Skip directly to content

Minimize RSR Award Detail

Research Spending & Results

Award Detail

Awardee:FLORIDA INTERNATIONAL UNIVERSITY
Doing Business As Name:Florida International University
PD/PI:
  • Michael Heithaus
  • (305) 919-5234
  • heithaus@fiu.edu
Award Date:03/21/2008
Estimated Total Award Amount: $ 725,191
Funds Obligated to Date: $ 725,191
  • FY 2011=$133,642
  • FY 2008=$141,433
  • FY 2012=$88,609
  • FY 2009=$182,381
  • FY 2010=$179,126
Start Date:05/01/2008
End Date:04/30/2014
Transaction Type:Grant
Agency:NSF
Awarding Agency Code:4900
Funding Agency Code:4900
CFDA Number:47.050
Primary Program Source:040100 NSF RESEARCH & RELATED ACTIVIT
Award Title or Description:CAREER: Does predator intimidation help structure a pristine seagrass community through multiple indirect pathways?
Federal Award ID Number:0745606
DUNS ID:071298814
Parent DUNS ID:159621697
Program:BIOLOGICAL OCEANOGRAPHY

Awardee Location

Street:11200 SW 8TH ST
City:Miami
State:FL
ZIP:33199-0001
County:Miami
Country:US
Awardee Cong. District:26

Primary Place of Performance

Organization Name:Florida International University
Street:11200 SW 8TH ST
City:Miami
State:FL
ZIP:33199-0001
County:Miami
Country:US
Cong. District:26

Abstract at Time of Award

A recent synthesis suggests that the role of grazing in seagrass ecosystems is generally under-appreciated and that our understanding of these critical marine communities would be greatly enhanced by long-term experimental studies that determine the impact of grazing by multiple guilds, especially megagrazers (green turtles, sirenians) that have declined dramatically in most coastal systems. Furthermore, given the steep declines in populations of marine predators, an understanding of how upper trophic levels structure spatio-temporal patterns of grazer impacts is needed to be able to predict how anthropogenic changes to marine environments will influence seagrass ecosystems. A predictive framework of community ecology in general has been hampered in part because non-lethal effects of predators, both direct and indirect, often are overlooked. Behaviorally mediated indirect species interactions (BMII) occur when a predator causes a change in the behavior of its prey that is transmitted to lower trophic levels. While BMII appear to be important in shaping community dynamics, most studies of BMII have been carried out in small-scale experiments, and have not considered that top predators might initiate multiple BMII that could either attenuate or amplify their indirect effects in natural communities. In this study, Dr. Heithaus will expand on previous investigations on one of the world's most pristine seagrass ecosystems (Shark Bay, Australia) to determine whether multiple BMII initiated by tiger sharks attenuate or amplify their indirect effects on seagrass communities. During previous NSF-funded research, the results show that tiger sharks can indirectly influence seagrass communities through two parallel non-lethal pathways rather than just one. In the first, well-established three-step BMII, tiger sharks cause shifts in megagrazer foraging locations, shielding seagrasses in dangerous microhabitats when sharks are present. In a second possible BMII, tiger sharks cause shifts in piscivore (dolphin, cormorant) microhabitat use that could result in enhanced grazing by herbivorous fishes in the microhabitats that megagrazers have abandoned. Depending on the nature of herbivorous fish interactions with seagrasses, these BMII could result in attenuation or amplification of tiger shark impacts on seagrass communities. In this new award, further monitoring visual and video surveys, experimental herbivory trials, underwater video monitoring, and turtle-borne video cameras will be used to determine whether and how spatiotemporal patterns of grazing vary. Experiments, in the field, will be employed using two types of exclosure and seagrass transplants to determine the relative importance of the BMII initiated by tiger sharks and whether they result in attenuation or amplification of shark effects on seagrass communities. This project will support some of the most comprehensive long-term studies of a relatively pristine community of highly interactive marine species (sharks, turtles, sea cows), extending the datasets to 15 years. This will enable Dr. Heithaus and collaborators to address new questions about how patterns of abundance are influenced by large-scale oceanographic and climatic factors. The project will also develop a broad education and outreach program that is integrated into the research program. This includes: 1) 5th-8th grade biology teacher research experiences in Shark Bay, 2) graduate student interactions with middle school students, 3) talks by graduate students and the PI at schools and regional and national science teacher conferences, 4) the development of lesson plans based on species in Shark Bay, 5) the development of DVDs for use in secondary school classrooms, 6) the development of video labs, 7) video content for National Geographic's online and on-demand channel - NGC Wild, 8) research experiences for undergraduate and graduate students, and 9) the enhancement of an educational website.

