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Diet composition and feeding habits of the crocodile shark, Pseudocarcharias kamoharai

Abstract

The objective of the present study was to determine the diet composition and feeding habits of the crocodile shark, Pseudocarcharias kamoharai, in Ecuadorian waters, Southeast Pacific Ocean, at a general level, as well as by sex, year, and sexual maturity stage. A total of 401 individuals with their respective stomachs were sampled in the Santa Rosa fishery port, Ecuador; 200 were females and 201 males, with a total length (TL) between 50 to 117 cm and 72.5 to 100 cm, respectively. The number of stomach contents analyzed in this study was sufficient to describe the diet of P. kamoharai, as the asymptote was reached at 100 digestive tracts. A total of 24 prey species were identified, out of which 16 were cephalopods and eight bony fishes. The main identified prey species were the cockeyed squid, Histioteuthis heteropsis, the sharpear enope squid, Ancistrocheirus lesueurii, the purpleback flying squid, Sthenoteuthis oualaniensis, the Jumbo flying squid, Dosidicus gigas, and the neon flying squid, Ommastrephes bartramii. Pseudocarcharias kamoharai was considered a specialist predator that preferred five prey species (Bi = 0.09), and differences were observed by sex, years, and maturity stages. The trophic overlap was high in both females and males ( = 0.98) between the years 2012–2013 and 2017–2018 ( = 0.91), as well as between immature and mature individuals ( = 0.95). The trophic level was Tlk = 4.37, which indicates that this species is a quaternary consumer or a tertiary carnivore.

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References

  • Allan JD, Castillo MM (2007) Stream ecology: structure and function of running waters, 2nd edn. Springer, New York

    Book  Google Scholar 

  • 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 Fishes 95:3–20

    Article  Google Scholar 

  • Buskirk SW, Millspaugh JJ (2006) Metrics for studies of resource selection. J Wildl Manage 70:358–366

    Article  Google Scholar 

  • Calle-Morán MD, Galván-Magaña F (2020) Diet composition and feeding habits of the pelagic thresher shark Alopias pelagicus in Eastern Central Pacific Ocean, Ecuadorian waters. J Mar Biol Assoc UK 100(5):837–845

    Article  Google Scholar 

  • Camhi M, Fowler S, Musick J, Bräutigam A, Fordham S (1998) Sharks and their relatives: ecology and conservation. Occasional Paper of the IUCN Species Survival Commission Occas. Pap. No. 20. IUCN, Oxford

  • Celis-De la Rosa AJ, Labrada Martagón V (2014) Bioestadística. 3° edición. Editorial El Manual Moderno, Ciudad de México

  • Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18(1):117–143

    Article  Google Scholar 

  • Clarke M (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, Oxford

    Google Scholar 

  • Clothier C (1950) A key to some southern California fishes based on vertebral characters. Fishery Bulletin no. 79. Bureau of Marine Fisheries, California

  • Clothier C, Baxter J (1969) Vertebral characters of some Californian fishes with notes on other Eastern Pacific species. The Resources Agency, California

  • Colwell RK (2019): Estatistical estimation of species richness and shared species from samples EstimateS V. 9.1.0 University of Connecticut, Storrs, USA. URL http://viceroy.eeb.uconn.edu/estimates/ Accessed 2 June 2021

  • Conrath CL (2005) Reproductive biology. In: Musick JA. Bonfil R (eds). Management techniques for elasmobranch fisheries. FAO Fisheries Technical Paper. No. 474. FAO, Rome, pp 133–164

  • Córdova-Zavaleta F, Mendo J, Briones-Hernández SA, Acuña-Perales N, González-Pestana A, Alfaro-Shigueto J, Mangel JC (2018) Food habits of the blue shark, Prionace glauca (Linnaeus, 1758), in waters off northern Peru. Fish Bull 116(3–4):310–322

    Article  Google Scholar 

  • 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(3):726–738

    Article  Google Scholar 

  • Cortés E (1999) Standardized diet composition and trophic level in sharks. ICES J Mar Sci 56(5):707–717

    Article  Google Scholar 

  • Cortés E (2000) Life history patterns and correlations in sharks. Rev Fish Sci 8(4):299–344

