The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem
Michael. R. Heithaus A D , A. J. Wirsing B and L. M. Dill C
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, School of Environment, Arts and Sciences, Florida International University, 3000 NE 151 Street, North Miami, FL 33181, USA.
B School of Environmental and Forest Sciences, Box 352100, University of Washington, Seattle, WA 98195, USA.
C Evolutionary and Behavioural Ecology Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada.
D Corresponding author. Email: heithaus@fiu.edu
Marine and Freshwater Research 63(11) 1039-1050 https://doi.org/10.1071/MF12024
Submitted: 27 January 2012 Accepted: 21 June 2012 Published: 26 November 2012
Abstract
The worldwide decline of large-bodied marine taxa has made it difficult to draw conclusions about the relative importance of top-down control, and the mechanisms through which it might operate, in coastal marine ecosystems. Since 1997, the Shark Bay Ecosystem Research Project has used the relatively pristine seagrass community of Shark Bay, Australia, to investigate the potential for tiger sharks, the apex predator in the ecosystem, to have an impact on their large-bodied prey through non-consumptive (‘risk’) effects. Here, we synthesise nearly 15 years of data to demonstrate that tiger sharks have widespread risk effects on both large-bodied herbivores and mesopredators in Shark Bay and explore the possibility that these impacts may cascade to lower trophic levels. Although much work remains to be done, our studies suggest that losses of top predators in subtropical estuaries may have greater consequences than generally appreciated and that efforts to conserve and restore their populations should be a priority. Furthermore, future management strategies and studies must explicitly consider the potential for predators to influence behaviour of even large-bodied marine taxa.
Additional keywords : behaviourally mediated indirect species interactions (BMII), community dynamics, dugong, Indo‐Pacific bottlenose dolphin, non-consumptive effects, risk effects, tiger shark.
References
Abrahams, M. V., and Dill, L. M. (1989). A determination of the energetic equivalence of the risk of predation. Ecology 70, 999–1007.| A determination of the energetic equivalence of the risk of predation.Crossref | GoogleScholarGoogle Scholar |
Abrams, P. A. (1993). Why predation rate should not be proportional to predator density. Ecology 74, 726–733.
| Why predation rate should not be proportional to predator density.Crossref | GoogleScholarGoogle Scholar |
Aragones, L. V. (2000). A review of the role of the green turtle in tropical seagrass ecosystems. In ‘Sea Turtles of the Indo-Pacific: Research Management and Conservation’. (Eds N. Pilcher and G. Ismails.) pp. 69–85. (ASEAN Academic Press: London.)
Aragones, L. V., and Marsh, H. (2000). Impact of dugong grazing and turtle cropping on tropical seagrass communities. Pacific Conservation Biology 5, 277–288.
Biro, P. A., Post, J. R., and Parkinson, E. A. (2003). From individuals to populations: risk-taking by prey fish mediates mortality in whole-system experiments. Ecology 84, 2419–2431.
| From individuals to populations: risk-taking by prey fish mediates mortality in whole-system experiments.Crossref | GoogleScholarGoogle Scholar |
Biro, P. A., Post, J. R., and Abrahams, M. V. (2005). Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in young fish cohorts. Proceedings. Biological Sciences 272, 1443–1448.
| Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in young fish cohorts.Crossref | GoogleScholarGoogle Scholar |
Brown, J. S. (1992). Patch use under predation risk I. Models and predictions. Annales Zoologici Fennici 29, 301–309.
Brown, J. S., Laundre, J. W., and Gurung, M. (1999). The ecology of fear: optimal foraging, game theory, and trophic interactions. Journal of Mammalogy 80, 385–399.
| The ecology of fear: optimal foraging, game theory, and trophic interactions.Crossref | GoogleScholarGoogle Scholar |
Burkholder, D. A., Heithaus, M. R., and Fourqurean, J. W. (2012). Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem. Marine and Freshwater Research 63, 1051–1058.
| Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem.Crossref | GoogleScholarGoogle Scholar |
Burkholder, D. A., Fourqurean, J. W., and Heithaus, M. R. (). Spatial pattern in seagrass stoichiometry indicates both N-limited and P-limited regions of an iconic P-limited subtropical bay. Marine Ecology Progress Series , .
