Skip to main content
Log in

Stingray life history trade-offs associated with nursery habitat use inferred from a bioenergetics model

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Consumption rates of marine predators are vital to assessing their trophic impacts and potential consequences of fisheries removal and habitat alteration, yet are rarely estimated. Standard metabolic rates were estimated for juvenile brown stingrays, Dasyatis lata, and used as input parameters for a bioenergetics model to predict consumption rates. Temperature and mass had significant effects on metabolic rates. The energy budget of juvenile brown stingrays was heavily weighted toward metabolism, accounting for 66 % of consumed energy. Growth accounted for 7 % of the energy budget indicating very slow growth potentially due to limited food resources. Population consumption rates suggest potential for strong top-down effects on prey populations due to stingray predation. This study suggests the use of Kāne‘ohe Bay as a nursery habitat for juvenile brown stingrays is a trade-off between increased juvenile survival through predator avoidance and a late age at first maturity due to slow growth rates resulting from low prey availability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bartell SM, Breck JE, Gardner RH, Brenkert AL (1986) Individual parameter perturbation and error analysis of fish bioenergetics models. Can J Fish Aquat Sci 43:160–168

    Article  Google Scholar 

  • Bascompte J, Melian CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. PNAS 102:5443–5447

    Article  CAS  Google Scholar 

  • Bethea DM, Hale LF, 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 152:1009–1020

    Article  Google Scholar 

  • Boisclair D, Sirois P (1993) Testing assumptions of fish bioenergetics models by direct estimation of growth, consumption, and activity rates. Trans Am Fish Soc 122:784–796

    Article  Google Scholar 

  • Brett JR, Groves TD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol VIII. Academic Press, New York, pp 279–352

    Google Scholar 

  • Brill RW (1996) Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish. Comp Biochem Phys A 113:3–15

    Article  Google Scholar 

  • Bush A (2002) Feeding ecology of juvenile scalloped hammerheads in Kaneohe Bay, Oahu, Hawaii. Dissertation, University of Hawaii

  • Bush A (2003) Diet and diel feeding periodicity of juvenile scalloped hammerhead sharks, Sphyrna lewini, in Kaneohe Bay, Oahu, Hawaii. Env Biol Fish 67:1–11

    Article  Google Scholar 

  • Bush A, Holland K (2002) Food limitation in a nursery area: estimates of daily ration in juvenile scalloped hammerheads, Sphyrna lewini (Griffith and Smith, 1834) in Kane’ohe Bay, O’ahu, Hawai’i. J Exp Mar Biol Ecol 278:157–178

    Article  Google Scholar 

  • Carlson JK, Goldman KJ, Lowe CG (2004) Metabolism, energetic demand, and endothermy. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 203–224

    Chapter  Google Scholar 

  • Carlson JK, Palmer CL, Parsons GR (1999) Oxygen consumption rate and swimming efficiency of the blacknose shark, Carcharhinus arconotus. Copeia 1:34–39

    Article  Google Scholar 

  • Cartamil DP, Vaudo JJ, Lowe CG, Weherbee BM, Holland KN (2003) Diel movement patterns of the Hawaiian stingray, Dasyatis lata: implications for ecological interactions between sympatric elasmobranch species. Mar Biol 142:841–847

    Google Scholar 

  • Chen W-K, Liu KM, Liao YY (2008) Bioenergetics of juvenile whitespotted bamboo shark Chiloscyllium plagiosum [Anonymous (Bennett)]. Fish Biol 72:1245–1258

    Article  CAS  Google Scholar 

  • Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717

    Article  Google Scholar 

  • Cortés E (2002) Incorporating uncertainty into demographic modeling: application to shark populations and their conservation. Cons Biol 16:1048–1062

    Article  Google Scholar 

  • Cortés E (2004) Life history patterns, demography, and population dynamics. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, FL, pp 449–469

    Chapter  Google Scholar 

  • Crowe GL, Lowe CG, Weherbee BM (1996) Shark records from longline fishing programs in Hawaii with comments on Pacific Ocean distributions. Pac Sci 50:382–392