    Article  Google Scholar 

  • Compagno LJV (2001) Sharks of the world. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). An annotated and illustrated catalogue of the shark species known to date. FAO Species Catalogue for Fisheries Purposes. Vol. 2. No. 1. FAO, Rome

  • Compagno LJV, Dando M, Fowler SL (2005) A field guide to the sharks of the World. Collins, London

    Google Scholar 

  • Dai XK, Zhu JF, Chen XJ, Xu LX, Chen Y (2012) Biological observations on the crocodile shark Pseudocarcharias kamoharai. J Fish Biol 8(5):1207–1212

    Article  Google Scholar 

  • Daniel WW (1991) Bioestadística, base para el análisis de las Ciencias de la Salud. 4 edición. Editorial Limusa, Ciudad de México

  • Ebert DA (2016) Deep–sea cartilaginous fishes of the southeastern Pacific Ocean. FAO Species Catalogue for Fishery Purposes No. 10. FAO, Rome

  • Estupiñán-Montaño C, Cedeño-Figueroa L, Estupiñán-Ortiz JF, Galván-Magaña F, Sandoval-Londoño A, Castañeda-Suárez D, Polo-Silva CJ (2019) Feeding habits and trophic level of the smooth hammerhead shark, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), off Ecuador. J Mar Biol Assoc UK 99(3):673–680

    Article  Google Scholar 

  • FAO (2021) Pseudocarcharias kamoharai (Matsubara, 1936). https://www.fao.org/fishery/en/aqspecies/14647. Accessed 15 February 2021

  • Ferry LA, Cailliet GM (1996) Sample size and data analysis: are we characterizing and comparing diet properly? In: MacKinlay D, Shearer K (eds) Feeding Ecology and Nutrition in Fish, International Congress of the Biology of Fishes. American Fisheries Society, Bethesda, pp 71–80

    Google Scholar 

  • Fischer W, Krupp F, Schneider W, Sommer C, Carpenter K, Niem V (1995) Guía FAO para la identificación de especies para los fines de la pesca. Pacífico centro oriental. Vol. 2–3. Vertebrados. partes 1 y 2. FAO, Roma

  • Froese R, Pauly D (2021) FishBase. www.fishbase.org. version. Accessed 10 April 2021

  • Fujita K (1981) Oviphagous embryos of the pseudocarchariid shark. Pseudocarcharias kamoharai from the central Pacific. Jap J Icthyol 28(1):37–44

  • García-Godos I (2001) Patrones morfológicos del otolito sagitta de algunos peces óseos del mar peruano. Vol. 20 (1–2). Instituto del Mar de Perú (IMARPE), Callao

  • Hammer O (2020) Paleontological statistics, PAST, Version 4.01. University of Oslo, Oslo

  • Hazin FHV, Couto AA, Kihara K, Otsuka K, Ishino M (1990) Distribution and abundance of pelagic sharks in the South-Western Equatorial Atlantic. J Tokyo Univ Fish 77:51–64

    Google Scholar 

  • Hoffman M (1978) The use of Pielou’s method to determine simple size in food studies. In: Fish Food Habits Studies. Proc. 2nd. Pac. NW Technical Workshop. University of Washington, Seattle, pp 56–61

  • Horn HS (1966) Measurement of overlap in comparative ecological studies. Am Nat 100(914):419–424

    Article  Google Scholar 

  • Hyslop E (1980) Stomach contents analysis, a review of methods and their application. J Fish Biol 17(4):411–429

    Article  Google Scholar 

  • Ingrid L, Iverson K, Pinkas L (1971) A pictorial guide to beaks of certain Eastern Pacific cephalopods. Fish Bull 152:7–35

    Google Scholar 

  • Jereb P, Roper CFE (2010) Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Myopsid and Oegopsid Squids. FAO Species Catalogue for Fishery Purposes. Vol. 2, No. 4. FAO, Rome

  • Jereb P, Roper CFE, Norman MD, Finn JK (2014) Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Octopods and Vampire Squids. FAO Species Catalogue for Fishery Purposes. Vol. 3, No. 4. FAO, Rome

