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The Role of Consumers in Structuring Seagrass Communities: Direct and Indirect Mechanisms

  • Robert J. Nowicki
  • James W. Fourqurean
  • Michael R. Heithaus
Chapter

Abstract

Seagrass ecosystems were traditionally assumed to be structured by competition as well as by “bottom up forces” such as resource availability and disturbance. However, a wealth of new evidence demonstrates that exertion of “top down control” by animals may be widespread. The strength and direction of top down control is context dependent, however, and varies with properties of organisms, the community, and the physical environment. Consumers can facilitate, consume, or destroy primary producers, aid or inhibit seagrass reproduction, or alter bottom up processes with implications for the properties and persistence of seagrass ecosystems. Studies in Australian ecosystems have been critical in helping to elucidate the role of consumers in seagrass ecosystems. Specifically, work investigating the roles of megaherbivores and apex predators and the pioneering of novel experimental approaches which allow for cage-free manipulations of mesograzers have substantially furthered our understanding of top-down control. At the broadest scale, megagrazers are likely to dominate grazing pathways in Australian tropical and subtropical seagrass ecosystems, while macrograzers and mesograzers do so in temperate seagrass ecosystems. However, while we have learned much about mechanisms through which top-down control can operate and its effects on seagrass ecosystems, predicting which grazing pathways dominate at smaller spatial scales, and net herbivore effects on seagrasses in specific ecosystems remains challenging due to context dependence and the highly complex nature of species interactions. Anthropogenic impacts further complicate these relationships. Australian seagrass habitats possess unusual properties, including relatively intact populations of megafauna, remote and pristine locations, and distinctive oceanographic features which allow these habitats to provide unique insights of top down control in seagrass ecosystems.

Notes

Acknowledgements

The authors would like to thank the editors for their invitation to write this chapter, and R. Sarabia for comments on an early copy of the manuscript. Financial support for RN was provided by Florida International University and by NSF GRF No. DGE-1038321. This is contribution number 81 from the Shark Bay Ecosystem Research Project (SBERP) and contribution number 12 from the Marine Education and Research Center (MERC) in the Institute for Water and the Environment at Florida International University.

References

  1. Agostini S, Desjobert J-M, Pergent G (1998) Distribution of phenolic compounds in the seagrass Posidonia oceanica. Phytochemistry 48:611–617CrossRefGoogle Scholar
  2. Alcoverro T, Duarte CM, Romero J (1997) The influence of herbivores on Posidonia oceanica epiphytes. Aquat Bot 56:93–104CrossRefGoogle Scholar
  3. Allgeier JE, Yeager LA, Layman CA (2013) Consumers regulate nutrient limitation regimes and primary production in seagrass ecosystems. Ecology 94:521–529PubMedCrossRefPubMedCentralGoogle Scholar
  4. Anderson PK (1986) Dugongs of Shark Bay, Australia-seasonal migration, water temperature, and forage. Natl Geogr Res 2:473–490Google Scholar
  5. André J, Gyuris E, Lawler IR (2005) Comparison of the diets of sympatric dugongs and green turtles on the Orman Reefs, Torres Strait, Australia. Wildl Res 32:53–62Google Scholar
  6. Aragones L, Marsh H (2000) Impact of dugong grazing and turtle cropping on tropical seagrass communities. Pacific Conserv Biol 5:277–288CrossRefGoogle Scholar
  7. Archer SK, Stoner EW, Layman CA (2015) A complex interaction between a sponge (Halichondria melanadocia) and a seagrass (Thalassia testudinum) in a subtropical coastal ecosystem. J Exp Mar Biol Ecol 465:33–40CrossRefGoogle Scholar
  8. Armitage AR, Fourqurean JW (2006) The short-term influence of herbivory near patch reefs varies between seagrass species. J Exp Mar Biol Ecol 339:65–74CrossRefGoogle Scholar
  9. Atwood TB, Connolly RM, Ritchie EG, Lovelock CE, Heithaus MR, Hays GC, Fourqurean JW, Macreadie PI (2015) Predators help protect carbon stocks in blue carbon ecosystems. Nat Clim Change 5:1038–1045CrossRefGoogle Scholar
  10. Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 91:2811–2818PubMedCrossRefPubMedCentralGoogle Scholar
  11. Baum JK, Myers RA, Kehler DG, Worm B, Harley SJ, Doherty PA (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299:389–392PubMedCrossRefPubMedCentralGoogle Scholar
  12. Belicka LL, Burkholder D, Fourqurean JW, Heithaus MR, Macko SA, Jaffé R (2012) Stable isotope and fatty acid biomarkers of seagrass, epiphytic, and algal organic matter to consumers in a pristine seagrass ecosystem. Mar Freshw Res 63:1085–1097CrossRefGoogle Scholar
  13. Bennett S, Wernberg T, Harvey ES, Santana-Garcon J, Saunders BJ (2015) Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. Ecol Lett 18:714–723Google Scholar
  14. Bessey C, Heithaus MR (2013) Alarm call production and temporal variation in predator encounter rates for a facultative teleost grazer in a relatively pristine seagrass ecosystem. J Exp Mar Biol Ecol 449:135–141CrossRefGoogle Scholar
