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Effects of body size, age and maturity stage on diet in a large shark: ecological and applied implications

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Ecological Research

Abstract

Ontogenetic diet shifts are a widespread phenomenon among vertebrates, although their relationships with life history traits are poorly known. We analyzed the relative importance of body size, age and maturity stage as determinants of the diet of a marine top predator, the copper shark, Carcharhinus brachyurus, by examining stomach contents using a multiple-hypothesis modeling approach. Copper sharks shifted their diet as size and age increased and as they became sexually mature, incorporated larger prey as they grew, and had a discrete shift in diet with body size, with only individuals larger than ≈200 cm total length able to prey on chondrichthyans. Body size was the most important trait explaining the consumption of chondrichthyans, while age determined the consumption of pelagic teleosts. Pelagic teleosts were consumed mostly by medium-aged sharks, a result, probably, of a risk-reducing feeding strategy at young ages coupled with either a senescence-related decline in performance or a change in sensory capabilities as sharks age. Copper sharks of all sizes were able to cut prey in pieces, implying that gape limitation (i.e., the impossibility of eating prey larger than a predator’s mouth) did not play a role in producing the diet shift. Our results suggest that, contrary to the current practice of setting minimum but not maximum size limits in catches, any plan to conserve or restore the ecological function of sharks, through their predatory control of large prey, should aim to maintain the largest individuals.

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References

  • Acevedo-Gutiérrez A (2002) Interactions between marine predators: dolphin food intake is related to the number of sharks. Mar Ecol Prog Ser 240:267–271

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46

    Article  Google Scholar 

  • Arim M, Bozinovic F, Marquet PA (2007) On the relationship between trophic position, body mass and temperature: reformulating the energy limitation hypothesis. Oikos 116:1524–1530

    Article  Google Scholar 

  • Arnold SJ (1993) Foraging theory and prey-size relations in snakes. In: Seigel RA, Collins JT (eds) Snakes: ecology and behaviour. McGraw-Hill, New York, pp 87–116

    Google Scholar 

  • Bascompte J, Melián CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Nat Acad Sci USA 102:5443–5447

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bishop SDH, Francis MP, Duffy C, Montgomery JC (2006) Age, growth, maturity, longevity and natural mortality of the shortfin mako shark (Isurus oxyrinchus) in New Zealand waters. Mar Freshw Res 57:143–154

    Article  Google Scholar 

  • Bjorndal KA (1997) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 199–231

    Google Scholar 

  • Carlson JK, Baremore IE (2003) Changes in biological parameters of Atlantic sharpnose shark Rhizoprionodon terraenovae in the Gulf of Mexico: evidence for density-dependent growth and maturity? Mar Freshw Res 54:227–234

    Article  Google Scholar 

  • Chapman DD, Gruber SH (2002) A further observation of the prey-handling behavior of the great hammerhead shark, Sphyrna mokarran: predation upon the spotted eagle ray, Aetobatus narinari. Bull Mar Sci 70:947–952

    Google Scholar 

  • Chiaramonte GE (1998) Shark fisheries in Argentina. Mar Freshw Res 49:601–609

    Article  Google Scholar 

  • Chiaramonte GE, Pettovello AD (2000) The biology of Mustelus schmitti in southern Patagonia, Argentina. J Fish Biol 57:930–942

    Article  Google Scholar 

  • Cliff G, Dudley SFJ (1991) Sharks caught in the protective gill nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes. S Afr J Mar Sci 10:253–270

    Google Scholar 

  • Cliff G, Dudley SFJ (1992) Sharks caught in the protective gill nets off Natal, South Africa. 6. The copper shark Carcharhinus brachyurus (Günther). S Afr J Mar Sci 12:663–674

    Google Scholar 

  • Cooper AB, Pettorelli N, Durant SM (2007) Large carnivore menus: factors affecting hunting decisions by cheetahs in the Serengeti. Anim Behav 73:651–659

    Article  Google Scholar 

  • Cortés E (1998) Demographic analysis as an aid in shark stock assessment and management. Fish Res 39:199–208

    Article  Google Scholar 

  • Cousseau MB, Perrotta RG (2000) Peces marinos de Argentina. Biología, distribución, pesca. Instituto Nacional de Investigación y Desarrollo Pesquero, Mar del Plata

  • Compagno L, Dando M, Fowler S (2005) A field guide to the sharks of the world. Harper Collins, London

    Google Scholar 

  • Crawley MJ (2005) Statistics: an introduction using R. Wiley, Chichester

    Google Scholar 

  • de Roos AM, Boukal DS, Persson L (2006) Evolutionary regime shifts in age and size at maturation of exploited fish stocks. Proc R Soc B 273:1876–1880

