2013, Oceanography 26(3):156–167, http://dx.doi.org/10.5670/oceanog.2013.59
Adam E. Rosenblatt | Florida International University, North Miami, FL, USA
Michael R. Heithaus | Florida International University, North Miami, FL, USA
Martha E. Mather | US Geological Survey, Kansas Cooperative Fish and Wildlife Research Unit, and Kansas State University, Manhattan, KS, USA
Philip Matich | Florida International University, North Miami, FL, USA
James C. Nifong | University of Florida, Gainesville, FL, USA
William J. Ripple | Oregon State University, Corvallis, OR, USA
Brian R. Silliman | University of Florida, Gainesville, FL, USA
During recent human history, human activities such as overhunting and habitat destruction have severely impacted many large top predator populations around the world. Studies from a variety of ecosystems show that loss or diminishment of top predator populations can have serious consequences for population and community dynamics and ecosystem stability. However, there are relatively few studies of the roles of large top predators in coastal ecosystems, so that we do not yet completely understand what could happen to coastal areas if large top predators are extirpated or significantly reduced in number. This lack of knowledge is surprising given that coastal areas around the globe are highly valued and densely populated by humans, and thus coastal large top predator populations frequently come into conflict with coastal human populations. This paper reviews what is known about the ecological roles of large top predators in coastal systems and presents a synthesis of recent work from three coastal eastern US Long Term Ecological Research (LTER) sites where long-term studies reveal what appear to be common themes relating to the roles of large top predators in coastal systems. We discuss three specific themes: (1) large top predators acting as mobile links between disparate habitats, (2) large top predators potentially affecting nutrient and biogeochemical dynamics through localized behaviors, and (3) individual specialization of large top predator behaviors. We also discuss how research within the LTER network has led to enhanced understanding of the ecological roles of coastal large top predators. Highlighting this work is intended to encourage further investigation of the roles of large top predators across diverse coastal aquatic habitats and to better inform researchers and ecosystem managers about the importance of large top predators for coastal ecosystem health and stability.
Rosenblatt, A.E., M.R. Heithaus, M.E. Mather, P. Matich, J.C. Nifong, W.J. Ripple, and B.R. Silliman. 2013. The roles of large top predators in coastal ecosystems: New insights from long term ecological research. Oceanography 26(3):156–167, http://dx.doi.org/10.5670/oceanog.2013.59.
Araujo, M., D.I. Bolnick, G. Machado, A.A. Giaretta, and S.F. dos Reis. 2007. Using δ13C stable isotopes to quantify individual-level diet variation. Oecologia 152:643–654, http://dx.doi.org/10.1007/s00442-007-0687-1.
Bando, K. 2006. The roles of competition and disturbance in a marine invasion. Biological Invasions 8:755–763, http://dx.doi.org/10.1007/s10530-005-3543-4.
Barbier, E., S.D. Hacker, C. Kennedy, E.W. Koch, A.C. Stier, and B.R. Silliman. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81:169–193, http://dx.doi.org/10.1890/10-1510.1.
Beschta, R., and W.J. Ripple. 2009. Large predators and trophic cascades in terrestrial ecosystems of the western United States. Biological Conservation 142:2,401–2,414, http://dx.doi.org/10.1016/j.biocon.2009.06.015.
Binkley, D., M.M. Moore, W.H. Romme, and P.M. Brown. 2006. Was Aldo Leopold right about the Kaibab deer herd? Ecosystems 9:227–241, http://dx.doi.org/10.1007/s10021-005-0100-z.
Bolnick, D., R. Svanback, J.A. Fordyce, L.H. Yang, J.M. Davis, C.D. Husley, and M.L. Forister. 2003. The ecology of individuals: Incidence and implications of individual specialization. The American Naturalist 161:1–28.
Boucek, R., and J.S. Rehage. 2013. No free lunch: Displaced marsh consumers regulate a prey subsidy to an estuarine consumer. Oikos, http://dx.doi.org/10.1111/j.1600-0706.2013.20994.x.
Bruno, J., J.J. Stachowicz, and M.D. Bertness. 2003. Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18:119–125, http://dx.doi.org/10.1016/S0169-5347(02)00045-9.