  15. Bessey C, Heithaus MR (2015) Ecological niche of an abundant teleost, Pelates octolineatus, in a subtropical seagrass ecosystem. Mar Ecol Prog Ser 541:195–204CrossRefGoogle Scholar
  16. Bessey C, Heithaus MR, Fourqurean JW, Gastrich KR, Burkholder DA (2016) Importance of teleost macrograzers to seagrass composition in a subtropical ecosystem with abundant populations of megagrazers and predators. Mar Ecol Prog Ser 553:81–92CrossRefGoogle Scholar
  17. Blaber SJM, Wassenberg TJ (1989) Feeding ecology of the piscivorous birds Phalacrocorax varius, P. melanoleucos and Sterna bergii in Moreton Bay, Australia: diets and dependence on trawler discards. Mar Biol 101:1–10CrossRefGoogle Scholar
  18. Borer ET, Seabloom EW, Shurin JB, Anderson KE, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2005) What determines the strength of a trophic cascade? Ecology 86:528–537CrossRefGoogle Scholar
  19. Borum J, Sand-Jensen K, Binzer T, Pedersen O, Greve TM (2007) Oxygen movement in seagrasses. In: Seagrasses: biology, ecology, and conservation. Springer, Netherlands, pp 255–270Google Scholar
  20. Borum J, Gruber RK, Kemp WM (2012) Seagrass and related submersed vascular plants. In: Estuarine ecology, 2nd edn, pp 111–127Google Scholar
  21. Borum J, Pedersen O, Kotula L, Fraser MW, Statton J, Colmer TD, Kendrick GA (2015) Photosynthetic response to globally increasing CO2 of co-occurring temperate seagrass species. Plant Cell EnvironGoogle Scholar
  22. Brand-Gardner SJ, Limpus CJ, Lanyon JM (1999) Diet selection by immature green turtles, Chelonia mydas, in subtropical Moreton Bay, south-east Queensland. Aust J Zool 47:181–191CrossRefGoogle Scholar
  23. Brearley A, Walker DI (1995) Isopod miners in the leaves of two Western Australian Posidonia species. Aquat Bot 52:163–181CrossRefGoogle Scholar
  24. Brearley A, Kendrick GA, Walker DI (2008) How does burrowing by the isopod Limnoria agrostisa (Crustacea: Limnoriidae) affect the leaf canopy of the southern Australian seagrass Amphibolis griffithii? Mar Biol 156:65–77CrossRefGoogle Scholar
  25. Brodeur MC, Piehler MF, Fodrie FJ (2015) Consumers mitigate heat stress and nutrient enrichment effects on eelgrass Zostera marina communities at its southern range limit. Mar Ecol Prog Ser 525:53–64CrossRefGoogle Scholar
  26. Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014CrossRefGoogle Scholar
  27. Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399CrossRefGoogle Scholar
  28. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  29. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: Context-dependent effects. Ecol 87:3128–3139Google Scholar
  30. Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Nat Acad Sci 105:16201–16206Google Scholar
  31. Burkholder DA, Heithaus MR, Fourqurean JW (2012) Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem. Mar Freshw Res 63:1051–1058CrossRefGoogle Scholar
  32. Burkholder DA, Heithaus MR, Fourqurean JW, Wirsing A, Dill LM (2013) Patterns of top-down control in a seagrass ecosystem: could a roving apex predator induce a behaviour-mediated trophic cascade? J Anim Ecol 82:1192–1202PubMedCrossRefPubMedCentralGoogle Scholar
  33. Burnell OW, Connell SD, Irving AD, Russell BD (2013a) Asymmetric patterns of recovery in two habitat forming seagrass species following simulated overgrazing by urchins. J Exp Mar Biol Ecol 448:114–120CrossRefGoogle Scholar
  34. Burnell OW, Russell BD, Irving AD, Connell SD (2013b) Eutrophication offsets increased sea urchin grazing on seagrass caused by ocean warming and acidification. Mar Ecol Prog Ser 485:37–46CrossRefGoogle Scholar
  35. Campbell JE, Fourqurean JW (2013) Effects of in situ CO2 enrichment on the structural and chemical characteristics of the seagrass Thalassia testudinum. Mar Biol 160:1465–1475CrossRefGoogle Scholar
  36. Carr LA, Boyer KE (2014) Variation at multiple trophic levels mediates a novel seagrass-grazer interaction. Mar Ecol Progr 508:117–128CrossRefGoogle Scholar
  37. Carr LA, Bruno JF (2013) Warming increases the top-down effects and metabolism of a subtidal herbivore. PeerJ 1:e109PubMedPubMedCentralCrossRefGoogle Scholar
  38. Cebrián J, Duarte CM (1998) Patterns in leaf herbivory on seagrasses. Aquat Bot 60:67–82CrossRefGoogle Scholar
  39. Cebrián J, Duarte CM, Agawin, NSR, Merino M (1998) Leaf growth response to simulated herbivory: a comparison among seagrass species. J Exp Mar Biol Ecol 220:67–81Google Scholar
  40. Cheung WW, Lam VW, Sarmiento JL, Kearney K, Watson R, Pauly D (2009) Projecting global marine biodiversity impacts under climate change scenarios. Fish Fish 10:235–251CrossRefGoogle Scholar
  41. Christianen MJ, Govers LL, Bouma TJ, Kiswara W, Roelofs JG, Lamers LP, van Katwijk MM (2012) Marine megaherbivore grazing may increase seagrass tolerance to high nutrient loads. J Ecol 100:546–560CrossRefGoogle Scholar
  42. Christianen MJ, Herman PM, Bouma TJ, Lamers LP, van Katwijk MM, van der Heide T et al (2014) Habitat collapse due to overgrazing threatens turtle conservation in marine protected areas. Proc R Soc Lond B Biol Sci 281:20132890CrossRefGoogle Scholar
  43. Cook K, Vanderklift MA, Poore AG (2011) Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow. Mar Ecol Prog Ser 442:263–269CrossRefGoogle Scholar
  44. Creel S, Christianson D, Liley S, Winnie JA (2007) Predation risk affects reproductive physiology and demography of elk. Science 315:960 960PubMedCrossRefGoogle Scholar