    Google Scholar 

  • Dale JJ, Holland KN (2012) Age, growth and maturity of the brown stingray (Dasyatis lata) around Oahu, Hawaii. Mar Fresh Res 63:475–484

    Article  CAS  Google Scholar 

  • Dale JJ, Stankus AM, Burns MS, Meyer CG (2011a) The shark assemblage at French Frigate Shoals Atoll, Hawaii: species composition, abundance and habitat use. PLoS ONE 6:e16962. doi:16910.11371/journal.pone.0016962

    Article  CAS  Google Scholar 

  • Dale JJ, Wallsgrove NJ, Popp BN, Holland KN (2011b) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar Ecol Prog Ser 433:221–236

    Article  Google Scholar 

  • Dowd WW, Brill RW, Bushnell PG, Musick JA (2006a) Estimating consumption rates of juvenile sandbar sharks (Carcharhinus plumbeus) in Chesapeake Bay, Virginia, using a bioenergetics model. Fish Bull 104:332–342

    Google Scholar 

  • Dowd WW, Brill RW, Bushnell PG, Musick JA (2006b) Standard and routine metabolic rates of juvenile sandbar sharks (Carcharhinus plumbeus), including the effects of body mass and acute temperature change. Fish Bull 104:323–331

    Google Scholar 

  • Drazen JC (2007) Depth related trends in proximate composition of demersal fishes in the eastern North Pacific. Deep-Sea Res I 54:203–219

    Article  Google Scholar 

  • Du Preez HH, McLachlan A, Marias JFK (1988) Oxygen consumption of two nearshore marine elasmobranchs, Rhinobatos annulatus (Muller and Henle, 1841) and Myliobatus aquila (Linnaeus, 1758). Comp Biochem Phys A 89:283–294

    Article  Google Scholar 

  • Duffy KA (1999) Feeding, growth and bioenergetics of the chain dogfish, Scyliorhinus retifer. Dissertation, University of Rhode Island

  • Duncan KM (2006) Estimation of daily energetic requirements in young scalloped hammerhead sharks, Sphyrna lewini. Environ Biol Fish 76:139–149

    Article  Google Scholar 

  • Duncan KM, Holland KN (2006) Habitat use, growth rates and dispersal patterns of juvenile scalloped hammerhead sharks Sphyrna lewini in a nursery habitat. Mar Ecol Prog Ser 312:211–221

    Article  Google Scholar 

  • Ebert DA, Bizzarro JJ (2007) Standardized diet compositions and trophic levels of skates (Chondrichthyes : rajiformes : Rajoidei). Environ Biol Fish 80:221–237

    Article  Google Scholar 

  • Elliott JM, Davison W (1975) Energy equivalents of oxygen consumption in animal energetics. Oecolog 19:195–201

    Article  Google Scholar 

  • Ezcurra JM (2001) The mass-specific routine metabolic rate of captive pelagic stingrays, Dasyatis violacea, with comments on energetics. Masters Thesis, California State University, Stanislaus

  • Ferry-Graham LA, Gibb AC (2001) Comparison of fasting and postfeeding metabolic rates in a sedentary shark, Cephaloscyllium ventriosum. Copeia 4:1108–1112

    Article  Google Scholar 

  • Fournier RW (1996) The metabolic rates of two species of benthic elasmobranchs, nurse sharks and southern stingrays. M.S. thesis, Hofstra University, Hempstead, NY 29 pp

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  CAS  Google Scholar 

  • Godø OR, Huse I, Michalsen K (1997) Bait defence behavior of wolffish and its impact on long-line catch rates. ICES J Mar Sci 54:273–275

    Article  Google Scholar 

  • Goodman-Lowe GD, Carpenter JR, Atkinson S, Ako H (1999) Nutrient, fatty acid, amino acid and mineral analysis of natural prey of the Hawaiian monk seal, Monachus schauinslandi. Comp Biochem Phys A 123:137–146

