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Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)?

  • Behavioral Ecology
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Abstract

Predators can influence plants indirectly by altering spatial patterns of herbivory, so studies assessing the relationship between perceived predation risk and habitat use by herbivores may improve our understanding of community organization. In marine systems, the effects of predation danger on space use by large herbivores have received little attention, despite the possibility that predator-mediated alterations in patterns of grazing by these animals influence benthic community structure. We evaluated the relationship between habitat use by foraging dugongs (Dugong dugon) and the threat of tiger shark predation in an Australian embayment (Shark Bay) between 1997 and 2004. Dugong densities were quantified in shallow (putatively dangerous) and deep (putatively safe) habitats (seven survey zones allocated to each habitat), and predation hazard was indexed using catch rates of tiger sharks (Galeocerdo cuvier); seagrass volume provided a measure of food biomass within each zone. Overall, dugongs selected shallow habitats, where their food is concentrated. Foragers used shallow and deep habitats in proportion to food availability (input matching) when large tiger sharks were scarce and overused deep habitats when sharks were common. Furthermore, strong synchrony existed between daily measures of shark abundance and the extent to which deep habitats were overused. Thus, dugongs appear to adaptively manage their risk of death by allocating time to safe but impoverished foraging patches in proportion to the likelihood of encountering predators in profitable but more dangerous areas. This apparent food-safety trade-off has important implications for seagrass community structure in Shark Bay, as it may result in marked temporal variability in grazing pressure.

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References

  • Abrahams MV, Dill LM (1989) A determination of the energetic equivalence of the risk of predation. Ecology 70:999–1007

    Google Scholar 

  • Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134

    Article  Google Scholar 

  • Anderson DR, Burnham KP, Thompson WL (2000) Null hypothesis testing: problems, prevalence, and an alternative. J Wildl Manage 64:912–923

    Article  Google Scholar 

  • Anderson PK (1986) Dugongs of Shark Bay, Australia—Seasonal migration, water temperature, and forage. Natl Geogr Res 2:473–490

    Google Scholar 

  • Anderson PK (1995) Scarring and photoidentification of dugongs (Dugong dugon) in Shark Bay, Western Australia. Aq Mam 21:205–211

    Google Scholar 

  • Anderson PK, Prince RIT (1985) Predation on dugongs: attacks by killer whales. J Mammal 66:554–556

    Article  Google Scholar 

  • Aragones LV, Lawler IR, Foley WJ, Marsh H (2006) Dugong grazing and turtle cropping: grazing optimization in tropical seagrass systems? Oecologia 149:635–647

    Article  PubMed  Google Scholar 

  • Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014

    Article  Google Scholar 

  • Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399

    Article  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Chilvers BL, Delean S, Gales NJ, Holley DK, Lawler IR, Marsh H, Preen AR (2004) Diving behaviour of dugongs, Dugong dugon. J Exp Mar Biol Ecol 304:203–224

    Article  Google Scholar 

  • Crawley MJ (1983) Herbivory. University of California Press, Los Angeles, CA

  • de Iongh HH, Wenno BJ, Meelis E (1995) Seagrass distribution and seasonal biomass changes in relation to dugong grazing in the Moluccas, East Indonesia. Aq Bot 50:1–19

    Article  Google Scholar 

  • Dill LM, Heithaus MR, Walters CJ (2003) Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84:1151–1157

    Article  Google Scholar 

  • Fretwell SD, Lucas HL (1970) On territorial behavior and other factors influencing habitat distributions in birds: I. Theoretical developments. Acta Biotheor 19:16–36

    Article  Google Scholar 

  • Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Cons Ecol 6(1):11 (http://www.consecol.org/vol6/iss1/art11)

    Google Scholar 

  • Gales N, McCauley RD, Lanyon J, Holley D (2004) Change in abundance of dugongs in Shark Bay, Ningaloo and Exmouth Gulf, Western Australia: evidence for large-scale migration. Wildl Res 31:283–290

    Article  Google Scholar 

  • Hays GC (2003) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia 503:163–170

    Article  Google Scholar 

  • Heithaus MR (2001) The biology of tiger sharks, Galeocerdo cuvier, in Shark Bay, Western Australia: sex ratio, size distribution, diet and seasonal changes in catch rates. Environ Biol Fish 61:25–36