  45. Cruz-Rivera E, Hay M (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar Ecol Prog Ser 218:249–266CrossRefGoogle Scholar
  46. Davis RC, Short FT, Burdick DM (1998) Quantifying the effects of green crab damage to eelgrass transplants. Restor Ecol 6:297–302Google Scholar
  47. Dayton PK, Thrush SF, Agardy MT, Hofman RJ (1995) Environmental effects of marine fishing. Aquat Conserv Mar Freshw Ecosyst 5:205–232CrossRefGoogle Scholar
  48. De los Santos CB, Brun FG, Onoda Y, Cambridge ML, Bouma TJ, Vergara JJ, Pérez-Lloréns JL (2012) Leaf-fracture properties correlated with nutritional traits in nine Australian seagrass species: implications for susceptibility to herbivory. Mar Ecol Prog Ser 458Google Scholar
  49. del Hoyo J, Elliott A, Sargatal J (1992) Handbook of the birds of the world, vol 1. Ostrich to ducks. Lynx Edicions, Barcelona. ISBN 84-87334-10-5Google Scholar
  50. Dennison WC, Orth RJ, Moore KA, Stevenson JC, Carter V, Kollar S, Bergstrom PW, Batiuk RA (1993) Assessing water quality with submersed aquatic vegetation. BioScience 86–94Google Scholar
  51. Dewsbury BM, Fourqurean JW (2010) Artificial reefs concentrate nutrients and alter benthic community structure in an oligotrophic, subtropical estuary. Bull Mar Sci 86:813–829CrossRefGoogle Scholar
  52. Dill LM, Heithaus MR, Walters CJ (2003) Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84:1151–1157CrossRefGoogle Scholar
  53. Domning D (2001) Sirenians, seagrasses, and Cenozoic ecological change in the Caribbean. Palaeogeogr Paleoclimatol Paleoecol 166:27–50CrossRefGoogle Scholar
  54. Duarte CM (1999) Seagrass ecology at the turn of the millennium: challenges for the new century. Aquat Bot 65:7–20CrossRefGoogle Scholar
  55. Duffy JE, Harvilicz AM (2001) Species-specific impacts of grazing amphipods in an eelgrass-bed community. Mar Ecol Prog Ser 223:201–211CrossRefGoogle Scholar
  56. Duffy JE, Macdonald KS, Rhode JM, Parker JD (2001) Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology 82:2417–2434CrossRefGoogle Scholar
  57. Duffy J, Richardson J, Canuel E (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6:637–645CrossRefGoogle Scholar
  58. Duffy JE, Paul Richardson J, France KE (2005) Ecosystem consequences of diversity depend on food chain length in estuarine vegetation. Ecol Lett 8:301–309CrossRefGoogle Scholar
  59. Duffy JE, Moksnes PI, Hughes AR (2013) Ecology of Seagrass Communities. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) Marine community ecology and conservation. Sinauer Associates, Sunderland, pp 271–297Google Scholar
  60. Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LN, Fordham SV, Francis MP et al (2014) Extinction risk and conservation of the world’s sharks and rays. eLife Sci 3:e00590Google Scholar
  61. Ebrahim A, Olds AD, Maxwell PS, Pitt KA, Burfeind DD, Connolly RM (2014) Herbivory in a subtropical seagrass ecosystem: separating the functional role of different grazers. Mar Ecol Prog Ser 511:83–91CrossRefGoogle Scholar
  62. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 586–608Google Scholar
  63. Eklöf JS, De la Torre-Castro M, Gullström M, Uku J, Muthiga N, Lyimo T, Bandeira SO (2008) Sea urchin overgrazing of seagrasses: a review of current knowledge on causes, consequences, and management. Estuar Coast Shelf Sci 79:569–580CrossRefGoogle Scholar
  64. Eklöf JS, McMahon K, Lavery PS (2010) Effects of multiple disturbances in seagrass meadows: shading decreases resilience to grazing. Mar Freshw Res 60:1317–1327CrossRefGoogle Scholar
  65. Eklöf JS, Alsterberg C, Havenhand JN, Sundbäck K, Wood HL, Gamfeldt L (2012) Experimental climate change weakens the insurance effect of biodiversity. Ecol Lett 15:864–872PubMedCrossRefGoogle Scholar
  66. Elton CS (1927) Anim ecol. University of Chicago PressGoogle Scholar
  67. Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071PubMedGoogle Scholar
  68. Ferreira LC, Thums M, Meeuwig JJ, Vianna GM, Stevens J, McAuley R, et al. (2015) Crossing latitudes—long-distance tracking of an apex predator. PLoS One 10:e0116916Google Scholar
  69. Fodrie F, Heck KL, Powers SP, Graham WM, Robinson KL (2010) Climate-related, decadal-scale assemblage changes of seagrass-associated fishes in the northern Gulf of Mexico. Glob Change Biol 16:48–59Google Scholar
  70. Fourqurean JW, Powell GV, Kenworthy WJ, Zieman JC (1995) The effects of long-term manipulation of nutrient supply on competition between the seagrasses Thalassia testudinum and Halodule wrightii in Florida Bay. Oikos 349–358Google Scholar
  71. Fourqurean JW, Moore TO, Fry B, Hollibaugh JT (1997) Spatial and temporal variation in C: N: P ratios, δ15N, and δ13C of eelgrass Zostera marina as indicators of ecosystem processes, Tomales Bay, California, USA. Mar Ecol Prog Ser 157:147–157CrossRefGoogle Scholar
  72. Fourqurean JW, Escorcia SP, Anderson WT, Zieman JC (2005) Spatial and seasonal variability in elemental content, δ13C, and δ15N of Thalassia testudinum from South Florida and its implications for ecosystem studies. Estuaries 28:447–461CrossRefGoogle Scholar
  73. Fourqurean JW, Marbà N, Duarte CM, Díaz-Almela E, Ruiz-Halpern S (2007) Spatial and temporal variation in the elemental and stable isotopic content of the seagrasses Posidonia oceanica and Cymodocea nodosa from the Illes Balears, Spain. Mar Biol 151:219–232CrossRefGoogle Scholar