Publications Produced as a Result of this Research

Note: When clicking on a Digital Object Identifier (DOI) number, you will be taken to an external site maintained by the publisher. Some full text articles may not yet be available without a charge during the embargo (administrative interval).

Some links on this page may take you to non-federal websites. Their policies may differ from this site.

Heithaus, M. R., A. J. Wirsing, D. Burkholder, J. Thomson, and L. M. Dill. "Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics" Journal of Animal Ecology, v.78, 2009, p.556.

Matich, P; Heithaus, MR; Layman, CA "Size-based variation in intertissue comparisons of stable carbon and nitrogen isotopic signatures of bull sharks (Carcharhinus leucas) and tiger sharks (Galeocerdo cuvier)" CANADIAN JOURNAL OF FISHERIES AND AQUATIC SCIENCES, v.67, 2010, p.877. doi:10.1139/F10-03  View record at Web of Science

Matich, P, Heithaus, MR, Layman, CA "Contrasting patterns of individual specialization and trophic coupling in two marine apex predators" Journal of Animal Ecology, v.80, 2011, p.294.

Vaudo, J. J. and M. R. Heithaus "Dietary niche overlap in a nearshore elasmobranch mesopredator community" Marine Ecology Progress Series, v.425, 2011, p.247.

Olson, E. L., A. K. Salomon, A. J. Wirsing and M. R. Heithaus "Large-scale movement patterns of male loggerhead sea turtles (Caretta caretta) in Shark Bay, Australia" Marine and Freshwater Research, v.63, 2012, p.1108.

Wirsing, A. J. and M. R. Heithaus "Behavioral transition probabilities in dugongs change with habitat and predator presence: implications for sirenian conservation." Marine and Freshwater Research, v.63, 2012, p.1069.

Burkholder, Derek A.; Fourqurean, James W.; Heithaus, Michael 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, v.472, 2013, p.101-115.

Wirsing, AJ; Heithaus, MR "Olive-headed sea snakes Disteria major shift seagrass microhabitats to avoid shark predation" MARINE ECOLOGY-PROGRESS SERIES, v.387, 2009, p.287. doi:10.3354/meps0812  View record at Web of Science

Belicka, Laura L.; Burkholder, Derek; Fourqurean, James W.; Heithaus, Michael R.; Macko, Stephen A.; Jaffe, Rudolf "Stable isotope and fatty acid biomarkers of seagrass, epiphytic, and algal organic matter to consumers in a pristine seagrass ecosystem." MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.1085.

Vaudo, J. J. and M. R. Heithaus "Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia" Marine Biology, v.156, 2009, p.2579.

Wirsing, AJ, Heithaus, MR, Dill, LM "Predator-induced modifications to diving behavior vary with foraging mode" Oikos, v.120, 2011, p.1005.

Heithaus, M. R., T. Alcoverro, R. Arthur, D. A. Burkholder, K. A. Coates, J. A. Christianen, N. Kelkar, W. J. Kenworthy, S. A. Manuel, A. J. Wirsing, and J. W. Fourqurean. "Seagrasses in the age of sea turtle conservation and shark overfishing" Frontiers in Marine Science, v.1, 2014, p.. doi:10.3389/fmars.2014.00028 

Wirsing, Aaron J.; Heithaus, Michael R. "Behavioural transition probabilities in dugongs change with habitat and predator presence: implications for sirenian conservation" MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.1069-1076.

Thomson, JA; Burkholder, D; Heithaus, MR; Dill, LM "Validation of a Rapid Visual-Assessment Technique for Categorizing the Body Condition of Green Turtles (Chelonia mydas) in the Field" COPEIA, v., 2009, p.251. doi:10.1643/CE-07-22  View record at Web of Science

Olson, Erica L.; Salomon, Anne K.; Wirsing, Aaron J.; Heithaus, Michael R. "Large-scale movement patterns of male loggerhead sea turtles (Caretta caretta) in Shark Bay, Australia" MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.1108-1116.

Burkholder, D. A., M. R. Heithaus, and J. A. Fourqurean "Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem." Marine and Freshwater Research, v.63, 2012, p.1051.

Wirsing, A. J. and M. R. Heithaus. "Olive-headed sea snakes (Disteria major) shift seagrass microhabitats to avoid predators" Marine Ecology Progress Series, v.387, 2009, p.287.