    Article  Google Scholar 

  • Heithaus MR (2004a) Fish communities of seagrass meadows and associated habitats in Shark Bay, Western Australia. B Mar Sci 75:79–99

    Google Scholar 

  • Heithaus MR (2004b) Predator-prey interactions. In: Carrier JC, Musick J, Heithaus MR (eds) The biology of sharks, skates, and rays. CRC Press, Boca Raton, FL, 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, Dill LM, Marshall GJ, Buhleier BM (2002) Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a subtropical seagrass ecosystem. Mar Biol 140:237–248

    Article  Google Scholar 

  • Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Bejder 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 (in press). doi:10.1111/j.1365-2656.2007.01260.x

  • Lanyon J, Johns T, Sneath HL (2005) Year round presence of dugongs in Pumicestone Passage, south-east Queensland, examined in response to water temperature and seagrass distribution. Wildl Res 32:361–368

    Article  Google Scholar 

  • Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elf, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, USA. Can J Zool 79:1401–1409

    Article  Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 27:215–290

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    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 

  • Marsh H, Channells PW, Heinsohn GE, Morrissey J (1982) Analysis of stomach contents of dugongs from Queensland. Aust Wildl Res 9:55–67

    Article  Google Scholar 

  • Marsh H, Prince RIT, Saalfeld WK, Shepherd R (1994) The distribution and abundance of the dugong in Shark Bay, Western Australia. Wildl Res 21:149–161

    Article  Google Scholar 

  • Masini RJ, Anderson PK, McComb AJ (2001) A Halodule-dominated community in a subtropical embayment: physical environment, productivity, biomass, and impact of dugong grazing. Aq Bot 71:179–197

    Article  Google Scholar 

  • McNamara JM, Houston AI (1987) Starvation and predation as factors limiting population size. Ecology 68:1515–1519

    Article  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

    PubMed  CAS  Google Scholar 

  • Nakaoka M, Aioi K (1999) Growth of the seagrass Halophila ovalis at the dugong trails compared to existing within-patch variation in a Thailand intertidal flat. Mar Ecol Prog Ser 184:97–103

    Article  Google Scholar 

  • Peacor SD, Werner EE (2000) Predator effects on an assemblage of consumers through induced changes in consumer foraging behavior. Ecology 81:1998–2010

    Article  Google Scholar 

  • Peacor S, Werner E (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci USA 98:3904–3908

    Article  PubMed  CAS  Google Scholar 

  • Power ME (1984a) Habitat quality and the distribution of algae-grazing catfish in a Panamanian stream. J Anim Ecol 53:357–374

    Article  Google Scholar 

  • Power ME (1984b) Depth distributions of armored catfish: predator-induced resource avoidance? Ecology 65:523–528

    Article  Google Scholar 

  • Preen A (1995) Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Mar Ecol Prog Ser 124:201–213

    Article  Google Scholar 

  • Preen AR, Marsh H, Lawler IR, Prince RIT, Shepherd R (1997) Distribution and abundance of dugongs, turtles, dolphins, and other megafauna in Shark Bay, Ningaloo Reef and Exmouth Gulf, Western Australia. Wildl Res 24:185–208

    Article  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509

    Article  Google Scholar 

  • Schmitz OJ (2003) Top predator control of plant biodiversity and productivity in an old-field ecosystem. Ecol Lett 6:156–163

    Article  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Article  Google Scholar 

  • Sheppard JK, Preen AR, Marsh H, Lawler IR, Whiting SD, Jones RE (2006) Movement heterogeneity of dugongs, Dugong dugon (Müller), over large spatial scales. J Exp Mar Biol Ecol 334:64–83

    Article  Google Scholar 

  • Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210:1041–1043

    Article  PubMed  Google Scholar 

  • Simpfendorfer CA, Goodreid AB, 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 

  • Travers MJ, Potter IC (2002) Factors influencing the characteristics of fish assemblages in a large subtropical marine embayment. J Fish Biol 61:764–784

    Article  Google Scholar 

  • van Baalen M, Sabelis MW (1993) Coevolution of patch selection strategies of predator and prey and the consequences for ecological stability. Am Nat 142:646–670