    CAS  Google Scholar 

  • Gruber SH (1984) Bioenergetics of captive and free-ranging lemon sharks. AAZPA Annual Conference Proceedings, pp 340–373

  • Gruber SH, Nelson DR, Morrissey JF (1988) Patterns of activity and space utilization of lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon. Bull Mar Sci 43:61–76

    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 487–522

    Chapter  Google Scholar 

  • Heppell SS, Crowder LB, Menzel TR (1999) Life table analysis of long-lived marine species with implications for conservation and management. In: Musick JA (ed) Life in the slow lane: ecology and conservation of long-lived marine animals, American Fisheries Society Symposium 23. Bethesda, Maryland, pp 137–148

    Google Scholar 

  • Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser 337:287–297

    Article  Google Scholar 

  • Hopkins TE, Cech JJ (1994) Effect of temperature on oxygen consumption of bat rays, Myliobatis californica (Chondrichthyes, Myliobatididae). Copeia 2:529–532

    Article  Google Scholar 

  • Jennings D, Gruber S, Franks B, Kessel S, Robertson A (2008) Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini, Bahamas. Environ Biol Fish 83:369–377

    Article  Google Scholar 

  • Jobling M (1981) The influence of feeding on the metabolic rate of fishes: a short review. J Fish Biol 18:385–400

    Article  Google Scholar 

  • Laprise R, Blaber SJM (1992) Predation by moses perch, Lutjanus russelli, and blue-spotted trevally, Caranx bucculentus, on juvenile brown tiger prawn, Penaeus esculentus: effects of habitat structure and time of day. J Fish Biol 40:627–635

    Article  Google Scholar 

  • Laws EA, Allen CB (1996) Water quality in a subtropical embayment more than a decade after diversion of sewage discharges. Pac Sci 50:194–210

    CAS  Google Scholar 

  • Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809

    Article  CAS  Google Scholar 

  • Lowe C (2001) Metabolic rates of juvenile scalloped hammerhead sharks (Sphyrna lewini). Mar Biol 139:447–453

    Google Scholar 

  • Lowe CG (2002) Bioenergetics of free-ranging juvenile scalloped hammerhead sharks (Sphyrna lewini) in Kane’ohe Bay, O’ahu, HI. J Exp Mar Biol Ecol 278:141–156

    Article  Google Scholar 

  • Mateo I (2007) A bioenergetics based comparison of growth conversion efficiency of Atlantic cod on Georges Bank and in the Gulf of Main. J North Atl Fish Sci 38:23–35

    Article  Google Scholar 

  • McEachran JD (1990) Diversity of rays: why are there so many species? Chondros 2:1–6

    Google Scholar 

  • McNab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, New York

    Google Scholar 

  • McNeill S, Lawton JH (1970) Annual production and respiration in animal populations. Nature 225:472–474

    Article  Google Scholar 

  • Medved RJ, Stillwell CE, Casey JG (1988) The rate of food consumption of young sandbar sharks (Carcharhinus plumbeus) in Chincoteague Bay, Virginia. Fish Bull 83:395–402

    Google Scholar 

  • Meyer CG, Holland KN, Wetherbee BM, Lowe CG (2001) Diet, resource partitioning and gear vulnerability of Hawaiian jacks captured in fishing tournaments. Fish Res 53:105–113

    Article  Google Scholar 

  • Neer J, Carlson J, Thompson B (2006) Standard oxygen consumption of seasonally acclimatized cownose rays, Rhinoptera bonasus (Mitchill 1815), in the northern Gulf of Mexico. Fish Phys Biochem 32:67–71

    Article  CAS  Google Scholar 

  • Neer JA, Rose KA, Cortés E (2007) Simulating the effects of temperature on individual and population growth of Rhinoptera bonasus: a coupled bioenergetics and matrix modeling approach. Mar Ecol Prog Ser 329:211–223

    Article  Google Scholar 

  • Pérez-Casanova JC, Lall SP, Gamperl AK (2009) Effect of feed composition and temperature on food consumption, growth and gastric evacuation of juvenile Atlantic cod (Gadus morhua L.) and haddock (Melanogrammus aeglefinus L.). Aquaculture 294:228–235