Dunphy-Daly, MM, Heithaus, MR, Wirsing, AJ, Mardon, JSF, Burkholder, DA "Predation risk influences the diving behavior of a marine mesopredator" Open Ecology Journal, v.3, 2010, p..

Ferretti, F; Worm, B; Britten, GL; Heithaus, MR; Lotze, HK "Patterns and ecosystem consequences of shark declines in the ocean" ECOLOGY LETTERS, v.13, 2010, p.1055. doi:10.1111/j.1461-0248.2010.01489.  View record at Web of Science

Burkholder, D. A., M. R. Heithaus, J. W. Fourqurean, A. Wirsing, and L. M. Dill. "Patterns of top-down control in a seagrass ecosystem: could a roving apex predator (Galeocerdo cuvier) induce a behavior-mediated trophic cascade?" Journal of Animal Ecology, v.82, 2013, p.1192.

Heithaus, M. R., A. Frid, J. Vaudo, B. Worm, and A. J. Wirsing "Unraveling the ecological importance of elasmobranchs" In Carrier, JC, JA Musick, and MR Heithaus (eds) Sharks and their relatives II: Biodiversity, adaptive physiology, and conservation., v.CRC Pre, 2010, p.608.

Vaudo, J. J. and M. R. Heithaus. "Microhabitat selection by marine mesoconsumers in a thermally heterogeneous habitat: behavioral thermoregulation or avoiding predation risk?" PLos One, v.8, 2013, p.e61907. doi:10.1371/journal.pone.0061907 

Vaudo, JJ; Heithaus, MR "Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia" MARINE BIOLOGY, v.156, 2009, p.2579. doi:10.1007/s00227-009-1282-  View record at Web of Science

Thomson, J. A., A. B. Cooper, D.A. Burkholder, M. R. Heithaus, and L. M. Dill. "Correcting for heterogeneous availability bias in surveys of long-diving marine turtles." Biological Conservation, v.165, 2013, p.154.

Vaudo, J. J. and M. R. Heithaus. "Seasonal and diel variation in the use of nearshore sandflats by five species of rays in a near pristine ecosystem." Marine and Freshwater Research, v.63, 2012, p..

Thomson, J. A., D. A. Burkholder, A. B. Cooper, M. R. Heithaus, and L. M. Dill. "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, v.3, 2012, p.378.

Wirsing, AJ, Cameron, KA, Heithaus, MR "Spatial responses to predators vary with prey escape mode" Animal Behaviour, v.79, 2010, p.531.

Wirsing, AJ, Cameron, KA, Heithaus, MR "Spatial responses to predators vary with prey escape mode" Animal Behaviour, v.79, 2010, p.531.

Thomson, J. A., M. R. Heithaus, and L. M. Dill "Informing the interpretation of dive profiles using animal-borne video: a marine turtle case study" Journal of Experimental Marine Biology and Ecology, v.410, 2011, p.12.

Bessey, C. and M. R. Heithaus "Alarm call production and temporal variation in predator encounter rates for a facultative teleost grazer in a relatively pristine seagrass ecosystem." Journal of Experimental Marine Biology and Ecology, v.449, 2013, p.135.

Burkholder, D. A, J. A. Fourqurean, and M. R. Heithaus "Spatial pattern in seagrass stoichiometry indicates both N-limited and P-limited regions of an iconic P-limited subtropical bay." Marine Ecology Progress Series, v.472, 2013, p.101.

Heithaus, ER, Heithaus, PA, Heithaus, MR, Layman CA, Burkholder, D "Trophic dynamics of a relatively pristine subtropical fringing mangrove community." Marine Ecology Progress Series, v.428, 2011, p.49.

Heithaus, E.R., P. A. Heithaus, M. R. Heithaus, D. Burkholder, and C. A. Layman "Trophic dynamics in a relatively pristine subtropical fringing mangrove community" Marine Ecology Progress Series, v.428, 2011, p.49.

Heithaus, M. R., J. J. Vaudo, S. Kreicker, C. A. Layman, M. Krutzen, D. A. Burkholder, K. Gastrich, C. Bessey, R. Sarabia, K. Cameron, A. Wirsing, J. A. Thomson, and M. M. Dunphy-Daly "Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem." Marine Ecology Progress Series, v.481, 2013, p.225.

Kendrick, G. A., J. W. Fourqurean, M. Fraser, M. R. Heithaus, G. Jackson, K. Friedman, and D. Hallac "Science behind management of Shark Bay and Florida Bay, two P-limited subtropical systems with different climatology and human pressures." Marine and Freshwater Research, v.63, 2012, p.941.