Burns, J. M., Costa, D. P., Fedak, M. A., Hindell, M. A., Bradshaw, C. J. A., Gales, N. J., McDonald, B., Trumble, S. J., and Crocker, D. E. (2004). Winter habitat use and foraging behavior of crabeater seals along the Western Antarctic peninsula. Deep-sea Research. Part II, Topical Studies in Oceanography 51, 2279–2303.
| Winter habitat use and foraging behavior of crabeater seals along the Western Antarctic peninsula.Crossref | GoogleScholarGoogle Scholar |
Clark, C. W. (1994). Antipredator behavior and the asset-protection principle. Behavioral Ecology 5, 159–170.
| Antipredator behavior and the asset-protection principle.Crossref | GoogleScholarGoogle Scholar |
Cowlishaw, G. (1997). Trade-offs between foraging and predation risk determine habitat use in a desert baboon population. Animal Behaviour 53, 667–686.
| Trade-offs between foraging and predation risk determine habitat use in a desert baboon population.Crossref | GoogleScholarGoogle Scholar |
Creel, S. (2011). Towards a predictive theory of risk effects: hypotheses for prey attributes and compensatory mortality. Ecology 92, 2190–2195.
| Towards a predictive theory of risk effects: hypotheses for prey attributes and compensatory mortality.Crossref | GoogleScholarGoogle Scholar |
Creel, S., and Christianson, D. (2008). Relationships between direct predation and risk effects. Trends in Ecology & Evolution 23, 194–201.
| Relationships between direct predation and risk effects.Crossref | GoogleScholarGoogle Scholar |
Creel, S., Christianson, D., Liley, S., and Winnie, J. (2007). Predation risk affects reproductive physiology and demography in elk. Science 315, 960.
| Predation risk affects reproductive physiology and demography in elk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Clu7Y%3D&md5=97c13e00a70046bc9b31223192807ef2CAS |
De Iongh, H., Wenno, B., and Meelis, E. (1995). Seagrass distribution and seasonal biomass changes in relation to dugong grazing in the Moluccas, East Indonesia. Aquatic Botany 50, 1–19.
| Seagrass distribution and seasonal biomass changes in relation to dugong grazing in the Moluccas, East Indonesia.Crossref | GoogleScholarGoogle Scholar |
Dill, L. M., Heithaus, M. R., and Walters, C. J. (2003). Behaviorally-mediated indirect interactions in marine communities and their conservation and implications. Ecology 84, 1151–1157.
| Behaviorally-mediated indirect interactions in marine communities and their conservation and implications.Crossref | GoogleScholarGoogle Scholar |
Dulvy, N. K., Baum, J. K., Clarke, S., Compagno, L. J. V., Cortes, E., Domingo, A., Fordham, S., Fowler, S., Francis, M. P., Gibson, C., Martinez, J., Musick, J. A., Soldo, A., Stevens, J. D., and Valenti, S. (2008). You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquatic Conservation – Marine and Freshwater Ecosystems 18, 459–482.
| You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays.Crossref | GoogleScholarGoogle Scholar |
Dunphy-Daly, M. M., Heithaus, M. R., Wirsing, A. J., Maradon, J. S. F., and Burkholder, D. A. (2010). Predation risk influences the diving behavior of a marine mesopredator. Open Journal of Ecology 3, 8–15.
| Predation risk influences the diving behavior of a marine mesopredator.Crossref | GoogleScholarGoogle Scholar |
Estes, J. A., Terborgh, J., Brashares, J. S., Power, M. E., Berger, J., Bond, W. J., Carpenter, S. R., Essington, T. E., Holt, R. D., Jackson, J. B. C., Marquis, R. J., Oksanen, L., Oksanen, T., Paine, R. T., Pikitch, E. K., Ripple, W. J., Sandin, S. A., Scheffer, M., Schoener, T. W., Shurin, J. B., Sinclaire, A. R. E., Soulé, M. E., Virtanen, R., and Wardle, D. A. (2011). Trophic downgrading of planet earth. Science 333, 301–306.
| Trophic downgrading of planet earth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1ylur0%3D&md5=393d0a3a590ef31246a06c2f1461ef0cCAS |
Ferretti, F., Worm, B., Britten, G. L., Heithaus, M. R., and Lotze, H. K. (2010). Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13, 1055–1071.
