J Fish Biol 80:1–15. doi: 10.1111/j.1095-8649.2011.03169.x Google Scholar
  29. Jardas I, Santic M, Nerlovic V, Pallaoro A (2007) Diet composition of blackspotted smooth-hound, Mustelus punctulatus (Risso, 1826), in the eastern Adriatic Sea. J Appl Ichthyol 23:279–281. doi: 10.1111/j.1439-0426.2006.00826.x CrossRefGoogle Scholar
  30. Jordan DS, Gilbert CH (1882) Description of four new species of sharks, from Mazatlan, México. Proc US Natl Mus 5:102–110. doi: 10.5479/si.00963801.5-268.102 CrossRefGoogle Scholar
  31. Kamler JF, Stenkewitz U, Klare U, Jacobsen NF, Macdonald DW (2012) Resource partitioning among cape foxes, bat-eared foxes, and black-backed jackals in South Africa. J Wildl Manag 76:1241–1253. doi: 10.1002/jwmg.354 CrossRefGoogle Scholar
  32. Kamura S, Hashimoto H (2004) The food habits of four species of triakid sharks, Triakis scyllium, Hemitriakis japanica, Mustelus griseus and Mustelus manazo, in the central Seto Inland Sea. Japan. Fish Sci 70:1019–1035. doi: 10.1111/j.1444-2906.2004.00902.x CrossRefGoogle Scholar
  33. Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ Biol Fish 18:27–40. doi: 10.1007/BF00002325 CrossRefGoogle Scholar
  34. Krebs CJ (1999) Ecologycal methodology, 2nd edn. Addison Wesley Longman, Inc., Menlo ParkGoogle Scholar
  35. Lévêque C (1997) Biodiversity dynamics and conservation: the freshwater fish of tropical Africa. Cambridge University Press, CambridgeGoogle Scholar
  36. Lipej L, Mavric B, Resek S, Cherif M, Capapé C (2011) Food and feeding habits of the blackspotted smooth-hound, Mustelus punctulatus (Elasmobranchii: Carchariniformes: Triakidae), from the northern Adriatic. Acta Ichthyol Piscat 41:171–177CrossRefGoogle Scholar
  37. Lucifora LO, García VB, Menni RC, Escalante AH (2006) Food habits, selectivity, and foraging modes of the school shark Galeorhinus galeus. Mar Ecol Prog Ser 315:259–270CrossRefGoogle Scholar
  38. Marshall AD, Kyne PM, Bennett MB (2008) Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Müller and Henle and Urolophus kapalensis Yearsley and last): evidence of ontogenetic shifts and possible resource partitioning. J Fish Biol 72:883–898. doi: 10.1111/j.1095-8649.2007.01762.x CrossRefGoogle Scholar
  39. Mejía-Falla PA, Navia AF (2011) Estadísticas pesqueras de tiburones y rayas en el Pacífico colombiano. Technical document Fundación SQUALUS No. FS0111Google Scholar
  40. Molina JM, López A (2011) Trophic ecology of Mustelus schmitti (Springer, 1939) in a nursery area of northern Patagonia. J Sea Res 65:381–389. doi: 10.1016/j.seares.2011.03.001 CrossRefGoogle Scholar
  41. Moreno-Sánchez XG, Escobar-Sánchez O, Abitia-Cárdenas LA, Cruz-Escalona VH (2012) Diet composition of the sicklefin smooth-hound shark Mustelus lunulatus caught off El Pardito Island, Baja California Sur, México. Mar Biodiversity Rec 5:1–5. doi: 10.1017/S1755267212000504 CrossRefGoogle Scholar
  42. Navia AF, Caldas JP (2011) Familia Triakidae. In: Mejía-Falla PA, Navia AF, Puentes V (eds) Guía para la identificación de especies de tiburones, rayas y quimeras de Colombia. Ministerio de medio ambiente y desarrollo sostenible, Corporación para el desarrollo sostenible del archipiélago de San Andrés, Providencia y Santa Catalina-Coralina. Gobernación de San Andrés, Providencia y Santa Catalina, Fundación SQUALUS, Bogotá D.C., pp. 104–117Google Scholar
  43. Navia AF, Giraldo A, Mejía-Falla PA (2006) Notas sobre la biología y dieta del tollo vieja (Mustelus lunulatus) en la zona central de pesca del Pacífico colombiano. Rev Investig Mar 34:217–222Google Scholar
  44. Navia AF, Mejía-Falla PA, Giraldo A (2007) Feeding ecology of elasmobranch fishes in coastal waters of the Colombian Eastern Tropical Pacific. BMC Ecol 7:1–10. doi: 10.1186/1472-6785-7-8 CrossRefGoogle Scholar
  45. Navia AF, Cortés E, Mejía-Falla PA (2010) Topological analysis of the ecological importance of elasmobranch fishes: a food web study on the Gulf of Tortugas, Colombia. Ecol Model 221:2918–2926. doi: 10.1016/j.ecolmodel.2010.09.006 CrossRefGoogle Scholar