Vaudo JJ, Heithaus MR "Dietary niche overlap in a nearshore elasmobranch mesopredator community." Marine Ecology Progress Series, v.425, 2011, p..

Ferretti, F., B. Worm, G. L. Britten, M. R. Heithaus, H. K. Lotze "Patterns and ecosystem consequences of shark declines in the ocean" Ecology Letters, v.13, 2010, p.1055.

Burkholder, D., M. R. Heithaus, J. Thomson, and J. A Fourqurean "Diversity in trophic interactions of green sea turtles (Chelonia mydas) on a relatively pristine coastal foraging ground" Marine Ecology Progress Series, v.439, 2011, p.277.

Heithaus, MR; Wirsing, AJ; Burkholder, D; Thomson, J; Dill, LM "Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics" JOURNAL OF ANIMAL ECOLOGY, v.78, 2009, p.556. doi:10.1111/j.1365-2656.2008.01512.  View record at Web of Science

Kendrick, Gary A.; Fourqurean, James W.; Fraser, Matthew W.; Heithaus, Michael R.; Jackson, Gary; Friedman, Kim; Hallac, David "Science behind management of Shark Bay and Florida Bay, two P-limited subtropical systems with different climatology and human pressures Introduction" MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.941-951.

Vaudo, Jeremy J.; Heithaus, Michael R. "Diel and seasonal variation in the use of a nearshore sandflat by a ray community in a near pristine system" MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.1077-1084.

Burkholder, Derek A.; Heithaus, Michael R.; Fourqurean, James W. "Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem" MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.1051-1058.

Matich, P., M. R. Heithaus, and C. A. Layman "Size-based inter-tissue comparisons of stable carbon and nitrogen isotope signatures of bull and tiger sharks" Canadian Journal of Fisheries and Aquatic Sciences, v.67, 2010, p.877.

Thomson, J. A. and M. R. Heithaus "Animal-borne video reveals seasonal activity patterns of green sea turtles and the importance of accounting for capture stress in short-term biologging." Journal of Experimental Marine Biology and Ecology, v.450, 2014, p.15.

Dunphy-Daly, M. M., M. R. Heithaus, A. J. Wirsing, J. S. F. Maradon, D. A. Burkholder "Predation risk influences the diving behavior of a marine mesopredator" Open Journal of Ecology, v.3, 2010, p.8.

Wirsing, A. J., K. Cameron, and M. R. Heithaus "Spatial responses to predators vary with prey escape mode" Animal Behavior, v.79, 2010, p.531.

Belicka, L. L., D. Burkholder, J. W. Fourqurean, M.R. Heithaus, S. A. Macko and R. Jaffé. "Stable isotope and fatty acid biomarkers of seagrass, epiphytic, and algal organic matter to consumers in a nearly pristine seagrass ecosystem." Marine and Freshwater Research, v.63, 2012, p.1085-1097.

Belicka, Laura L.; Burkholder, Derek; Fourqurean, James W.; Heithaus, Michael R.; Macko, Stephen A.; Jaffe, Rudolf "Stable isotope and fatty acid biomarkers of seagrass, epiphytic, and algal organic matter to consumers in a pristine seagrass ecosystem" MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.1085-1097.

Vadudo, Jeremy J; Heithaus, Michael R "Microhabitat selection by marine mesoconsumers in a thermally heterogeneous habitat: behavioral thermoregulation or avoiding predation risk?" PLos One, v.8, 2013, p.e61907. doi:10.1371/journal.pone.0061907 

Wirsing, A. J., M. R. Heithaus, and L.M. Dill "Predator-induced modifications to diving behavior vary with foraging mode" Oikos, v.120, 2011, p.1005.

Thomson, J. A., M. R. Heithaus, D. A. Burkholder, J. J. Vaudo, A. J. Wirsing, and L. M. Dill. "Site specialists, diet generalists? Isotopic variation, site fidelity and foraging by loggerhead turtles in Shark Bay, Western Australia." Marine Ecology Progress Series, v.453, 2012, p.213.

Burkholder, D, Heithaus MR, Thomson JA, Fourqurean JF "Diversity in trophic interactions of green sea turtles (Chelonia mydas) on a relatively pristine coastal foraging ground." Marine Ecology Progress Series, v.439, 2012, p.277.