Fourqurean, J. W., Manuel, S., Coates, K. A., Kenworthy, W. J., and Smith, S. R. (2010). Effects of excluding sea turtle herbivores from a seagrass bed: overgrazing may have led to loss of seagrass meadows in Bermuda. Marine Ecology Progress Series 419, 223–232.
| Effects of excluding sea turtle herbivores from a seagrass bed: overgrazing may have led to loss of seagrass meadows in Bermuda.Crossref | GoogleScholarGoogle Scholar |
Fretwell, S. D., and Lucas, H. L. (1969). On territorial behavior and other factors influencing habitat distributions in birds: I. Theoretical developments. Acta Biotheoretica 19, 16–36.
| On territorial behavior and other factors influencing habitat distributions in birds: I. Theoretical developments.Crossref | GoogleScholarGoogle Scholar |
Frid, A., and Dill, L. M. (2002). Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6, 11.
Frid, A., Heithaus, M. R., and Dill, L. M. (2007). Dangerous dive cycles and the proverbial ostrich. Oikos 116, 893–902.
| Dangerous dive cycles and the proverbial ostrich.Crossref | GoogleScholarGoogle Scholar |
Frid, A., Marglive, J., and Heithaus, M. R. (2012). Interspecific variation in life history relates to antipredator decisions by marine mesopredators on temperate reefs. PLoS ONE 7, e40083.
| Interspecific variation in life history relates to antipredator decisions by marine mesopredators on temperate reefs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVaitrk%3D&md5=91f82bff0dab0ca7150468923392e753CAS |
Heck, K. L., and Valentine, J. F. (2007). The primacy of top-down effects in shallow benthic ecosystems. Estuaries and Coasts 30, 371–381.
| The primacy of top-down effects in shallow benthic ecosystems.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R. (2001a). Shark attacks on bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia: attack rate, bite scar frequencies, and attack seasonality. Marine Mammal Science 17, 526–539.
| Shark attacks on bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia: attack rate, bite scar frequencies, and attack seasonality.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R. (2001b). The biology of tiger sharks (Galeocerdo cuvier) in Shark Bay, Western Australia: sex ratio, size distribution, diet, and seasonal changes in catch rates. Environmental Biology of Fishes 61, 25–36.
| The biology of tiger sharks (Galeocerdo cuvier) in Shark Bay, Western Australia: sex ratio, size distribution, diet, and seasonal changes in catch rates.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R. (2001c). Habitat selection by predators and prey in communities with asymmetrical intraguild predation. Oikos 92, 542–554.
| Habitat selection by predators and prey in communities with asymmetrical intraguild predation.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R. (2005). Habitat use and group size of pied cormorants (Phalacrocorax varius) in a seagrass ecosystem: possible effects of food abundance and predation risk. Marine Biology 147, 27–35.
| Habitat use and group size of pied cormorants (Phalacrocorax varius) in a seagrass ecosystem: possible effects of food abundance and predation risk.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., and Dill, L. M. (2002). Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology 83, 480–491.
| Food availability and tiger shark predation risk influence bottlenose dolphin habitat use.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., and Dill, L. M. (2006). Does tiger shark predation risk influence foraging habitat use by bottlenose dolphins at multiple spatial scales? Oikos 114, 257–264.
| Does tiger shark predation risk influence foraging habitat use by bottlenose dolphins at multiple spatial scales?Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., and Frid, A. (2003). Optimal diving under the risk of predation. Journal of Theoretical Biology 223, 79–92.
| Optimal diving under the risk of predation.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Frid, A., Vaudo, J., Worm, B., and Wirsing, A. J. (2010). Unraveling the ecological importance of elasmobranchs. In ‘Sharks and Their Relatives. II: Biodiversity, Adaptive Physiology, and Conservation’. (Eds J. C. Carrier, J. Musick and M. R. Heithaus.) pp. 611–637. (CRC Press: Boca Raton, FL.)
Heithaus, M. R., Marshall, G. J., Buhleier, B. M., and Dill, L. M. (2001). Employing Crittercam to study habitat use and behavior of large sharks. Marine Ecology Progress Series 209, 307–310.
| Employing Crittercam to study habitat use and behavior of large sharks.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Dill, L. M., Marshall, G. J., and Buhleier, B. (2002a). Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Marine Biology 140, 237–248.
| Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Frid, A., and Dill, L. M. (2002b). Species and sex-class differences in shark-inflicted injury frequencies, escape ability, and habitat use of green and loggerhead turtles. Marine Biology 140, 229–236.