  • Jiménez P, Béarez P (2004) Peces marinos del Ecuador continental. Tomo 2. SIMBIOE/NAZCA/IFEA, Quito

  • Jiménez-Valverde A, Hortal J (2003) Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Rev Iber Aracnol 8:151–161

    Google Scholar 

  • Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71

    Article  Google Scholar 

  • Kindong R, Wang H, Wu F, Dai X, Tian S (2020) Age, growth and sexual maturity of the crocodile shark Pseudocarcharias kamoharai from the eastern Atlantic Ocean. Front Mar Sci 7:586024. https://doi.org/10.3389/fmars.2020.586024

    Article  Google Scholar 

  • Krebs CJ (1985) Ecología: estudio de la distribución y la abundancia (2° ed). Editorial Harla, Ciudad de México

  • Kyne PM, Romanov E, Barreto R, Carlson J, Fernando D, Fordham S, Francis MP, Jabado RW, Liu KM, Marshall A, Pacoureau N, Sherley RB (2019) Pseudocarcharias kamoharai. The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2019-1.RLTS.T39337A171964644.en.Accessed3January2021

    Article  Google Scholar 

  • Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. J Fish Biol 50(2):324–340

    Article  Google Scholar 

  • Langton RW (1982) Diet overlap between Atlantic cod, Gadus morhua, silver hake, Merluccius bilinearis, and fifteen other northwest Atlantic finfish. Fish Bull 80(4):745–759

    Google Scholar 

  • Last PR, Stevens JD (1994) Sharks and Rays of Australia. CSIRO, Hobart

    Google Scholar 

  • Lessa R, Andrade HA, De Lima KL, Santana FM (2015) Age and growth of the midwater crocodile shark Pseudocarcharias kamoharai. J Fish Biol 89(1):1–15

    Google Scholar 

  • Loor-Andrade P, Pincay-Espinoza J, Rosas-Luis R (2017) Diet of the blue shark Prionace glauca in the Ecuadorian Pacific Ocean during the years 2013 to 2015. J Appl Ichthyol 33(8):558–562

    Article  Google Scholar 

  • Martin RA (2003) Biology of the crocodile shark. ReefQuest Centre for Shark Research. http://www.elasmo-research.org/education/shark_profiles/pseudocarcharias.htm Accessed 8 December 2021

  • Martínez-Ortiz J, García-Domínguez M (2013) Guía de campo: condrictios del Ecuador. Quimeras, tiburones y rayas. Ministerio de Agricultura, Ganadería, Acuacultura y Pesca (MAGAP). Viceministerio de Acuicultura y Pesca (VMAP)/ Subsecretaría de Recursos Pesqueros (SRP), Manta

  • Matsubara K (1936) A new carcharoid shark found in Japan. Zoological Magazine 48(7):380–382

    Google Scholar 

  • Morisita M (1959) Measuring interspecific association and similarity between communities. Mem Facy Sci Kyushu Univ Ser E Bio 3:65–80

    Google Scholar 

  • Munroe SEM, Simpfendorfer CA, Heupel MR (2014) Defining shark ecological specialisation: concepts, context, and examples. Rev Fish Biol Fisheries 24:317–331

    Article  Google Scholar 

  • Muñoz H (2012) Características de los otolitos sagitales de peces pelágicos pequeños de interés comercial en las costas de Santa Elena, Pacífico ecuatoriano, julio 2011-enero 2012. Dissertation, Universidad Península de Santa Elena

  • Murua H, Santiago J, Coelho R, Zudaire I, Neves C, Rosa D, Zudaire I, Semba Y, Geng Z, Bach P, Arrizabalaga H, Bach P, Baez JC, Ramos ML, Zhu JF, Ruiz J (2018) Updated ecological risk assessment (ERA) for shark species caught in fisheries managed by the Indian Ocean Tuna Commission (IOTC). Conference: 21st Scientific Committee IOTC. IOTC, Seychelles

  • Musick JA (1999) Ecology and conservation of long-lived marine animals. In: Musick JA (ed) Life in the slow lane: ecology and conservation of long-lived marine animals. Am Fish Soc Symp 23 pp 1–10