    Google Scholar 

  • Ebert DA (2002) Ontogenetic changes in the diet of the sevengill shark (Notorynchus cepedianus). Mar Freshw Res 53:517–523

    Article  Google Scholar 

  • Engen S, Stenseth NC (1989) Age-specific optimal diets and optimal foraging tactics: a life-history approach. Theor Pop Biol 36:281–295

    Article  CAS  Google Scholar 

  • Fishelson L, Montgomery LW, Myrberg AH Jr (1987) Biology of surgeonfish Acanthurus nigrofuscus with emphasis on changeover in diet and annual gonadal cycles. Mar Ecol Prog Ser 39:37–47

    Article  Google Scholar 

  • Forsman A (1991) Variation in sexual size dimorphism and maximum body size among adder populations: effects of prey size. J Anim Ecol 60:253–267

    Article  Google Scholar 

  • Franklin AB, Shenk TM, Anderson DR, Burnham KP (2001) Statistical model selection: an alternative to null hypothesis testing. In: Shenk TM, Franklin AB (eds) Modeling in natural resource management: development, interpretation, and application. Island Press, Washington, pp 75–90

    Google Scholar 

  • Frid A, Baker GG, Dill LM (2008) Do shark declines create fear-related systems? Oikos 117:191–201

    Article  Google Scholar 

  • Hairston NG Jr, Hairston NG Sr, (1993) Cause-effect relationships in energy flow, trophic structure, and interspecific interactions. Am Nat 142:379–411

    Article  Google Scholar 

  • Heithaus MR (2004) Predator-prey interactions. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 487–521

    Google Scholar 

  • Heithaus MR (2005) Habitat use and group size of pied cormorants (Phalacrocorax varius) in a seagrass ecosystem: possible effects of food abundance and predation risk. Mar Biol 147:27–35

    Article  Google Scholar 

  • Heithaus MR, Dill LM (2002) Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology 83:480–491

    Google Scholar 

  • Heithaus MR, Dill LM (2006) Does tiger shark predation risk influence foraging habitat use by bottlenose dolphins at multiple spatial scales? Oikos 114:257–264

    Article  Google Scholar 

  • Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Berjder L (2007) State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844

    Article  PubMed  Google Scholar 

  • Helfman GS, Clark JB (1986) Rotational feeding: overcoming gape-limited foraging in anguillid eels. Copeia 1986:679–685

    Article  Google Scholar 

  • Hemida F, Seridji R, Labidi N, Bensaci J, Capapé C (2002) Records of Carcharhinus spp. (Chondrichthyes: Carcharhinidae) from off the Algerian coast (southern Mediterranean). Acta Adriat 43:83–92

    Google Scholar 

  • Herrel A, Gibb AC (2006) Ontogeny of performance in vertebrates. Physiol Biochem Zool 79:1–6

    Article  PubMed  Google Scholar 

  • Herrel A, O’Reilly JC (2006) Ontogenetic scaling of bite force in lizards and turtles. Physiol Biochem Zool 79:31–42

    Article  PubMed  Google Scholar 

  • Hines AH, Whitlach RB, Thrush SF, Hewitt JE, Cummings VJ, Dayton PK, Legendre P (1997) Nonlinear foraging response of a large marine predator to benthic prey: eagle ray pits and bivalves in a New Zealand sandflat. J Exp Mar Biol Ecol 216:191–210

    Article  Google Scholar 

  • Huber DR, Weggelaar CL, Motta PJ (2006) Scaling of bite force in the blacktip shark Carcharhinus limbatus. Zoology 109:109–119

    Article  PubMed  Google Scholar 

  • Kardong KV (1996) Evolution of aging: theoretical and practical implications from rattlesnakes. Zoo Biol 15:267–277

    Article  Google Scholar 

  • King JR, Murphy ME (1985) Periods of nutritional stress in the annual cycles of endotherms: fact or fiction? Am Zool 25:955–964

    Google Scholar 

  • Kitowski I (2003) Age-related differences in foraging behavior of Montagu’s harrier Circus pygargus males in south-east Poland. Acta Ethol 6:35–38

    Article  Google Scholar 

  • Lind AJ, Welsh HH Jr, (1994) Ontogenetic changes in foraging behaviour and habitat use by the Oregon garter snake, Thamnophis atratus hydrophilus. Anim Behav 48:1261–1273

    Article  Google Scholar 

  • Lisney TJ, Bennett MB, Collin SP (2007) Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs. Raffles Bull Zool 14(Suppl):7–15