  74. Fourqurean JW, Duarte CM, Kennedy H, Marbà N, Holmer M, Mateo MA, Apostolaki ET, Kendrick GA, Krause-Jensen D, McGlathery KJ et al (2012) Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5:505–509CrossRefGoogle Scholar
  75. Fourqurean JW, Manuel SA, Coates KA, Kenworthy WJ, Boyer JN (2015) Water quality, isoscapes and stoichioscapes of seagrasses indicate general P limitation and unique N cycling in shallow water benthos of Bermuda. Biogeosciences 12:6235–6249CrossRefGoogle Scholar
  76. Fraser MW, Kendrick GA, Statton J, Hovey RK, Zavala-Perez A, Walker DI (2014) Extreme climate events lower resilience of foundation seagrass at edge of biogeographical range. J Ecol 102:1528–1536CrossRefGoogle Scholar
  77. Garthwin RG, Poore AGB, Vergés A (2014) Seagrass tolerance to herbivory under increased ocean temperatures. Mar Pollut Bull 83:475–482PubMedCrossRefPubMedCentralGoogle Scholar
  78. Ghedini G, Russell BD, Connell SD (2015) Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances. Ecol Lett 18:182–187PubMedCrossRefPubMedCentralGoogle Scholar
  79. Goecker ME, Heck KL Jr, Valentine JF (2005) Effects of nitrogen concentrations in turtlegrass Thalassia testudinum on consumption by the bucktooth parrotfish Sparisoma radians. Mar Ecol Prog Ser 286:239–248CrossRefGoogle Scholar
  80. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 421–425Google Scholar
  81. Hay ME (1986) Associational plant defenses and the maintenance of species diversity: turning competitors into accomplices. Am Nat 617–641Google Scholar
  82. Hays CG (2005) Effect of nutrient availability, grazer assemblage and seagrass source population on the interaction between Thalassia testudinum (turtle grass) and its algal epiphytes. J Exp Mar Biol Ecol 314:53–68CrossRefGoogle Scholar
  83. Heck KL Jr, Hays G, Orth RJ (2003) Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar Ecol Prog Ser 253:123–136CrossRefGoogle Scholar
  84. Heck KL, Valentine JF (1995) Sea urchin herbivory: evidence for long-lasting effects in subtropical seagrass meadows. J Exp Mar Biol Ecol 189:205–217CrossRefGoogle Scholar
  85. Heck KL, Valentine JF (2006) Plant–herbivore interactions in seagrass meadows. J Exp Mar Biol Ecol 330:420–436CrossRefGoogle Scholar
  86. Heck KL, Valentine JF (2007) The primacy of top-down effects in shallow benthic ecosystems. Estuaries Coasts 30:371–381CrossRefGoogle Scholar
  87. Heck KL, Pennock JR, Valentine JF, Coen LD, Sklenar SA (2000) Effects of nutrient enrichment and small predator density on seagrass ecosystems: an experimental assessment. Limnol Oceanogr 45:1041–1057CrossRefGoogle Scholar
  88. Heck KL Jr, Fodrie FJ, Madsen S, Baillie CJ, Byron DA (2015) Seagrass consumption by native and a tropically associated fish species: potential impacts of the tropicalization of the northern Gulf of Mexico. Mar Ecol Prog Ser 520:165–173Google Scholar
  89. Heithaus MR (2004) Fish communities of subtropical seagrass meadows and associated habitats in Shark Bay, Western Australia. Bull Mar Sci 75:79–99Google Scholar
  90. 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 147:27–35CrossRefGoogle Scholar
  91. Heithaus MR (2013) Predators, prey, and ecological roles of sea turtles. In: Wyneken JJ, Lohman K, Musick JA (eds) Biology of sea turtlesGoogle Scholar
  92. Heithaus MR, Dill LM (2002) Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology 83:480–491CrossRefGoogle Scholar
  93. Heithaus M, Dill L (2006) Does tiger shark predation risk influence foraging habitat use by bottlenose dolphins at multiple spatial scales? Oikos 114:257–264CrossRefGoogle Scholar
  94. 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 76:837–844PubMedCrossRefPubMedCentralGoogle Scholar
  95. Heithaus MR, Wirsing AJ, Thomson JA, Burkholder DA (2008a) A review of lethal and non-lethal effects of predators on adult marine turtles. J Exp Mar Biol Ecol 356:43–51CrossRefGoogle Scholar
  96. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008b) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210PubMedCrossRefPubMedCentralGoogle Scholar
  97. Heithaus MR, Wirsing AJ, Dill LM (2012) The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem. Mar Freshw Res 63:1039–1050CrossRefGoogle Scholar
  98. Heithaus MR, Alcoverro T, Arthur R, Burkholder DA, Coates KA, Christianen MJ, Kelkar N, Manuel SA, Wirsing AJ, Kenworthy WJ et al (2014) Seagrasses in the age of sea turtle conservation and shark overfishing. Front Mar Sci 1:28CrossRefGoogle Scholar
  99. Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009) Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. J Anim Ecol 78:556–562Google Scholar
  100. Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University PressGoogle Scholar
  101. Hillebrand H, Borer ET, Bracken ME, Cardinale BJ, Cebrian J, Cleland EE, Elser JJ, Gruner DS, Stanley Harpole W, Ngai JT et al (2009) Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems. Ecol Lett 12:516–527PubMedCrossRefPubMedCentralGoogle Scholar
  102. Holbrook SJ, Reed DC, Hansen K, Blanchette CA (2000) Spatial and temporal patterns of predation on seeds of the surfgrass Phyllospadix torreyi. Mar Biol 136:739–747CrossRefGoogle Scholar