  • Oliveira P, Hazin FHV, Carvalho F, Rego M, Coelho R, Piercy A, Burgess G (2010) Reproductive biology of the crocodile shark Pseudocarcharias kamoharai. J Fish Biol 76(7):1655–1670

    CAS  Article  Google Scholar 

  • Olson J, Galván-Magaña F (2002) Food habits and consumption rates of dolphinfish (Coryphaena hippurus) in the Eastern Pacific Ocean. Fish Bull 100(2):279–298

    Google Scholar 

  • Pacoureau N, Rigby CL, Kyne PM, Sherley RB, Winker H, Carlson JK, Fordham SV, Barreto R, Fernando D, Francis MP et al (2021) Half a century of global decline in oceanic sharks and rays. Nature 589:567–571

    CAS  Article  Google Scholar 

  • Palomares MLD, Pauly D (2021) SeaLifeBase. www.sealifebase.org. Accessed 5 May 2021

  • Peláez M (1997) Hábitos alimenticios de la cabrilla sardinera Mycteroperca rosacea Streets. (Pisces: Serranidae) en la Bahía de La Paz, BCS y las zonas adyacentes. Dissertation, Universidad Autónoma de Baja California Sur

  • Robertson DR, Allen GR (2015) Peces costeros del Pacífico oriental tropical: sistema de información en línea. Versión 2.0. Instituto Smithsoniano de Investigaciones Tropicales. https://biogeodb.stri.si.edu/sftep/es/pages Accessed 10 March 2020

  • Rosas-Luis R, Loor-Andrade P, Carrera-Fernández M, Pincay-Espinoza JE, Vinces-Ortega C, Chompoy-Salazar L (2015) Cephalopod species in the diet of large pelagic fish (sharks and billfishes) in Ecuadorian waters. Fish Res 173(2):159–168

    Google Scholar 

  • Rosas-Luis R, Pincay-Espinoza JE, Loor-Andrade P, Carrera-Fernández M (2016) Trophic ecology of the shortfin mako Isurus oxyrinchus (Lamniformes: Lamnidae) in the Eastern Pacific Ocean. In: Kovács A, Nagy P (eds) Advances in Marine Biology, vol 1. Nova Science Publishers, New York, pp 147–182

    Google Scholar 

  • Sagar MV, Gop AM, Nair RJ (2018) Stomach content analysis techniques in fishes. In: Nair RJ (ed) Recent advances in fishery biology techniques for biodiversity evaluation and conservation. Indian Agricultural Statistics Research Institute, New Delhi, pp 104–115

  • Saikia SK (2015) Food and feeding of fishes. What do we need to know? Transylv Rev Syst Ecol Res 17(1):71–84

  • Sminkey TR (1995) Musick JA (1995) Age and growth of the sandbar shark, Carcharhinus plumbeus, before and after population depletion. Copeia 4:871–883

    Article  Google Scholar 

  • Sminkey TR, Musick JA (1996) Demographic analysis of the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic. Fish Bull 94(2):341–347

    Google Scholar 

  • Smith P, Zaret M (1982) Bias in estimating niche overlap. Ecology 63(5):1248–1253

    Article  Google Scholar 

  • Subsecretaría de Recursos Pesqueros (2013) Peces pelágicos, grandes y tiburones. MAGAP/. VAP/SRP. http://tiburon.viceministerioap.gob.ec/tiburon-ecuador/estadisticas-globales-por-mes-todos-los-puertos-264.html. Accessed 20 June 2014

  • Stillwell C, Kohler N (1982) Food, feeding habits, and estimates of daily ration of the shortfin mako (Isurus oxyrinchus) in the Northwest Atlantic. Can J Fish Aquat Sci 39(3):407–414

    Article  Google Scholar 

  • Van der Laan R, Fricke R, Eschmeyer WN (2021) Eschmeyer’s catalog of fishes: classification. http://www.calacademy.org/scientists/catalog-of-fishes-classification/. Accessed 4 august 2021

  • Vinueza E (2015) Catálogo de otolitos sagitta de especies comerciales en los cantones de Sucre y San Vicente, Manabí, Pacífico ecuatoriano. Dissertation, Pontificia Universidad Católica del Ecuador Sede Manabí