Burkholder, D.A., M.R. Heithaus, J.W. Fourqurean, A. Wirsing, and L.M. Dill. 2013. Patterns of top-down control in a seagrass ecosystem: Could a roving apex induce a behaviour-mediated trophic cascade? Journal of Animal Ecology, http://dx.doi.org/10.1111/1365-2656.12097.
Campbell, M., and F.J. Mazzotti. 2004. Characterization of natural and artificial alligator holes. Southeastern Naturalist 3:583–594, http://dx.doi.org/10.1656/1528-7092(2004)003[0583:CONAAA]2.0.CO;2.
Childers, D. 2006. A synthesis of long-term research by the Florida Coastal Everglades LTER Program. Hydrobiologia 569:531–544, http://dx.doi.org/10.1007/s10750-006-0154-8.
Childers, D., J.N. Boyer, S.E. Davis, C.J. Madden, D.T. Rudnick, and F.H. Sklar. 2006. Relating precipitation and water management to nutrient concentrations in the oligotrophic ‘‘upside-down’’ estuaries of the Florida Everglades. Limnology and Oceanography 51:602–616, http://dx.doi.org/10.4319/lo.2006.51.1_part_2.0602.
Conrad, J., K.L. Weinersmith, T. Brodin, J.B. Saltz, and A. Sih. 2011. Behavioural syndromes in fishes: A review with implications for ecology and fisheries management. Journal of Fish Biology 78:395–435, http://dx.doi.org/10.1111/j.1095-8649.2010.02874.x.
Coulson, R., and T. Hernandez. 1964. Biochemistry of the Alligator. Louisiana State University Press, Baton Rouge, LA.
Craighead, F. 1968. The role of the alligator in shaping plant communities and maintaining wildlife in the southern Everglades. The Florida Naturalist 41:3–7, 69–74.
Croll, D., J.L. Maron, J.A. Estes, E.M. Danner, and G.V. Byrd. 2005. Introduced predators transform subarctic islands from grassland to tundra. Science 307:1,959–1,961, http://dx.doi.org/10.1126/science.1108485.
Dall, S., A.M. Bell, D.I. Bolnick, and F.L.W. Ratnieks. 2012. An evolutionary ecology of individual differences. Ecology Letters 15:1,189–1,198, http://dx.doi.org/10.1111/j.1461-0248.2012.01846.x.
Darimont, C., P.C. Paquet, and T.E. Reimchen. 2009. Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. Journal of Animal Ecology 78:126–133, http://dx.doi.org/10.1111/j.1365-2656.2008.01473.x.
Estes, J., K. Crooks, and R. Holt. 2001. Predators, ecological role of. Pp. 857–878 in Encyclopedia of Biodiversity, vol. 4. S. Levin, ed., Academic Press, San Diego, CA.
Estes, J., and D.O. Duggins. 1995. Sea otters and kelp forests in Alaska: Generality and variation in a community ecological paradigm. Ecological Monographs 65:75–100, http://dx.doi.org/10.2307/2937159.
Estes, J., M.L. Riedman, M.M. Staedler, M.T. Tinker, and B.E. Lyon. 2003. Individual variation in prey selection by sea otters: Patterns, causes and implications. Journal of Animal Ecology 72:144–155, http://dx.doi.org/10.1046/j.1365-2656.2003.00690.x.
Estes, J., J. Terborgh, J.S. Brashares, M.E. Power, J. Berger, W.J. Bond, S.R. Carpenter, T.E. Essington, R.D. Holt, J.B.C. Jackson, and others. 2011. Trophic downgrading of planet earth. Science 333:301–306, http://dx.doi.org/10.1126/science.1205106.
Estes, J., M.T. Tinker, T.M. Williams, and D.F. Doak. 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473–476, http://dx.doi.org/10.1126/science.282.5388.473.
Ferretti, F., B. Worm, G.L. Britten, M.R. Heithaus, and H.K. Lotze. 2010. Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13:1,055–1,071, http://dx.doi.org/10.1111/j.1461-0248.2010.01489.x.
Fittkau, E. 1970. Role of caimans in the nutrient regime of mouth-lakes of Amazon affluents (an hypothesis). Biotropica 2:138–142.
Fittkau, E. 1973. Crocodiles and the nutrient metabolism of Amazonian waters. Amazoniana 4:103–133.