  103. Holmes BJ, Pepperell JG, Griffiths SP, Jaine FR, Tibbetts IR Bennett MB (2014) Tiger shark (Galeocerdo cuvier) movement patterns and habitat use determined by satellite tagging in eastern Australian waters. Mar biol 161, 2645–2658Google Scholar
  104. Holzer KK, Rueda JL, McGlathery KJ (2011) Differences in the feeding ecology of two seagrass-associated snails. Estuaries Coasts 34:1140–1149CrossRefGoogle Scholar
  105. Hughes ARR, Bando KJ, Rodriguez LF, Williams SL (2004) Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Mar Ecol Prog Ser 282Google Scholar
  106. Humphries P, Hyndes GA, Potter IC (1992) Comparisons between the diets of distant taxa (teleost and cormorant) in an Australian estuary. Estuaries 15:327–334CrossRefGoogle Scholar
  107. Jackson JB (2001) What was natural in the coastal oceans? Proc Natl Acad Sci 98:5411–5418PubMedCrossRefPubMedCentralGoogle Scholar
  108. Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA et al (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637PubMedCrossRefPubMedCentralGoogle Scholar
  109. Jernakoff P, Nielsen J (1997) The relative importance of amphipod and gastropod grazers in Posidonia sinuosa meadows. Aquat Bot 56:183–202CrossRefGoogle Scholar
  110. Kelkar N, Arthur R, Marbà N, Alcoverro T (2013) Greener pastures? High-density feeding aggregations of green turtles precipitate species shifts in seagrass meadows. J Ecol 101:1158–1168CrossRefGoogle Scholar
  111. Kendrick GA, Aylward MJ, Hegge BJ, Cambridge ML, Hillman K, Wyllie A, Lord DA (2002) Changes in seagrass coverage in Cockburn Sound, Western Australia between 1967 and 1999. Aquat Bot 73:75–87CrossRefGoogle Scholar
  112. Keuskamp D (2004) Limited effects of grazer exclusion on the epiphytes of Posidonia sinuosa in South Australia. Aquat Bot 78:3–14Google Scholar
  113. Kirkman H, Reid DD (1979) A study of the role of the seagrass Posidonia australis in the carbon budget of an estuary. Aquat Bot 7:173–183CrossRefGoogle Scholar
  114. Kirsch KD, Valentine JF, Heck KL (2002) Parrotfish grazing on turtlegrass Thalassia testudinum: evidence for the importance of seagrass consumption in food web dynamics of the Florida Keys National Marine Sanctuary. Mar Ecol Prog Ser 227:71–85CrossRefGoogle Scholar
  115. Klumpp D, Howard R, Pollard D (1989) Trophodynamics and nutritional ecology of seagrass communities (Chap. 13, pp 394–457). In: Larkum A, McComb A (eds) The Larkrum book. In: Biology of seagrasses: a treatise on the biology of seagrasses with special reference to the Australian Region. Elsevier, Amsterdam, pp 394–457Google Scholar
  116. Kordas RL, Harley CDG, O’Connor MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Biol Ecol 400:218–226CrossRefGoogle Scholar
  117. Lanyon J, Limpus C, Marsh H (1989) Dugongs and turtles: grazers in the seagrass ecosystem. In: Biology of seagrasses. Elsevier, Amsterdam, pp 610–634Google Scholar
  118. Larkum AWD, West RJ (1990) Long-term changes of seagrass meadows in Botany Bay, Australia. Aquat Bot 37:55–70CrossRefGoogle Scholar
  119. Last PR, White WT, Gledhill DC, Hobday AJ, Brown R, Edgar GJ, Pecl G (2011) Long-term shifts in abundance and distribution of a temperate fish fauna: a response to climate change and fishing practices. Glob Ecol Biogeogr 20:58–72CrossRefGoogle Scholar
  120. Lavery TJ, Roudnew B, Mitchell JG (2015) Nitrogen transport from sea to land by a threatened and declining population of Australian sea lions (Neophoca cinerea) on Kangaroo Island, South Australia. Aust mammal 37:92–96Google Scholar
  121. Lee C-L, Huang Y-H, Chung C-Y, Hsiao S-C, Lin H-J (2015) Herbivory in multi-species, tropical seagrass beds. MEPS 525:65–80CrossRefGoogle Scholar
  122. Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecol 93;2483–2489Google Scholar
  123. Lewis LS, Anderson TW (2012) Top-down control of epifauna by fishes enhances seagrass production. Ecol 93:2746–2757Google Scholar
  124. Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. Bioscience 48:25–34CrossRefGoogle Scholar
  125. Ling SD (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156:883–894PubMedCrossRefPubMedCentralGoogle Scholar
  126. Lipkin Y (1975) Halophila stipulacea, a review of a successful immigration. Aquat Bot 1:203–215CrossRefGoogle Scholar
  127. Lobel PS, Ogden JC (1981) Foraging by the herbivorous parrotfish Sparisoma radians. Mar Biol 64:173–183CrossRefGoogle Scholar
  128. Long HA, Grosholz ED (2015) Overgrowth of eelgrass by the invasive colonial tunicate Didemnum vexillum: consequences for tunicate and eelgrass growth and epifauna abundance. J Exp Mar Biol Ecol 473:188–194CrossRefGoogle Scholar
  129. Long BG, Skewes TD (1996) On the trail of seagrass dieback in Torres Strait. Prof Fish 15–18Google Scholar
  130. Lowther AD, Harcourt RG, Hamer DJ, Goldsworthy SD (2011) Creatures of habit: foraging habitat fidelity of adult female Australian sea lions. Mar Ecol Prog Ser 443:249–263CrossRefGoogle Scholar
  131. MacArthur LD, Hyndes GA (2007) Varying foraging strategies of Labridae in seagrass habitats: herbivory in temperate seagrass meadows? J Exp Mar Biol Ecol 340:247–258CrossRefGoogle Scholar
  132. Mach ME, Wyllie-Echeverria S, Chan KM (2014) Ecological effect of a nonnative seagrass spreading in the Northeast Pacific: a review of Zostera japonica. Ocean Coast Manag 102:375–382CrossRefGoogle Scholar