| Species and sex-class differences in shark-inflicted injury frequencies, escape ability, and habitat use of green and loggerhead turtles.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., McLash, J. M., Frid, A., Dill, L. M., and Marshall, G. J. (2002c). Novel insights into the behavior of sea turtles from animal-borne cameras. Journal of the Marine Biological Association of the United Kingdom 82, 1049–1050.
| Novel insights into the behavior of sea turtles from animal-borne cameras.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Frid, A., Wirsing, A. J., Bejder, L., and Dill, L. M. (2005). The biology of green and loggerhead turtles under risk from tiger sharks at a foraging ground. Marine Ecology Progress Series 288, 285–294.
| The biology of green and loggerhead turtles under risk from tiger sharks at a foraging ground.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Hamilton, I. M., Wirsing, A. J., and Dill, L. M. (2006). Validation of a randomization procedure to assess animal habitat preferences: microhabitat use of tiger sharks in a seagrass ecosystem. Journal of Animal Ecology 75, 666–676.
| Validation of a randomization procedure to assess animal habitat preferences: microhabitat use of tiger sharks in a seagrass ecosystem.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Frid, A., Wirsing, A. J., Dill, L. M., Fourqurean, J., Burkholder, D., Thomson, J., and Bejder, L. (2007a). State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. Journal of Animal Ecology 76, 837–844.
| State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Wirsing, A. J., Frid, A., and Dill, L. M. (2007b). Species interactions and marine conservation: lessons from an undisturbed ecosystem. Israel Journal of Ecology and Evolution 53, 355–370.
| Species interactions and marine conservation: lessons from an undisturbed ecosystem.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Wirsing, A. J., Dill, L. M., and Heithaus, L. I. (2007c). Long-term movements of tiger sharks satellite-tagged in Shark Bay, Western Australia. Marine Biology 151, 1455–1461.
| Long-term movements of tiger sharks satellite-tagged in Shark Bay, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Burkholder, D., Hueter, R. E., Heithaus, L. I., Pratt, H. W., Jr, and Carrier, J. C. (2007d). Spatial and temporal variation in shark communities of the lower Florida Keys and evidence for historical population declines. Canadian Journal of Fisheries and Aquatic Sciences 64, 1302–1313.
| Spatial and temporal variation in shark communities of the lower Florida Keys and evidence for historical population declines.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Frid, A., Wirsing, A. J., and Worm, B. (2008a). Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23, 202–210.
| Predicting ecological consequences of marine top predator declines.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Wirsing, A. J., Thompson, J., and Burkholder, D. (2008b). A review of lethal and non-lethal effects of predators on adult marine turtles. Journal of Experimental Marine Biology and Ecology 356, 43–51.
| A review of lethal and non-lethal effects of predators on adult marine turtles.Crossref | GoogleScholarGoogle Scholar |
Heithaus, M. R., Wirsing, A. J., Burkholder, D., Thomson, J., and Dill, L. M. (2009). Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. Journal of Animal Ecology 78, 556–562.
| Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics.Crossref | GoogleScholarGoogle Scholar |
Houston, A. I., McNamara, J. M., and Hutchinson, J. M. C. (1993). General results concerning the trade-off between gaining energy and avoiding predation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 341, 375–397.
| General results concerning the trade-off between gaining energy and avoiding predation.Crossref | GoogleScholarGoogle Scholar |
Hugie, D. M., and Dill, L. M. (1994). Fish and game: a game theoretic approach to habitat selection by predators and prey. Journal of Fish Biology 45, 151–169.
Jackson, J. B. C., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., Bradbury, R. H., Cooke, R. G., Erlandson, J., Estes, J. A., Hughes, T. P., Kidwell, S. M., Lange, C. B., Lenihan, H. S., Pandolfi, J. M., Peterson, C. H., Steneck, R. S., Tegner, M. J., and Warner, R. R. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637.
| Historical overfishing and the recent collapse of coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1Khu7o%3D&md5=98ccd86049f9fdc8323e27948a1366d1CAS |
James, M. C., Ottensmeyer, C. A., and Myers, R. A. (2005). Identification of high-use areas and threats to leatherback sea turtles in northern waters: new directions for conservation. Ecology Letters 8, 195–201.
| Identification of high-use areas and threats to leatherback sea turtles in northern waters: new directions for conservation.Crossref | GoogleScholarGoogle Scholar |
Kauffman, M. J., Brodie, J. F., and Jules, E. S. (2010). Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally-mediated trophic cascade. Ecology 91, 2742–2755.
| Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally-mediated trophic cascade.Crossref | GoogleScholarGoogle Scholar |
Kerford, M., Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2008). Danger on the rise: habitat use by bar-bellied sea snakes in Shark Bay, Western Australia. Marine Ecology Progress Series 358, 289–294.
| Danger on the rise: habitat use by bar-bellied sea snakes in Shark Bay, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Křivan, V., Cressman, R., and Schneider, C. (2008). The ideal free distribution: a review and synthesis of the game-theoretic perspective. Theoretical Population Biology 73, 403–425.
| The ideal free distribution: a review and synthesis of the game-theoretic perspective.Crossref | GoogleScholarGoogle Scholar |
Lal, A., Arthur, R., Marbà, N., Lill, A. W. T., and Alcoverro, T. (2010). Implications of conserving an ecosystem modifier: increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadowns. Biological Conservation 143, 2730–2738.
| Implications of conserving an ecosystem modifier: increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadowns.Crossref | GoogleScholarGoogle Scholar |
Lima, S. L. (1998). Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Advances in the Study of Behavior 27, 215–290.
| Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives.Crossref | GoogleScholarGoogle Scholar |
Lima, S. L., and Dill, L. M. (1990). Behavioural decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68, 619–640.
| Behavioural decisions made under the risk of predation: a review and prospectus.Crossref | GoogleScholarGoogle Scholar |
Marsh, H., Thomas, J. O., and Reynolds, J. E., III (2011). ‘Ecology and Conservation of the Sirenia: Dugongs and Manatees.’ (Cambridge University Press: Cambridge, UK.)
Masini, R. J., Anderson, P. K., and McComb, A. J. (2001). A Halodule-dominated community in a subtropical embayment: physical environment, productivity, biomass, and impact of dugong grazing. Aquatic Botany 71, 179–197.
| A Halodule-dominated community in a subtropical embayment: physical environment, productivity, biomass, and impact of dugong grazing.Crossref | GoogleScholarGoogle Scholar |
Miksis-Olds, J. L., Donaghay, P. L., Miller, J. H., Tyack, P. L., and Reynolds, J. E. (2007). Simulated vessel approaches elicit differential responses from manatees. Marine Mammal Science 23, 629–649.
| Simulated vessel approaches elicit differential responses from manatees.Crossref | GoogleScholarGoogle Scholar |
Mills, M. G. L., and Gorman, M. L. (1997). Factors affecting the density and distribution of wild dogs in the Kruger National Park. Conservation Biology 11, 1397–1406.
| Factors affecting the density and distribution of wild dogs in the Kruger National Park.Crossref | GoogleScholarGoogle Scholar |
Moran, K. L., and Bjorndal, K. A. (2005). Simulated green turtle grazing affects structure and productivity of seagrass patches. Marine Ecology Progress Series 305, 235–247.
| Simulated green turtle grazing affects structure and productivity of seagrass patches.Crossref | GoogleScholarGoogle Scholar |
Mori, Y., Mitani, Y., Watanabe, Y., and Katsufumi, S. (2007). A behavioral indicator of prey patch richness derived from diving behavior: the proportion of residence time to the standard time. Israel Journal of Ecology and Evolution 53, 347–354.
| A behavioral indicator of prey patch richness derived from diving behavior: the proportion of residence time to the standard time.Crossref | GoogleScholarGoogle Scholar |
Muhly, T. B., Semeniuk, C., Massolo, A., Hickman, L., and Musiani, M. (2011). Human activity helps prey win the predator-prey space race. PLoS ONE 6, e17050.
| Human activity helps prey win the predator-prey space race.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtl2lsLg%3D&md5=9c40aea5e065d5e3bf52f580a7085e40CAS |
Murdoch, T. J. T., Glasspool, A. F., Outerbridge, M., Ward, J., Manuel, S., Gray, J., Nash, A., Coates, K. A., Pitt, J., Fourqurean, J. W., Barnes, P. A., Vierros, M., Holzer, K., and Smith, S. R. (2007). Large-scale decline of offshore seagrass meadows in Bermuda. Marine Ecology Progress Series 339, 123–130.
| Large-scale decline of offshore seagrass meadows in Bermuda.Crossref | GoogleScholarGoogle Scholar |
Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P., and Peterson, C. H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.