Goldschmidt, T., F. Witte, and J. Wanink. 1993. Cascading effects of the introduced Nile perch on the detritivorous/phytoplanktivorous species in the sublittoral areas of Lake Victoria. Conservation Biology 7:686–700, http://dx.doi.org/10.1046/j.1523-1739.1993.07030686.x.
Hawlena, D., M.S. Strickland, M.A. Bradford, and O.J. Schmitz. 2012. Fear of predation slows plant-litter decomposition. Science 336:1,434–1,438, http://dx.doi.org/10.1126/science.1220097.
Heithaus, M., G.J. Marshall, B.M. Buhleier, and L.M. Dill. 2001. Employing Crittercam to study habitat use and behavior of large sharks. Marine Ecology Progress Series 209:307–310, http://dx.doi.org/10.3354/meps209307.
Heithaus, M., A.J. Wirsing, and L.M. Dill. 2012. The ecological importance of intact top-predator populations: A synthesis of 15 years of research in a seagrass ecosystem. Marine and Freshwater Research 63:1,039–1,050, http://dx.doi.org/10.1071/MF12024.
Heithaus, M., A.J. Wirsing, J.A. Thomson, and D.A. Burkholder. 2008. A review of lethal and non-lethal effects of predators on adult marine turtles. Journal of Experimental Marine Biology and Ecology 356:43–51, http://dx.doi.org/10.1016/j.jembe.2007.12.013.
Helfield, J., and R.J. Naiman. 2006. Keystone interactions: Salmon and bear in riparian forests of Alaska. Ecosystems 9:167–180, http://dx.doi.org/10.1007/s10021-004-0063-5.
Herbert, D., and J.W. Fourqurean. 2008. Ecosystem structure and function still altered two decades after short-term fertilization of a seagrass meadow. Ecosystems 11:688–700, http://dx.doi.org/10.1007/s10021-008-9151-2.
Holtgrieve, G., and D.E. Schindler. 2011. Marine-derived nutrients, bioturbation, and ecosystem metabolism: Reconsidering the role of salmon in streams. Ecology 92:373–385, http://dx.doi.org/10.1890/09-1694.1.
Imhoff, M., L. Bounoua, T. Ricketts, C. Loucks, R. Harriss, and W.T. Lawrence. 2004. Global patterns in human consumption of net primary production. Nature 429:870–873, http://dx.doi.org/10.1038/nature02619.
Jackson, J., M.X. Kirby, W.H. Berger, K.A. Bjorndal, L.W. Botsford, B.J. Bourque, R.H. Bradbury, R. Cooke, J. Erlandson, J.A. Estes, and others. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638, http://dx.doi.org/10.1126/science.1059199.
Kennedy, C. 2013. Habitat heterogeneity concentrates predators in the seascape: Linking intermediate-scale estuarine habitat to striped bass distribution. MS Thesis, University of Massachusetts, Amherst.
Lancaster, J., M. Dobson, A.M. Magana, A. Arnold, and J.M. Mathooko. 2008. An unusual trophic subsidy and species dominance in a tropical stream. Ecology 89:2,325–2,334, http://dx.doi.org/10.1890/07-0553.1.
Leopold, A. 1943. Deer irruptions. Wisconsin Academy of Sciences, Arts, and Letters 35:351–366.
Maron, J., J.A. Estes, D.A. Croll, E.M. Danner, S.C. Elmendorf, and S.L. Buckelew. 2006. An introduced predator alters Aleutian island plant communities by thwarting nutrient subsidies. Ecological Monographs 76:3–24, http://dx.doi.org/10.1890/05-0496.
Mather, M., J.T. Finn, K.H. Ferry, L.A. Deegan, and G.A. Nelson. 2009. Use of non-natal estuaries by migratory striped bass (Morone saxatilis) in summer. Fishery Bulletin 107:329–338.
Mather, M.E., J.T. Finn, C.G. Kennedy, L.A. Deegan, and J.M. Smith. 2013. What happens in an estuary doesn’t stay there: Patterns of biotic connectivity resulting from long term ecological research. Oceanography 26(3):168–179, http://dx.doi.org/10.5670/oceanog.2013.60.
Mather, M., J.T. Finn, S.M. Pautzke, D. Fox, T. Savoy, H.M. Brundage, L.A. Deegan, and R.M. Muth. 2010. Diversity in destinations, routes and timing of small adult and sub-adult striped bass Morone saxatilis on their southward autumn migration. Journal of Fish Biology 77:2,326–2,337, http://dx.doi.org/10.1111/j.1095-8649.2010.02811.x.