    Article  Google Scholar 

  • Pierce SJ, Bennett MB (2010) Destined to decline? Intrinsic susceptibility of the threatened estuary stingray to anthropogenic impacts. Mar Fresh Res 61:1468–1481

    Article  CAS  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Schindler DE, Essington TE, Kitchell JF, Boggs C, Hilborn R (2002) Sharks and tunas: fisheries impacts on predators with contrasting life histories. Ecol App 12:735–748

    Article  Google Scholar 

  • Secor SM, Wooten JA, Cox CL (2007) Effects of meal size, meal type, and body temperature on the specific dynamic action of anurans. J Comp Phys B 177:165–182

    Article  Google Scholar 

  • Sims DW (1996) The effect of body size on the standard metabolic rate of the lesser spotted dogfish. J Fish Biol 48:542–544

    Article  Google Scholar 

  • Sims DW, Davies SJ (1994) Does specific dynamic action (SDA) regulate return of appetite in the lesser spotted dogfish, Scyliorhinus canicula? J Fish Biol 45:341–348

    Google Scholar 

  • Smith CR, Kukert H (1996) Macrobenthic community structure, secondary production, and rates of bioturbation and sedimentation at the Kaneohe Bay lagoon floor. Pac Sci 50:211–229

    Google Scholar 

  • Smith SV, Kimmerer WJ, Laws EA, Brock RW, Walsh TW (1981) Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation. Pac Sci 35:279–395

    CAS  Google Scholar 

  • 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 

  • Stevens M, Maes J, Ollevier F (2006) A bioenergetics model for juvenile flounder Platichthys flesus. J App Ichthy 22:79–84

    Article  Google Scholar 

  • Stewart DJ, Ibarra M (1991) Predation and production by salmonine fishes in Lake Michigan, 1978–88. Can J Fish Aqua Sci 48:909–922

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Stillwell CE, Kohler NE (1993) Food habits of the sandbar shark Carcharhinus plumbeus off the U.S. northeast coast, with estimates of daily ration. Fish Bull 91:138–150

    Google Scholar 

  • Sundström LF, Gruber SH (1998) Using speed-sensing transmitters to construct a bioenergetics model for subadult lemon sharks, Negaprion brevirostris (Poey), in the field. Hydrobiologia 371(372):241–247

    Article  Google Scholar 

  • Thayer GW, Schaaf JW, Angelovic JW, LaCroix MW (1973) Caloric measurements of some estuarine organisms. Fish Bull 71:289–296

    Google Scholar 

  • Vaudo JJ, Heithaus MR (2009) Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia. Mar Biol 165:2579–2590

    Article  Google Scholar 

  • Wetherbee BM, Gruber SH (1993) Absorption efficiency of the lemon shark Negaprion brevirostris at varying rates of energy intake. Copeia 2:416–425

    Article  Google Scholar 

Download references

Acknowledgments

We thank M. Burns, A. Stankus, C. Clark and C. Espasandin for assistance with the collection and husbandry of animals used in this study. For general support and assistance, we thank Y. Papastamatiou, M. Hutchinson, J. Anderson, C. Meyer and K. Gavey. Special thanks to M. Donahue for modeling insight, N. Condon for assistance with proximate analysis, R. Kanno for assistance with respirometer design and construction, and C. Lowe for equipment. This manuscript was improved by the comments of two anonymous reviewers. Partial funding was provided by the PADI Foundation (2007-324). This study was carried out in accordance with the animal use protocols of the University of Hawaii (protocol 06-030-5).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan J. Dale.

Additional information

Communicated by M. A. Peck.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 123 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dale, J.J., Drazen, J.C. & Holland, K.N. Stingray life history trade-offs associated with nursery habitat use inferred from a bioenergetics model. Mar Biol 160, 3181–3192 (2013). https://doi.org/10.1007/s00227-013-2305-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2305-6

Keywords

Navigation