  • Wetherbee BM, Gruber SH, Cortes E (1990) Diet, feeding habits, digestion and consumption in sharks with special reference to the lemon shark Negaprion brevirostris. In: Pratt HL Jr, Gruber SH, Taniuchi T (eds) Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of the fisheries, NOAA Technical Report NMFS 90, Proceedings of the Second United States-Japan Workshop 9–14 December 1987. U.S. Department of Commerce, Hawaii, pp 29–48

  • White WT (2007) Biological observations on lamnoid sharks (Lamniformes) caught by fisheries in eastern Indonesia. J Mar Biol Assoc UK 87(3):781–788

    Article  Google Scholar 

  • Wolff G (1982) A beak key for eight Eastern Tropical Pacific cephalopod species, with relationship between their beak dimension and size. Fish Bull 80(2):357–370

    Google Scholar 

  • Wolff G (1984) Identification and estimation of size from beaks of eighteen species of cephalopods from the Pacific Ocean. NOAA Technical Report NMFS no. 17. NOAA, USA

  • Wu F, Kindong R, Dai X, Sarr O, Zhu J, Tian S, Li Y, Nsangue BTN (2020) Aspects of the reproductive biology of two pelagic sharks in the eastern Atlantic Ocean. J Fish Biol 97(6):1651–1661

    Article  Google Scholar 

  • Young RE, Vecchione M, Mangold KM (2019) Cephalopoda, Cuvier 1797, octopods, squids, nautiluses. http://tolweb.org/Cephalopoda/19386/2019.03.26. Accessed 5 March 2021

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Acknowledgements

The authors thank the Facultad de Ciencias Naturales of the Universidad de Guayaquil and the Escuela de Biología of the Pontificia Universidad Católica del Ecuador Sede Manabí for the use of their laboratories for the analysis of the samples during this study. Also, we want to thank Ofelia Escobar Sánchez for helping in the construction of the cumulative curve of prey species and for her advice on the trophic ecology of fishes.

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Marcos D. Calle-Morán: conceptualization, methodology, software, validation, formal analysis, investigation, resources, data curation, writing – original draft, writing – review and editing, visualization, supervision; Ana R. Hernández-Téllez: conceptualization, methodology, software, validation, formal analysis, investigation, resources, writing – original draft, writing – review and editing, visualization, supervision; Evelyn R. Tibán-Vivar: conceptualization, methodology, software, validation, formal analysis, investigation, resources, data curation, writing – original draft, writing – review and editing, visualization, supervision; Yari E. Intriago-Vera: conceptualization, methodology, software, validation, formal analysis, investigation, resources, data curation, writing – original draft, writing – review and editing, visualization, supervision; Israel G. Del Valle-Coello: conceptualization, methodology, software, validation, formal analysis, investigation, resources, data curation, writing – original draft, writing – review and editing, visualization, supervision; Beatriz C. Loor-Jama: conceptualization, methodology, software, validation, formal analysis, investigation, resources, data curation, writing – original draft, writing – review and editing, visualization, supervision; Ángel R. Ganchozo-López: conceptualization, methodology, software, validation, formal analysis, investigation, resources, data curation, writing – original draft, writing – review and editing, visualization, supervision.

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Correspondence to Ana R. Hernández-Téllez.

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All experiments have been conducted as per the guidelines of the Institutional Animal Ethics Committee from the Universidad de Guayaquil and Pontificia Universidad Católica del Ecuador Sede Manabí. However, the unregulated shark species used in this study were collected for commercial sale as food. Therefore, the use of this species in research does not require ethical clearance.

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Calle-Morán, M.D., Hernández-Téllez, A.R., Tibán-Vivar, E.R. et al. Diet composition and feeding habits of the crocodile shark, Pseudocarcharias kamoharai. Environ Biol Fish 105, 685–697 (2022). https://doi.org/10.1007/s10641-022-01277-x

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Keywords

  • Width of trophic niche
  • Diet overlap
  • Trophic level
  • Trophic ecology
  • Ecuador