Matich, P., and M.R. Heithaus. 2012. Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas. Marine Ecology Progress Series 447:165–178, http://dx.doi.org/10.3354/meps09497.
Matich, P., and M.R. Heithaus. 2013. Multi-tissue stable isotope analysis and acoustic telemetry reveal seasonal variability in the trophic interactions of juvenile bull sharks in a coastal estuary. Journal of Animal Ecology, http://dx.doi.org/10.1111/1365-2656.12106.
Matich, P., M.R. Heithaus, and C.A. Layman. 2011. Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. Journal of Animal Ecology 80:294–305, http://dx.doi.org/10.1111/j.1365-2656.2010.01753.x.
Meserve, P., D.A. Kelt, W.B. Milstead, and J.R. Gutierrez. 2003. Thirteen years of shifting top-down and bottom-up control. BioScience 53:633–646, http://dx.doi.org/10.1641/0006-3568(2003)053[0633:TYOSTA]2.0.CO;2.
Myers, R., J.K. Baum, T.D. Shepherd, S.P. Powers, and C.H. Peterson. 2007. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1,846–1,850, http://dx.doi.org/10.1126/science.1138657.
Noe, G., D.L. Childers, and R.D. Jones. 2001. Phosphorus biogeochemistry and the impact of phosphorus enrichment: Why is the Everglades so unique? Ecosystems 4:603–624, http://dx.doi.org/10.1007/s10021-001-0032-1.
Ogden, L. 2012. Do animals have personality? BioScience 62:533–537.
Österblom, H., S. Hansson, U. Larsson, O. Hjerne, F. Wulff, R. Elmgren, and C. Folke. 2007. Human-induced trophic cascades and ecological regime shifts in the Baltic Sea. Ecosystems 10:877–889, http://dx.doi.org/10.1007/s10021-007-9069-0.
Pace, M., J.J. Cole, S.R. Carpenter, and J.F. Kitchell. 1999. Trophic cascades revealed in diverse ecosystems. Trends in Ecology and Evolution 14:483–488, http://dx.doi.org/10.1016/S0169-5347(99)01723-1.
Paine, R.T. 1980. Food webs: Linkage, interaction strength and community infrastructure. Journal of Animal Ecology 49:666–685.
Palmer, M., and F.J. Mazzotti. 2004. Structure of Everglades alligator holes. Wetlands 24:115–122, http://dx.doi.org/10.1672/0277-5212(2004)024[0115:SOEAH]2.0.CO;2.
Pautzke, S., M.E. Mather, J.T. Finn, L.A. Deegan, and R.M. Muth. 2010. Seasonal use of a New England estuary by foraging contingents of migratory striped bass. Transactions of the American Fisheries Society 139:257–269, http://dx.doi.org/10.1577/T08-222.1.
Polis, G., W.B. Anderson, and R.D. Holt. 1997. Toward an integration of landscape and food web ecology: The dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28:289–316, http://dx.doi.org/10.1146/annurev.ecolsys.28.1.289.
Polis, G., F. Sanchez-Pinero, P.T. Stapp, W.B. Anderson, and M.D. Rose. 2004. Trophic flows from water to land: Marine input affects food webs of islands and coastal ecosystems worldwide. Pp. 200–216 in Food Webs at the Landscape Level. G. Polis, M.E. Power, and G.R. Huxel, eds, The University of Chicago Press, Chicago, IL.
Power, M. 1992. Top-down and bottom-up forces in food webs: Do plants have primacy? Ecology 73:733–746, http://dx.doi.org/10.2307/1940153.
Reed, D.C., A. Rassweiler, M.H. Carr, K.C. Cavanaugh, D.P. Malone, and D.A. Siegel. 2011. Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests. Ecology 92:2,108–2,116, http://dx.doi.org/10.1890/11-0377.1.
Ripple, W., and R.L. Beschta. 2012. Trophic cascades in Yellowstone: The first 15 years after wolf reintroduction. Biological Conservation 145:205–213, http://dx.doi.org/10.1016/j.biocon.2011.11.005.