  46. Navia AF, Cortés E, Jordán F, Cruz-Escalona VH, Mejía-Falla PA (2012) Changes to marine trophic networks caused by fishing. In: Mahamane A (ed) Diversity of ecosystems. InTeO, pp. 417–452. Available at: http://www.intechopen.com/books/diversity-of-ecosystems/ changes-to-marine-food-webs-caused-by-fishing
  47. Navia AF, Mejía-Falla PA, López-García J, Giraldo A, Cruz VH (2016) How many roles can play elasmobranchs in a tropical network. Mar Freshwater Res 38:1–12. doi: 10.1071/MF16161
  48. O’shea OR, Thums M, van Keulen M, Kempste RM, Meekan MG (2013) Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. J Fish Biol 82:1805–1820. doi: 10.1111/jfb.12104 CrossRefPubMedGoogle Scholar
  49. Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL (2006) Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 320:239–251. doi: 10.3354/meps320239 CrossRefGoogle Scholar
  50. Pinkas L, Oliphant MS, Iverson LR (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bull 152:1–105Google Scholar
  51. Platell ME, Potter IC (2001) Partitioning of food resources amongst 18 abundant benthic carnivorous fish species in marine waters on the lower west coast of Australia. J Exp Mar Biol Ecol 261:31–54CrossRefPubMedGoogle Scholar
  52. Platell ME, Potter IC, Clarke KR (1998) Resource partitioning by four species of elasmobranchs (Batoidea: Urolophidae) in coastal waters of temperate Australia. Mar Biol 131:719–734CrossRefGoogle Scholar
  53. Plumlee JD, Wells RJ (2016) Feeding ecology of three coastal shark species in the northwest Gulf of Mexico. Mar Ecol Prog Ser 550:163–174CrossRefGoogle Scholar
  54. Prahl HV, Cantera JR, Contreras R (1990) Maglares y hombres del pacífico colombiano. FEN, ColombiaGoogle Scholar
  55. Robertson DR, Allen G (2002) (CD ROM) Peces Costeros del Pacífico Oriental Tropical: Un sistema de información, Instituto Smithsonian de Investigaciones Tropicales, Balboa, República de PanamáGoogle Scholar
  56. Rodríguez-Romero J, Álvarez-Bauman E, Ochoa-Díaz MR, López-Martínez J, Maldonado-García M (2013) Feeding habits of Mustelus henlei on the western coast of Baja California Sur, México. Rev Biol Mar Oceanogr 48:261–271CrossRefGoogle Scholar
  57. Rojas P (2000) Contribución al conocimiento biológico de Mustelus lunulatus un recurso pesquero potencial en el Pacífico Colombiano. Thesis presented as requirements for the degree of Bachelor in Biology, Facultad de Ciencias, Departamento de Biología, Universidad del Valle, Cali, ColombiaGoogle Scholar
  58. Root RB (1967) The niche exploitation pattern of the blue-gray gnatcatcher. Ecol Soc Am 37:317–350Google Scholar
  59. Ross ST (1986) Resource partitioning in fish assemblage: a review of field studies. Copeia 1986:352–388CrossRefGoogle Scholar
  60. Russo RA (1975) Observations on the food habits of leopard sharks (Triakis semifasciata) and brown smoothhounds (Mustelus henlei). Calif Fish Game 61:95–103Google Scholar
  61. Saidi B, Bradai MN, Bouaın A (2009a) Reproductive biology and diet of Mustelus punctulatus (Risso, 1826) (Chondrichthyes: Triakidae) from the Gulf of Gabes, central Mediterranean Sea. Sci Mar 73:249–258. doi: 10.3989/scimar.2009.73n2249 CrossRefGoogle Scholar
  62. Saıdi B, Enajjar S, Bradaı MN, Bouaın A (2009b) Diet composition of smooth-hound shark, Mustelus mustelus (Linnaeus, 1758), in the Gulf of Gabe, southern Tunisia. J Appl Ichthyol 25:113–118CrossRefGoogle Scholar
  63. Sale PF (1980) The ecology of fishes on coral reefs. Oceanogr Mar Biol 18:367–421Google Scholar
  64. Scharf FS, Juanes F, Rountree RA (2000) Predator size - prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248. doi: 10.3354/meps208229 CrossRefGoogle Scholar
  65. Schoener TW (1970) Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51:408–418CrossRefGoogle Scholar