| Cascading effects of the loss of apex predatory sharks from a coastal ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFSitrw%3D&md5=ef94c52575e03549acde2d326c7a950fCAS |
Nakaoka, M., and Aioi, K. (1999). Growth of seagrass Halophila ovalis at dugong trails compared to existing within-patch variation in a Thailand intertidal flat. Marine Ecology Progress Series 184, 97–103.
| Growth of seagrass Halophila ovalis at dugong trails compared to existing within-patch variation in a Thailand intertidal flat.Crossref | GoogleScholarGoogle Scholar |
Papastamatiou, Y., Wetherbee, B., Lowe, C., and Crow, G. (2006). Distribution and diet of four species of Carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion. Marine Ecology Progress Series 320, 239–251.
| Distribution and diet of four species of Carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion.Crossref | GoogleScholarGoogle Scholar |
Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., and Torres, F. (1998). Fishing down marine food webs. Science 279, 860–863.
| Fishing down marine food webs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtVOjtro%3D&md5=5b2952934630ee04c456acf08a6a3a2dCAS |
Peacor, S. D., and Werner, E. E. (2000). Predator effects on an assemblage of consumers through induced changes in consumer foraging behavior. Ecology 81, 1998–2010.
| Predator effects on an assemblage of consumers through induced changes in consumer foraging behavior.Crossref | GoogleScholarGoogle Scholar |
Peacor S. D.,Werner E. E. (2001 ).
Peckarsky, B. L., Abrams, P. A., Bolnick, D. I., Dill, L. M., Grabowski, J. H., Luttbeg, B., Orrock, J. L., Peacor, S. D., Preisser, E. L., and Schmitz, O. J. (2008). Revisiting the classics: considering nonconsumptive effects in textbook examples of predator–prey interactions. Ecology 89, 2416–2425.
| Revisiting the classics: considering nonconsumptive effects in textbook examples of predator–prey interactions.Crossref | GoogleScholarGoogle Scholar |
Power, M. E. (1984). Depth distributions of armored catfish: predator-induced resource avoidance? Ecology 65, 523–528.
| Depth distributions of armored catfish: predator-induced resource avoidance?Crossref | GoogleScholarGoogle Scholar |
Preen, A. (1995). Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Marine Ecology Progress Series 124, 201–213.
| Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing.Crossref | GoogleScholarGoogle Scholar |
Preen, A. R., Marsh, H., Lawler, I. R., Prince, R. I. T., and Shepherd, R. (1997). Distribution and abundance of dugongs, turtles, dolphins, and other megafauna in Shark Bay, Ningaloo Reef, and Exmouth Gulf, Western Australia. Wildlife Research 24, 185–208.
| Distribution and abundance of dugongs, turtles, dolphins, and other megafauna in Shark Bay, Ningaloo Reef, and Exmouth Gulf, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Preisser, E. L., Bolnick, D. I., and Benard, M. F. (2005). Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86, 501–509.
| Scared to death? The effects of intimidation and consumption in predator-prey interactions.Crossref | GoogleScholarGoogle Scholar |
Preisser, E. L., Orrock, J. L., and Schmitz, O. J. (2007). Predator hunting mode and habitat domain alter nonconsumptive effects in predator-prey interactions. Ecology 88, 2744–2751.
| Predator hunting mode and habitat domain alter nonconsumptive effects in predator-prey interactions.Crossref | GoogleScholarGoogle Scholar |
Ripple, W. J., and Beschta, R. L. (2004). Wolves and the ecology of fear: can predation risk structure ecosystems? Bioscience 54, 755–766.
| Wolves and the ecology of fear: can predation risk structure ecosystems?Crossref | GoogleScholarGoogle Scholar |
Schmitz, O. J. (2008). Effects of predator hunting mode on grassland ecosystem function. Science 319, 952–954.
| Effects of predator hunting mode on grassland ecosystem function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhslOmtrc%3D&md5=3d7a23babc871b041492ed1004ff93b9CAS |
Schmitz, O. J., Beckerman, A. P., and O’Brien, K. M. (1997). Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78, 1388–1399.
| Behaviorally mediated trophic cascades: effects of predation risk on food web interactions.Crossref | GoogleScholarGoogle Scholar |
Schmitz, O. J., Krivan, V., and Ovadia, O. (2004). Trophic cascades: the primacy of trait-mediated indirect interactions. Ecology Letters 7, 153–163.