Rooney, N., K. McCann, G. Gellner, and J.C. Moore. 2006. Structural asymmetry and the stability of diverse food webs. Nature 442:265–269, http://dx.doi.org/10.1038/nature04887.
Rosenblatt, A.E., and M.R. Heithaus. 2011. Does variation in movement tactics and trophic interactions among American alligators create habitat linkages? Journal of Animal Ecology 80:786–798, http://dx.doi.org/10.1111/j.1365-2656.2011.01830.x.
Rule, S., B.W. Brook, S.G. Haberle, C.S.M. Turney, A.P. Kershaw, and C.N. Johnson. 2012. The aftermath of megafaunal extinction: Ecosystem transformation in Pleistocene Australia. Science 335:1,483–1,486, http://dx.doi.org/10.1126/science.1214261.
Sabo, J., and M.E. Power. 2002. River-watershed exchange: Effects of riverine subsidies on riparian lizards and their terrestrial prey. Ecology 83:1,860–1,869, http://dx.doi.org/10.1890/0012-9658(2002)083[1860:RWEEOR]2.0.CO;2.
Schlesinger, W. 2006. Global change ecology. Trends in Ecology and Evolution 21:348–351, http://dx.doi.org/10.1016/j.tree.2006.03.004.
Schmitz, O. 2003. Top predator control of plant biodiversity and productivity in an old-field ecosystem. Ecology Letters 6:156–163, http://dx.doi.org/10.1046/j.1461-0248.2003.00412.x.
Schmitz, O., D. Hawlena, and G.C. Trussell. 2010. Predator control of ecosystem nutrient dynamics. Ecology Letters 13:1,199–1,209, http://dx.doi.org/10.1111/j.1461-0248.2010.01511.x.
Secor, D., J.R. Rooker, E. Zlokovitz, and V.S. Zdanowicz. 2001. Identification of riverine, estuarine, and coastal contingents of Hudson River striped bass based upon otolith elemental fingerprints. Marine Ecology Progress Series 211:245–253, http://dx.doi.org/10.3354/meps211245.
Sih, A., J. Cote, M. Evans, S. Fogarty, and J. Pruitt. 2012. Ecological implications of behavioural syndromes. Ecology Letters 15:278–289, http://dx.doi.org/10.1111/j.1461-0248.2011.01731.x.
Simard, M., K. Zhang, V.H. Rivera-Monroy, M.S. Ross, P.L. Ruiz, E. Castañeda-Moya, R.R. Twilley, and E. Rodriguez. 2006. Mapping height and biomass of mangrove forests in Everglades National Park with SRTM elevation data. Photogrammetric Engineering & Remote Sensing 72:299–311.
Small, C., and R.J. Nicholls. 2003. A global analysis of human settlement in coastal zones. Journal of Coastal Research 19:584–599.
Sousa, W. 1984. The role of disturbance in natural communities. Annual Review of Ecology and Systematics 15:353–391, http://dx.doi.org/10.1146/annurev.es.15.110184.002033.
Steneck, R., J. Vavrinec, and A.V. Leland. 2004. Accelerating trophic-level dysfunction in kelp forest ecosystems of the western North Atlantic. Ecosystems 7:323–332, http://dx.doi.org/10.1007/s10021-004-0240-6.
Strong, D., and K.T. Frank. 2010. Human involvement in food webs. Annual Review of Environment and Resources 35:1–23, http://dx.doi.org/10.1146/annurev-environ-031809-133103.
Terborgh, J., and J.A. Estes, eds. 2010. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature. Island Press, Washington, DC, 488 pp.
Terborgh, J., L. Lopez, P. Nunez, M. Rao, G. Shahabuddin, G. Orihuela, M. Riveros, R. Ascanio, G.H. Adler, T.D. Lambert, and others. 2001. Ecological meltdown in predator-free forest fragments. Science 294:1,923–1,926, http://dx.doi.org/10.1126/science.1064397.
Turner, M.G. 2010. Disturbance and landscape dynamics in a changing world. Ecology 91:2,833–2,849, http://dx.doi.org/10.1890/10-0097.1.
Vanni, M.J. 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics 33:341–370, http://dx.doi.org/10.1146/annurev.ecolsys.33.010802.150519.
Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, J.W. Fourqurean, K.L. Heck, A.R. Hughes, and others. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106:12,377–12,381, http://dx.doi.org/10.1073/pnas.0905620106.