    Google Scholar 

  • Lowe CG, Wetherbee BM, Crow GL, Tester AL (1996) Ontogenetic dietary shifts and feeding behavior of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environ Biol Fish 47:203–211

    Article  Google Scholar 

  • Lucas Z, Stobo WT (2000) Shark-inflicted mortality on a population of harbour seals (Phoca vitulina) at Sable Island, Nova Scotia. J Zool 252:405–414

    Article  Google Scholar 

  • Lucifora LO, Menni RC, Escalante AH (2005a) Reproduction, abundance and feeding habits of the broadnose sevengill shark Notorynchus cepedianus in north Patagonia, Argentina. Mar Ecol Prog Ser 289:237–244

    Article  Google Scholar 

  • Lucifora LO, Menni RC, Escalante AH (2005b) Reproduction and seasonal occurrence of the copper shark, Carcharhinus brachyurus, from north Patagonia, Argentina. ICES J Mar Sci 62:107–115

    Article  Google Scholar 

  • 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 315:259–270

    Article  Google Scholar 

  • Magurran AE (2004) Measuring biological diversity. Blackwell, Malden

    Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Google Scholar 

  • McCormick MI (1998) Ontogeny of diet shift by a microcarnivorous fish, Cheilodactylus spectabilis: relationship between feeding mechanics, microhabitat selection and growth. Mar Biol 132:9–20

    Article  Google Scholar 

  • Menni RC (1983) Los peces en el medio marino. Editorial Hemisferio Sur, Buenos Aires

  • Motta PJ, Wilga CD (2001) Advances in the study of feeding behaviors, mechanisms and mechanics of sharks. Environ Biol Fish 60:131–156

    Article  Google Scholar 

  • Muñoz-Chápuli R (1984) Ethologie de la reproduction chez quelques requins de l’Atlantique Nord-Est. Cybium 8:1–14

    Google Scholar 

  • Myers RA, Ottensmeyer CA (2005) Extinction risk in marine species. In: Norse EA, Crowder LB (eds) Marine conservation biology: the science of maintaining the sea’s biodiversity. Island Press, Washington, pp 58–79

    Google Scholar 

  • Myers RA, Worm B (2005) Extinction, survival or recovery of large predatory fishes. Phil Trans R Soc B 360:13–20

    Article  PubMed  Google Scholar 

  • Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850

    Article  PubMed  CAS  Google Scholar 

  • Okey TA, Banks S, Born AF, Bustamante RH, Calvopiña M, Edgar GJ, Espinoza E, Fariña JM, Garske LE, Reck GK, Salazar S, Shepherd S, Toral-Granda V, Wallem P (2004) A trophic model of a Galápagos subtidal rocky reef for evaluating fisheries and conservation strategies. Ecol Model 172:383–401

    Article  Google Scholar 

  • Page B, McKenzie J, Goldsworthy SD (2005) Dietary resource partitioning among sympatric New Zealand and Australian fur seals. Mar Ecol Prog Ser 293:283–302

    Article  Google Scholar 

  • Pauly DA, Christensen V, Guénette S, Pitcher TJ, Sumaila UR, Walters CJ, Watson R, Zeller D (2002) Towards sustainability in world fisheries. Nature 418:689–695

    Article  PubMed  CAS  Google Scholar 

  • Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleosts fishes. Chapman & Hall, London, pp 363–439

    Google Scholar 

  • Price TD, Grant PR (1984) Life history traits and natural selection for small body size in a population of Darwin’s finches. Evolution 38:483–494

    Article  Google Scholar 

  • Punzo F, Chávez S (2003) Effects of aging on spatial learning and running speed in the shrew (Cryptotis parva). J Mammal 84: 1112–1120

    Article  Google Scholar 

  • Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154

    Article  Google Scholar 

  • Reznick DN, Ghalambor CK (2005) Can commercial fishing cause evolution? Answers from guppies (Poecilia reticulata). Can J Fish Aquat Sci 62:791–801

    Article  Google Scholar 

  • Robbins CT (1983) Wildlife feeding and nutrition. Academic Press, New York

    Google Scholar 

  • Rutz C, Whittingham MJ, Newton I (2006) Age-dependent diet choice in an avian top predator. Proc R Soc B 273:579–586

    Article  PubMed  Google Scholar 

  • Scharf FS, Buckel JA, Juanes F, Conover DO (1997) Estimating piscine prey size from partial remains: testing for shifts in foraging mode by juvenile bluefish. Environ Biol Fish 49:377–388

    Article  Google Scholar 

  • Scharf FS, Juanes F, Sutherland MS (1998) Inferring ecological relationships from the edges of scatter diagrams: comparison of regression techniques. Ecology 79:448–460