| Trophic cascades: the primacy of trait-mediated indirect interactions.Crossref | GoogleScholarGoogle Scholar |
Semeniuk, C. A. D., and Dill, L. M. (2005). Cost/benefit analysis of group and solitary resting in the cowtail stingray, Pastinachus sephen. Behavioral Ecology 16, 417–426.
| Cost/benefit analysis of group and solitary resting in the cowtail stingray, Pastinachus sephen.Crossref | GoogleScholarGoogle Scholar |
Semeniuk, C. A. D., and Dill, L. M. (2006). Anti-predator benefits of mixed-species groups of cowtail stingrays (Pastinachus sephen) and whiprays (Himantura uarnak) at rest. Ethology 112, 33–43.
| Anti-predator benefits of mixed-species groups of cowtail stingrays (Pastinachus sephen) and whiprays (Himantura uarnak) at rest.Crossref | GoogleScholarGoogle Scholar |
Sheppard, J. K., Marsh, H., Jones, R. E., and Lawler, I. R. (2010). Dugong habitat use in relation to seagrass nutrients, tides, and diel cycles. Marine Mammal Science 26, 855–879.
| Dugong habitat use in relation to seagrass nutrients, tides, and diel cycles.Crossref | GoogleScholarGoogle Scholar |
Simpfendorfer, C. A. (1992). Biology of tiger sharks (Galeocerdo cuvier) caught by the Queensland shark meshing program off Townsville, Australia. Australian Journal of Marine and Freshwater Research 43, 33–43.
| Biology of tiger sharks (Galeocerdo cuvier) caught by the Queensland shark meshing program off Townsville, Australia.Crossref | GoogleScholarGoogle Scholar |
Simpfendorfer, C. A., Goodreid, A. B., and McAuley, R. B. (2001). Size, sex and geographic variation in the diet of the tiger shark (Galeocerdo cuvier) in Western Australian waters. Environmental Biology of Fishes 61, 37–46.
| Size, sex and geographic variation in the diet of the tiger shark (Galeocerdo cuvier) in Western Australian waters.Crossref | GoogleScholarGoogle Scholar |
Sinclair, A. R. E., and Arcese, P. (1995). Population consequences of predation-sensitive foraging: the Serengeti wildebeest. Ecology 76, 882–891.
Sinclair, A. R. E., and Pech, R. P. (1996). Density dependence, stochasticity, compensation, and regulation. Oikos 75, 164–173.
| Density dependence, stochasticity, compensation, and regulation.Crossref | GoogleScholarGoogle Scholar |
Thomson, J. A., Burkholder, D. A., Heithaus, M. R., and Dill, L. M. (2009). Validation of a rapid visual-assessment technique for categorizing the body condition of green sea turtles (Chelonia mydas) in the field. Copeia 2009, 251–255.
| Validation of a rapid visual-assessment technique for categorizing the body condition of green sea turtles (Chelonia mydas) in the field.Crossref | GoogleScholarGoogle Scholar |
Thomson, J. A., Burkholder, D. A., Cooper, A. B., Heithaus, M. R., and Dill, L. M. (2012). Heterogeneous patterns of availability for detection during visual surveys: spatiotemporal variation in sea turtle dive-surfacing behaviour on a feeding ground. Methods in Ecology and Evolution 3, 378–387.
| Heterogeneous patterns of availability for detection during visual surveys: spatiotemporal variation in sea turtle dive-surfacing behaviour on a feeding ground.Crossref | GoogleScholarGoogle Scholar |
Vaudo, J. J., and Heithaus, M. R. (2009). Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia. Marine Biology 156, 2579–2590.
| Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia.Crossref | GoogleScholarGoogle Scholar |
Walker, D. I., Kendrick, G. A., and McComb, A. J. (1988). The distribution of seagrass species in Shark Bay, Western Australia, with notes on their ecology. Aquatic Botany 30, 305–317.
| The distribution of seagrass species in Shark Bay, Western Australia, with notes on their ecology.Crossref | GoogleScholarGoogle Scholar |
Warner, R. R. (1998). The role of extreme iteroparity and risk avoidance in the evolution of mating systems. Journal of Fish Biology 53, 82–93.
| The role of extreme iteroparity and risk avoidance in the evolution of mating systems.Crossref | GoogleScholarGoogle Scholar |
Waycott, M., Duarte, C. M., Carruthers, T. J. B., Orth, R. J., Dennison, W. C., Olyarnike, S., Calladine, A., Fourqurean, J. W., Heck, K. L., Hughes, A. R., Kendrick, G. A., Kenworthy, W. J., Short, F. T., and Williams, S. L. (2009). Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106, 12 377–12 381.