Matich, P., M. R. Heithaus, and C. A. Layman "Contrasting patterns of individual specialization and trophic coupling in two marine apex predators." Journal of Animal Ecology, v.80, 2011, p.294.

Thomson, Jordan A.; Cooper, Andrew B.; Burkholder, Derek A.; Heithaus, Michael R.; Dill, Lawrence M. "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, v.3, 2012, p.378-387.

Wirsing, A. J. and M. R. Heithaus "Accounting for individual behavioral variation in studies of habitat selection." Journal of Animal Ecology, v.83, 2014, p.319.

Heithaus, M. R., A. J. Wirsing, and L. M. Dill "The ecological importance of intact top predator populations: a synthesis of 15 years of research in a seagrass ecosystem" Marine and Freshwater Research, v.63, 2012, p.1039.

Thomson, Jordan A.; Heithaus, Michael R.; Burkholder, Derek A.; Vaudo, Jeremy J.; Wirsing, Aaron J.; Dill, Lawrence M. "Site specialists, diet generalists? Isotopic variation, site fidelity, and foraging by loggerhead turtles in Shark Bay, Western Australia" MARINE ECOLOGY PROGRESS SERIES, v.453, 2012, p.213-226.

Heithaus, Michael. R.; Wirsing, A. J.; Dill, L. M. "The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem" MARINE AND FRESHWATER RESEARCH, v.63, 2012, p.1039-1050.


Project Outcomes Report

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Intellectual Merit

Since 1997, the Shark Bay Ecosystem Research Project of Florida International University has investigated the ecological importance of marine top predators.  During this award, we were able to use a combination of ecosystem-scale surveys, manipulative experiments, and long-term behavioral observations across a range of environmental conditions to show that tiger sharks play a critical role in structuring Shark Bay’s relatively pristine seagrass ecosystem.  Interestingly, tiger sharks play this role not by consuming large numbers of prey, but instead by modifying the behavior of key prey species – especially large plant-eaters like sea turtles and sea cows (dugongs) and fish-eating dolphins and cormorants.  When large tiger sharks are abundant (most of the year and in most years) their prey avoid dangerous shallow seagrass habitats and spend more time in safer deeper habitats.  This results in high herbivory on seagrasses, including destructive removal of seagrass stems by dugongs, in deeper waters.  In contrast, in shallower waters that are preferred by tiger sharks, destructive grazing by large plant-eaters is limited.   Fish-eating dolphins and comorants also avoid tiger sharks, and since many of the fish that they eat in turn consume seagrasses, fish grazing of their preferred seagrass species is higher in the habitats that dolphins and comorants avoid because of tiger sharks.  The net result of these “behavioral cascades” is that the presence of tiger sharks promotes the existence of dense, valuable seagrass meadows in dangerous shallow habitats and heavily grazed low-biomass seagrass beds in safer habitats.   By extension, the loss of tiger sharks would likely result in substantial losses of ecosystem services due to unrestricted grazing by herbivores no longer constrained by predation risk.

 

In the final year of our work, Shark Bay experienced a ‘marine heatwave’ that resulted in massive (>80%) declines in the foundational seagrass species.  Based on our past work and opportunistic field experiments, we are determining whether tiger sharks, through their influence on the behavior of their prey, help determine the way that Shark Bay’s seagrasses recover from the heatwave.

 

Overall, our NSF-funded work in Shark Bay has provided the most in-depth empirical investigation of the ecological role and importance of large sharks in coastal ecosystems and suggests that ongoing declines in these species may trigger trophic cascades with detrimental impacts to ecosystem structure and function, including the ability of ecosystems to sequester carbon (“blue carbon”).  Importantly, these impacts may operate largely through anti-predator behavior of prey rather than death rates inflicted by predators- suggesting that traditional ecological models may underestimate the effects of top predator declines in the oceans and on land. When viewed in light of changes in other ecosystems, where sharks have declined and their prey (sea turtles) have been protected, it is now apparent that restoration of large shark populations should be a management priority. 

 

Broader Impacts

This project has produced substantial broader impacts.  We developed a comprehensive project website (sberp.org) that provides details on our research methods, projects, and results, species fact sheets, image and video galleries, and teacher resources.  Video vignettes and clips are disseminated through the website, a YouTube Channel, and Heithaus lab blog (heithauslab.blogspot.com).  Perhaps most importantly, we developed a new style for using high production-quality video and science-based activities for use in K-12 classrooms.  These “video-based projects...

For specific questions or comments about this information including the NSF Project Outcomes Report, contact us.