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Shepherd TD, Myers RA (2005) Direct and indirect fishery effects on small coastal elasmobranchs in the northern Gulf of Mexico. Ecol Lett 8:1095–1104

    Article  Google Scholar 

  • Simpfendorfer CA, Goodreid A, McAuley RB (2001) Size, sex and geographic variation in the diet of the tiger shark, Galeocerdo cuvier, from Western Australian waters. Environ Biol Fish 61:37–46

    Article  Google Scholar 

  • Smale MJ (1991) Occurrence and feeding of three shark species, Carcharhinus brachyurus, C. obscurus and Sphyrna zygaena, on the Eastern Cape coast of South Africa. S Afr J Mar Sci 11:31–42

    Google Scholar 

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

  • Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494

    Article  Google Scholar 

  • Strong WR Jr, Snelson FF Jr, Gruber SH (1990) Hammerhead shark predation on stingrays: an observation of prey handling by Sphyrna mokarran. Copeia 1990:836–840

    Article  Google Scholar 

  • Taniuchi T (1990) The role of elasmobranchs in Japanese fisheries. 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 Tech Rep NMFS 90:415–426

  • Thrush SF, Pridmore RD, Hewitt JE, Cummings VJ (1991) Impact of ray feeding disturbances on sandflat macrobenthos: do communities dominated by polychaetes or shellfish respond differently? Mar Ecol Prog Ser 69:245–252

    Article  Google Scholar 

  • VanBlaricom GR (1982) Experimental analyses of structural regulation in a marine sand community exposed to oceanic swell. Ecol Monogr 52:283–305

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S-Plus, 4th edn. Springer, New York

    Google Scholar 

  • Walter JP, Ebert DA (1991) Preliminary estimates of age of the bronze whaler Carcharhinus brachyurus (Chondrichthyes: Carcharhinidae) from southern Africa, with a review of some life history parameters. S Afr J Mar Sci 10:37–44

    Google Scholar 

  • Ward P, Myers RA (2005) Shifts in open-ocean fish communities coinciding with the commencement of commercial fishing. Ecology 86:835–847

    Article  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

  • Whitney NM, Crow GL (2007) Reproductive biology of the tiger shark (Galeocerdo cuvier) in Hawaii. Mar Biol 151:63–70

    Article  Google Scholar 

  • Wirsing AJ, Heithaus MR, Dill LM (2007) Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)? Oecologia 153:1031–1040

    Article  PubMed  Google Scholar 

  • Wood S (2006) Generalized additive models: an introduction with R. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

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Acknowledgements

Field work was supported by CONICET (Argentina) (scholarship to L.O.L.). L.O.L. and V.B.G. were supported by the Pew Charitable Trusts through the Pew Global Shark Assessment. We thank the fishermen and fish processing plants from Bahía San Blas (Tiburón I, Deró, Penélope, La Barca, Atlántida and La Filetera) for allowing us the access to sample sharks. We thank Claudia Bremec and Diego Giberto for help in the identification of invertebrate prey, and Marti Anderson for advice for conducting the NPMANOVA analysis. We thank Julia Baum, Ariel Farías, Alejandro Frid, Boris Worm and two anonymous reviewers for valuable comments that greatly improved the manuscript. Field work procedures of this study comply with the laws of Argentina.

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Authors and Affiliations

  1. Department of Biology, Dalhousie University, 1355 Oxford Street, B3H 4J1, Halifax, NS, Canada

    Luis O. Lucifora & Verónica B. García

  2. Departamento Científico Zoología Vertebrados, Museo de La Plata, Paseo del Bosque s/n, La Plata, B1900FWA, Argentina

    Roberto C. Menni

  3. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Roberto C. Menni & Alicia H. Escalante

  4. Departamento de Biología, Universidad Nacional de Mar del Plata, Funes 3250, Segundo Piso, Mar del Plata, B7602AYJ, Argentina

    Alicia H. Escalante

  5. Instituto Nacional de Investigación y Desarrollo Pesquero, Paseo Victoria Ocampo s/n, Mar del Plata, B7602HSA, Argentina

    Natalia M. Hozbor

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  1. Luis O. Lucifora
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  2. Verónica B. García
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  3. Roberto C. Menni
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Correspondence to Luis O. Lucifora.

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Lucifora, L.O., García, V.B., Menni, R.C. et al. Effects of body size, age and maturity stage on diet in a large shark: ecological and applied implications. Ecol Res 24, 109–118 (2009). https://doi.org/10.1007/s11284-008-0487-z

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