  133. Madin EMP, Dill LM, Ridlon AD, Heithaus MR, Warner RR (2016) Human activities change marine ecosystems by altering predation risk. Glob Change Biol 22:44–60CrossRefGoogle Scholar
  134. Marco-Méndez C, Prado P, Heck KL, Cebrián J, Sánchez-Lizaso JL (2012) Epiphytes mediate the trophic role of sea urchins in Thalassia testudinum seagrass beds. Mar Ecol Prog Ser 460:91–100Google Scholar
  135. Mariani S, Alcoverro T (1999) A multiple-choice feeding-preference experiment utilising seagrasses with a natural population of herbivorous fishes. Mar Ecol Prog Ser 295–299Google Scholar
  136. Marsh H (2002) Dugong: status report and action plans for countries and territories. UNEP/EarthprintGoogle Scholar
  137. Marsh H, Lawler IR (2002) Dugong distribution and abundance in the northern Great Barrier Reef Marine Park-November 2000Google Scholar
  138. Masini RJ, Anderson PK, McComb AJ (2001) A Halodule-dominated community in a subtropical embayment: physical environment, productivity, biomass, and impact of dugong grazing. Aquat Bot 71:179–197CrossRefGoogle Scholar
  139. McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: animal loss in the global ocean. Science 347:1255641PubMedCrossRefPubMedCentralGoogle Scholar
  140. McGlathery KJ (1995) Nutrient and grazing influences on a subtropical seagrass community. Mar Ecol Prog Ser 122:239–252CrossRefGoogle Scholar
  141. Mcleod E, Chmura GL, Bouillon S, Salm R, Björk M, Duarte CM, Lovelock CE, Schlesinger WH, Silliman BR (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–560CrossRefGoogle Scholar
  142. McSkimming C, Tanner JE, Russell BD, Connell SD (2015) Compensation of nutrient pollution by herbivores in seagrass meadows. J Exp Mar Biol Ecol 471:112–118CrossRefGoogle Scholar
  143. Mertens NL, Russell BD, Connell SD (2015) Escaping herbivory: ocean warming as a refuge for primary producers where consumer metabolism and consumption cannot pursue. Oecologia 179:1223–1229PubMedCrossRefPubMedCentralGoogle Scholar
  144. Moksnes P-O, Gullström M, Tryman K, Baden S (2008) Trophic cascades in a temperate seagrass community. Oikos 117:763–777CrossRefGoogle Scholar
  145. Murdoch WW (1966) Community structure, population control, and competition-a critique. Am Nat 100:219–226Google Scholar
  146. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283PubMedCrossRefPubMedCentralGoogle Scholar
  147. 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 315:1846–1850PubMedCrossRefGoogle Scholar
  148. Nakaoka M (2002) Predation on seeds of seagrasses Zostera marina and Zostera caulescens by a tanaid crustacean Zeuxo sp. Aquat Bot 72:99–106CrossRefGoogle Scholar
  149. Nakaoka M (2005) Plant–animal interactions in seagrass beds: ongoing and future challenges for understanding population and community dynamics. Popul Ecol 47:167–177CrossRefGoogle Scholar
  150. Newell RI (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23:51–62Google Scholar
  151. Newell RI, Koch EW (2004) Modeling seagrass density and distribution in response to changes in turbidity stemming from bivalve filtration and seagrass sediment stabilization. Estuaries 27:793–806CrossRefGoogle Scholar
  152. Nienhuis PH, Groenendijk AM (1986) Consumption of eelgrass (Zostera marina) by birds and invertebrates: an annual budget. Mar Ecol Prog Ser 29Google Scholar
  153. Norse EA (1993) Global marine biological diversity: a strategy for building conservation into decision making. Island PressGoogle Scholar
  154. Orth RJ (1975) Destruction of eelgrass, Zostera marina, by the cownose ray, Rhinoptera bonasus, in the Chesapeake Bay. Chesapeake Sci 16:205–208CrossRefGoogle Scholar
  155. Orth RJ, Van Montfrans J (1984) Epiphyte-seagrass relationships with an emphasis on the role of micrograzing: a review. Aquat Bot 18:43–69CrossRefGoogle Scholar
  156. Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S et al (2006a) A global crisis for seagrass ecosystems. Bioscience 56:987–996CrossRefGoogle Scholar
  157. Orth RJ, Kendrick GA, Marion SR (2006b) Predation on Posidonia australis seeds in seagrass habitats of Rottnest Island, Western Australia: patterns and predators. Mar Ecol Prog Ser 313:105–114CrossRefGoogle Scholar
  158. O’Connor Mary I (2009) Warming strengthens an herbivore–plant interaction. Ecol 90:388–398Google Scholar
  159. O’Connor MI, Piehler MF, Leech DM, Anton A, Bruno JF (2009) Warming and resource availability shift food web structure and metabolism. PLoS Biol 7:e1000178Google Scholar
  160. Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol 49:667–685CrossRefGoogle Scholar
  161. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42PubMedCrossRefGoogle Scholar
  162. Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F (1998) Fishing down marine food webs. Science 279:860–863PubMedCrossRefGoogle Scholar
  163. Peacor SD, Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci 98:3904–3908PubMedCrossRefGoogle Scholar
  164. Pearce AF, Feng M (2013) The rise and fall of the “marine heat wave” off Western Australia during the summer of 2010/2011. J Mar Syst 111:139–156CrossRefGoogle Scholar
  165. Peterson BJ, Heck KL Jr (2001) Positive interactions between suspension-feeding bivalves and seagrass-a facultative mutualism. Mar Ecol Prog Ser 213:143–155CrossRefGoogle Scholar
  166. Phillips RC, Menez EG (1988) Seagrasses. Smithsonian Contrib Mar Sci 34: 1–104Google Scholar