    Article  PubMed  Google Scholar 

  • Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464

    Article  Google Scholar 

  • Walker DI, Kendrick GA, McComb AJ (1988) The distribution of seagrass species in Shark Bay, Western Australia, with notes on their ecology. Aq Bot 30:305–317

    Article  Google Scholar 

  • Ward JF, Austin RM, Macdonald DW (2000) A simulation model of foraging behaviour and the effect of predation risk. J Anim Ecol 69:16–30

    Article  Google Scholar 

  • Warner RR (1998) The role of extreme iteroparity and risk-avoidance in the evolution of mating systems. J Fish Biol 53(Suppl A):82–93

    Article  Google Scholar 

  • Werner EE (1998) Ecological experiments and a research program in community ecology. In: Resetarits WJ, Bernardo J (eds) Experimental ecology: issues and perspectives. Oxford University Press, Oxford, UK, pp 3–26

    Google Scholar 

  • White GC, Bennetts RE (1996) Analysis of frequency count data using the negative binomial distribution. Ecology 77:2549–2557

    Article  Google Scholar 

  • Wirsing AJ, Heithaus MR, Dill LM (2006) Tiger shark (Galeocerdo cuvier) abundance and growth in a subtropical embayment: evidence from 7 years of standardized fishing effort. Mar Biol 149:961–968

    Article  Google Scholar 

  • Wirsing AJ, Heithaus MR, Dill LM (2007) Dugongs prefer to forage in microhabitats that allow escape from rather than avoidance of predators. Anim Behav 74:93–101

    Article  Google Scholar 

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Acknowledgments

We thank R. Abernethy, V. Alla, L. Barre, F. Bretos, S. Buchannan, T. Bujas, J. Burghardt, S. Burghardt, C. Chow, M. Davis, H. Finn, C. Genrich, P. Green, A. Greenley, K. Harper, L. Heithaus, M. Kerford, S. Kowalewsky, A. Krickan, J. Lasky, L. Marshall, K. Martin, J. McLash, R. McPhie, B. Stalvey, J. Wilder, and K. Wirsing for field assistance. This material is based in part upon work supported by the National Science Foundation under Grant Number 0526065. Other grants and support were provided by Australian Geographic, Humminbird, Mercury Marine Australia, Monkey Mia Dolphin Resort, Monkey Mia Wildsights (Shotover), National Geographic Society Expeditions Council, National Geographic Remote Imaging, NSERC Canada grant A6869 to L.M. Dill, PADI Foundation, Shakespeare Electronics, Shark Bay Fish Factory, University of Western Australia, and public donations. We are grateful to I. Anderson, B. Barton, C. Beck, K. Crane, A. Fraser, I. Gordon, D. Rose, R. Swann, and D. Witt for logistical support. Special thanks go to D. Charles for advice, D. Capewell, and the Yadgalah Aboriginal Corporation for information about dugongs, D. Massey for extra field housing, H. Raven for temperature data, E. Elle, J. Estes, G. Hays, P. Peterson, B. Sargeant, R. Ydenberg, and anonymous reviewers for helpful comments, B. Smith, and T. Steury for statistical help, B. Black, J. Heyman, and R. Holst for their hospitality, and the Dill lab for helpful suggestions. This research was conducted under Fisheries Western Australia permits 67/97 and 08/01, Western Australia Department of Conservation and Land Management permits NE001808, SF002347, SF003818, SF004228, and SF004542, SW008085, and renewals, and Simon Fraser University Animal Care permits 639B and 653B, and complied with the current laws of the country in which it was performed. This is contribution number 27 of the Shark Bay Ecosystem Research Project.

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Authors and Affiliations

  1. Behavioural Ecology Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6

    Aaron J. Wirsing & Lawrence M. Dill

  2. Honorary Research Associate, School of Animal Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Aaron J. Wirsing

  3. Department of Biological Sciences, Marine Biology Program, Florida International University, Biscayne Bay Campus MSB, 3000 NE 151 St, North Miami, FL, 33181, USA

    Aaron J. Wirsing & Michael R. Heithaus

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  1. Aaron J. Wirsing
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Correspondence to Aaron J. Wirsing.

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Communicated by Peter Peterson.

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Wirsing, A.J., Heithaus, M.R. & Dill, L.M. Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)?. Oecologia 153, 1031–1040 (2007). https://doi.org/10.1007/s00442-007-0802-3

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