| Accelerating loss of seagrasses across the globe threatens coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpslGjsbo%3D&md5=7e1510411eb7aca56add4bf0902bc0c6CAS |
Werner, E. E., and Hall, D. J. (1988). Ontogenetic habitat shifts in the bluegill sunfish (Lepomis macrochirus): the foraging rate-predation risk tradeoff. Ecology 69, 1352–1366.
| Ontogenetic habitat shifts in the bluegill sunfish (Lepomis macrochirus): the foraging rate-predation risk tradeoff.Crossref | GoogleScholarGoogle Scholar |
Werner, E. E., and Peacor, S. D. (2003). A review of trait-mediated indirect interactions in ecological communities. Ecology 84, 1083–1100.
| A review of trait-mediated indirect interactions in ecological communities.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., and Heithaus, M. R. (2009). Olive-headed sea snakes (Disteria major) shift seagrass microhabitats to avoid predators. Marine Ecology Progress Series 387, 287–293.
| Olive-headed sea snakes (Disteria major) shift seagrass microhabitats to avoid predators.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., and Heithaus, M. R. (2012). Behavioural transition probabilities in dugongs change with habitat and predator presence: implications for sirenian conservation. Marine and Freshwater Research 63, 1069–1076.
| Behavioural transition probabilities in dugongs change with habitat and predator presence: implications for sirenian conservation.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., and Ripple, W. J. (2011). A comparison of shark and wolf research reveals similar behavioral responses by prey. Frontiers in Ecology and the Environment 9, 335–341.
| A comparison of shark and wolf research reveals similar behavioral responses by prey.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2006). Tiger shark (Galeocerdo cuvier) abundance and growth rates in a subtropical embayment: evidence from seven years of standardized fishing effort. Marine Biology 149, 961–968.
| Tiger shark (Galeocerdo cuvier) abundance and growth rates in a subtropical embayment: evidence from seven years of standardized fishing effort.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007a). Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)? Oecologia 153, 1031–1040.
| Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)?Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007b). Living on the edge: dugongs prefer foraging microhabitats that allow escape rather than avoidance of predators. Animal Behaviour 74, 93–101.
| Living on the edge: dugongs prefer foraging microhabitats that allow escape rather than avoidance of predators.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007c). Can you dig it? Use of excavation, a risky foraging tactic, by dugongs is sensitive to predation danger. Animal Behaviour 74, 1085–1091.
| Can you dig it? Use of excavation, a risky foraging tactic, by dugongs is sensitive to predation danger.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2007d). Can measures of prey availability improve our ability to predict the abundance of large marine predators? Oecologia 153, 563–568.
| Can measures of prey availability improve our ability to predict the abundance of large marine predators?Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., Frid, A., and Dill, L. M. (2008a). Seascapes of fear: methods for evaluating sublethal predator effects experienced and generated by marine mammals. Marine Mammal Science 24, 1–15.
| Seascapes of fear: methods for evaluating sublethal predator effects experienced and generated by marine mammals.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Abernethy, R., and Heithaus, M. R. (2008b). Speed and maneuverability of adult loggerhead turtles (Caretta caretta): do the sexes differ? Journal of Herpetology 42, 411–413.
| Speed and maneuverability of adult loggerhead turtles (Caretta caretta): do the sexes differ?Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Cameron, K. E., and Heithaus, M. R. (2010). Spatial responses to predators vary with prey escape mode. Animal Behaviour 79, 531–537.
| Spatial responses to predators vary with prey escape mode.Crossref | GoogleScholarGoogle Scholar |
Wirsing, A. J., Heithaus, M. R., and Dill, L. M. (2011). Predator-induced modifications to diving behavior vary with foraging mode. Oikos 120, 1005–1012.
| Predator-induced modifications to diving behavior vary with foraging mode.Crossref | GoogleScholarGoogle Scholar |
Yen, P. P. W., Sydeman, W. J., and Hyrenbach, K. D. (2004). Marine bird and cetacean associations with bathymetric habitats and shallow-water topographies: implications for trophic transfer and conservation. Journal of Marine Systems 50, 79–99.
| Marine bird and cetacean associations with bathymetric habitats and shallow-water topographies: implications for trophic transfer and conservation.Crossref | GoogleScholarGoogle Scholar |