  167. Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien M-L, Hereu B, Milazzo M, Zabala M, d’Anna G et al (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200CrossRefGoogle Scholar
  168. Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 3–15Google Scholar
  169. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147: 813–846Google Scholar
  170. Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT et al (2013) Global imprint of climate change on marine life. Nat Clim Change 3:919–925CrossRefGoogle Scholar
  171. Poore AG, Campbell AH, Steinberg PD (2009) Natural densities of mesograzers fail to limit growth of macroalgae or their epiphytes in a temperate algal bed. J Ecol 97:164–175CrossRefGoogle Scholar
  172. Poore AG, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA et al (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922PubMedCrossRefGoogle Scholar
  173. Powell GV, Fourqurean JW, Kenworthy WJ, Zieman JC (1991) Bird colonies cause seagrass enrichment in a subtropical estuary: observational and experimental evidence. Estuar Coast Shelf Sci 32:567–579CrossRefGoogle Scholar
  174. Prado P, Heck KL (2011) Seagrass selection by omnivorous and herbivorous consumers: determining factors. Mar Ecol Prog Ser 429:45–55CrossRefGoogle Scholar
  175. Prado P, Romero J, Alcoverro T et al (2010) Nutrient status, plant availability and seasonal forcing mediate fish herbivory in temperate seagrass beds. Mar Ecol Prog Ser 409:229–239Google Scholar
  176. Preen AR (1992) Interactions between dugongs and seagrasses in a subtropical environment, PhD Thesis. James Cook UniversityGoogle Scholar
  177. Preen A (1995) Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Mar Ecol Prog Ser 124:201–213CrossRefGoogle Scholar
  178. 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 24:185–208CrossRefGoogle Scholar
  179. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86: 501–509Google Scholar
  180. Randall JE (1965) Grazing effect on sea grasses by herbivorous reef fishes in the West Indies. Ecology 46:255–260CrossRefGoogle Scholar
  181. Reynolds LK, Carr LA, Boyer KE et al (2012) A non-native amphipod consumes eelgrass inflorescences in San Francisco Bay. Mar Ecol Prog Ser 451:107–118Google Scholar
  182. Reynolds PL, Richardson JP, Duffy JE (2014) Field experimental evidence that grazers mediate transition between microalgal and seagrass dominance. Limnol Oceanogr 59:1053–1064CrossRefGoogle Scholar
  183. Ricklefs R, Miller G (1999) Ecology. W.H. FreemanGoogle Scholar
  184. Roelofs A, Coles R, Smit N (2005) A survey of intertidal seagrass from Van Diemen Gulf to Castlereagh Bay, Northern Territory, and from Gove to Horn Island, Queensland. Queensland Department of Primary Industries and Fisheries: Brisbane, Qld, Australia.Google Scholar
  185. Rose CD, Sharp WC, Kenworthy WJ, Hunt JH, Lyons WG, Prager EJ, Valentine JF, Hall MO, Whitfield PE, Fourqurean JW (1999) Overgrazing of a large seagrass bed by the sea urchin Lytechinus variegatus in Outer Florida Bay. Mar Ecol Prog Ser 190:211–222CrossRefGoogle Scholar
  186. Rosenblatt AE, Schmitz OJ (2014) Interactive effects of multiple climate change variables on trophic interactions: a meta-analysis. Clim Change Responses 1:8CrossRefGoogle Scholar
  187. Rossini RA, Rueda JL, Tibbetts IR (2014) Feeding ecology of the seagrass-grazing nerite Smaragdia souverbiana (Montrouzier, 1863) in subtropical seagrass beds of eastern Australia. J Molluscan Stud 80(2):139–147Google Scholar
  188. Rueda JL, Salas C (2007) Trophic dependence of the emerald neritid Smaragdia viridis (Linnaeus, 1758) on two seagrasses from European coasts. J Mollus Stud 73:211–214CrossRefGoogle Scholar
  189. Russell B, Connell S (2007) Response of grazers to sudden nutrient pulses in oligotrophic versus eutrophic conditions. Mar Ecol Prog Ser 349:73–80CrossRefGoogle Scholar
  190. Sanmart N, Saiz L, Llagostera I, Prez M, Romero J (2014) Tolerance responses to simulated herbivory in the seagrass Cymodocea nodosa. Mar Ecol Prog Ser 517:159–169CrossRefGoogle Scholar
  191. Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954PubMedCrossRefGoogle Scholar
  192. Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399CrossRefGoogle Scholar
  193. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163CrossRefGoogle Scholar
  194. Sheppard JK, Carter AB, McKenzie LJ, Pitcher CR, Coles RG (2008) Spatial patterns of sub-tidal seagrasses and their tissue nutrients in the Torres Strait, northern Australia: implications for management. Cont Shelf Res 28: 2282–2291Google Scholar
  195. Sheppard JK, Marsh H, Jones RE, Lawler IR (2010) Dugong habitat use in relation to seagrass nutrients, tides, and diel cycles. Mar Mammal Sci 26:855–879CrossRefGoogle Scholar
  196. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791CrossRefGoogle Scholar
  197. Simpfendorfer CA, Milward NE (1993) Utilisation of a tropical bay as a nursery area by sharks of the families Carcharhinidae and Sphyrnidae. Environ Biol Fish 37:337–345CrossRefGoogle Scholar
  198. Smale DA, Wernberg T (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proc R Soc Lond B Biol Sci 280:20122829CrossRefGoogle Scholar
  199. Steele L, Valentine JF (2015) Seagrass deterrence to mesograzer herbivory: evidence from mesocosm experiments and feeding preference trialsGoogle Scholar
  200. Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754CrossRefGoogle Scholar