  66. Schoener TW (1974) The compression hypothesis and temporal resource partitioning. Proc Natl Acad Sci U S A 71:4169–4172CrossRefPubMedPubMedCentralGoogle Scholar
  67. Schückel S, Sell A, Kröncke I, Reiss H (2011) Diet composition and resource partitioning in two small flatfish species in the German Bight. J Sea Res 66:195–204. doi: 10.1016/j.seares.2011.06.003 CrossRefGoogle Scholar
  68. Sibbing FA, Nagelkerke LAJ, Stet RJM, Osse JWM (1998) Speciation of endemic Lake Tana barbs (Cyprinidae, Ethiopia) driven by trophic resource partitioning; a molecular and ecomorphological approach. Aquat Ecol 32:217–227CrossRefGoogle Scholar
  69. Smale MJ, Compagno LJ (1997) Life history and diet of two southern African smoothhound sharks, Mustelus mustelus (Linnaeus, 1758) and Mustelus palumbes Smith, 1957 (Pisces: Triakidae). S Afr J Mar Sci 18:229–248CrossRefGoogle Scholar
  70. Sommerville E, Platell ME, White WT, Jones AA, Potter IC (2011) Partitioning of food resources by four abundant, co-occurring elasmobranch species: relationships between diet and both body size and season. Mar Freshw Res 62:54–65. doi: 10.1071/MF10164 CrossRefGoogle Scholar
  71. Springer S (1967) Social organization of shark populations. In: Gilbert PW, Mathewson RF, Rail DP (eds) Sharks, Skates and Rays. Johns Hopkins Press, Baltimore, pp 149–174Google Scholar
  72. Stevens JD (2010) Epipelagic oceanic elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II: Biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 3–35CrossRefGoogle Scholar
  73. Talent LG (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. Calif Fish Game 68:224–234Google Scholar
  74. Valls M, Quetglas A, Ordines F, Moranta J (2011) Feeding ecology of demersal elasmobranchs from the shelf and slope off the Balearic Sea (western Mediterranean). Sci Mar 75:633–639CrossRefGoogle Scholar
  75. Wearmouth VJ, Sims DW (2008) Sexual segregation of marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. Adv Mar Biol 54:107–170. doi: 10.1016/S0065-2881(08)00002-3 CrossRefPubMedGoogle Scholar
  76. Wetherbee BM, Cortés E (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 223–244Google Scholar
  77. Wetherbee BM, Cortés E (2012) Food consumption and feeding habits. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 229–264Google Scholar
  78. White WT, Potter IC (2004) Habitat partitioning among four elasmobranch species in nearshore, shallow waters of a subtropical embayment in Western Australia. Mar Biol 145:1023–1032. doi: 10.1007/s00227-004-1386-7 CrossRefGoogle Scholar
  79. White WT, Platell ME, Potter IC (2004) Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for resource partitioning. Mar Biol 144:439–448CrossRefGoogle Scholar
  80. Yamaguchi A, Taniuchi T (2000) Food variations and ontogenetic dietary shift of the starspotted-dogfish Mustelus manazo at five locations in Japan and Taiwan. Fish Sci 66:1039–1048CrossRefGoogle Scholar
  81. Yick JL, Tracey SR, White WG (2011) Niche overlap and trophic resource partitioning of two sympatric batoids co-inhabiting an estuarine system in southeast Australia. J Appl Ichthyol 27:1272–1277. doi: 10.1111/j.1439-0426.2011.01819.x CrossRefGoogle Scholar
  82. Yick JL, Barnett A, Tracey SR (2012) The trophic ecology of two abundant mesopredators in south-east coastal waters of Tasmania, Australia. Mar Biol 159:1183–1196. doi: 10.1007/s00227-012-1899-4 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Diego F. Amariles
    • 1
    • 2
  • Andrés F. Navia
    • 2
    • 3
    Email author
  • Alan Giraldo
    • 3
  1. 1.Departamento de BiologíaUniversidad del ValleCaliColombia
  2. 2.Fundación Colombiana para la Investigación y Conservación de Tiburones y Rayas, SQUALUSCaliColombia
  3. 3.Grupo de Investigación en Ecología Animal, Sección de Zoología, Departamento de BiologíaUniversidad del ValleCaliColombia

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