  201. Sumoski SE, Orth RJ (2012) Biotic dispersal in eelgrass Zostera marina. Mar Ecol Prog Ser 471:1–10CrossRefGoogle Scholar
  202. Targett NM, Targett TE, Vrolijk NH, Ogden JC (1986) Effect of macrophyte secondary metabolites on feeding preferences of the herbivorous parrotfish Sparisoma radians. Mar Biol 92:141–148CrossRefGoogle Scholar
  203. Thayer GW, Bjorndal KA, Ogden JC, Williams SL, Zieman JC (1984) Role of larger herbvores in seagrass communities. Estuaries 7: 351–376Google Scholar
  204. Thomson JA, Burkholder DA, Heithaus MR, Fourqurean JW, Fraser MW, Statton J, et al (2015) Extreme temperatures, foundation species, and abrupt ecosystem change: an example from an iconic seagrass ecosystem. Glob Change Biol 21: 1463–1474Google Scholar
  205. Tomas F, Abbott JM, Steinberg C, Balk M, Williams SL, Stachowicz JJ (2011) Plant genotype and nitrogen loading influence seagrass productivity, biochemistry, and plant–herbivore interactions. Ecology 92: 1807–1817Google Scholar
  206. Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. Seagrasses: Biol, Ecol Conserv: 463–501Google Scholar
  207. Valentine JF, Heck KL (1991) The role of sea urchin grazing in regulating subtropical seagrass meadows: evidence from field manipulations in the northern Gulf of Mexico. J Exp Mar Biol Ecol 154:215–230CrossRefGoogle Scholar
  208. Valentine, J.F. & Heck Jr, K.L. (1999). Seagrass herbivory: evidence for the continued grazing of marine grasses. Marine Ecology Progress Series, 291–302. Google Scholar
  209. Valentine JF, Heck KL (2001) The role of leaf nitrogen content in determining turtlegrass (Thalassia testudinum) grazing by a generalized herbivore in the northeastern Gulf of Mexico. J Exp Mar Biol Ecol 258:65–86PubMedCrossRefPubMedCentralGoogle Scholar
  210. Valentine JF, Heck KL, Busby J, Jr, Webb D (1997) Experimental evidence that herbivory increases shoot density and productivity in a subtropical turtlegrass (Thalassia testudinum) meadow. Oecologia 112:193–200Google Scholar
  211. van der Heide T, van Nes EH, Geerling GW, Smolders AJ, Bouma TJ, van Katwijk MM (2007) Positive feedbacks in seagrass ecosystems: implications for success in conservation and restoration. Ecosystems 10:1311–1322CrossRefGoogle Scholar
  212. van der Heide T, van Nes EH, van Katwijk MM, Olff H, Smolders AJ (2011) Positive feedbacks in seagrass ecosystems—evidence from large-scale empirical data. PLoS ONE 6:e16504PubMedPubMedCentralCrossRefGoogle Scholar
  213. van der Heide T, Govers LL, de Fouw J, Olff H, van der Geest M, van Katwijk MM, Piersma T, van de Koppel J, Silliman BR, Smolders AJP et al (2012) A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336:1432–1434PubMedCrossRefPubMedCentralGoogle Scholar
  214. van Gils JA, van der Geest M, Jansen EJ, Govers LL, de Fouw J, Piersma T (2012) Trophic cascade induced by molluscivore predator alters pore-water biogeochemistry via competitive release of prey. Ecol 93:1143–1152Google Scholar
  215. van Montfrans J, Wetzel RL, Orth RJ (1984) Epiphyte-grazer relationships in seagrass meadows: consequences for seagrass growth and production. Estuaries 7:289–309CrossRefGoogle Scholar
  216. van Tussenbroek BI, Brearley A (1998) Isopod burrowing in leaves of turtle grass, Thalassia testudinum, in a Mexican Caribbean reef lagoon. Mar Freshw Res 49:525–531CrossRefGoogle Scholar
  217. van Tussenbroek BI, Muhlia-Montero M (2012) Can floral consumption by fish shape traits of seagrass flowers? Evol Ecol 27:269–284CrossRefGoogle Scholar
  218. van Tussenbroek BI, Monroy-Velazquez LV, Solis-Weiss V (2012) Meso-fauna foraging on seagrass pollen may serve in marine zoophilous pollination. Mar Ecol Prog Ser 469:1CrossRefGoogle Scholar
  219. Vergés A, Becerro MA, Alcoverro T, Romero J (2006) Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant–herbivore interactions. Oecologia 151:675–686PubMedCrossRefPubMedCentralGoogle Scholar
  220. Vergés A, Pérez M, Alcoverro T, Romero J (2008) Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish. Oecologia 155:751–760PubMedCrossRefPubMedCentralGoogle Scholar
  221. Vergés A, Alcoverro T, Romero J (2010) Plant defences and the role of epibiosis in mediating within-plant feeding choices of seagrass consumers. Oecologia 166:381–390PubMedCrossRefPubMedCentralGoogle Scholar
  222. Vergés A, Steinberg PD, Hay ME, Poore AG, Campbell AH, Ballesteros E et al (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 20140846Google Scholar
  223. Verhoeven MPC, Kelaher BP, Bishop MJ, Ralph PJ (2012) Epiphyte grazing enhances productivity of remnant seagrass patches. Austral Ecol 37:885–892CrossRefGoogle Scholar
  224. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395PubMedCrossRefPubMedCentralGoogle Scholar
  225. Wassenberg T (1990) Seasonal feeding on Zostera capricorni seeds by Juvenile Penaeus esculentus (Crustacea: Decapoda) in Moreton Bay, Queensland. Mar Freshw Res 41:301–310CrossRefGoogle Scholar
  226. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR et al (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. PNAS 106:12377–12381PubMedCrossRefPubMedCentralGoogle Scholar
  227. Wernberg T, Russell BD, Moore PJ, Ling SD, Smale DA, Campbell A, Coleman MA, Steinberg PD, Kendrick GA, Connell SD (2011a) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J Exp Mar Biol Ecol 400:7–16CrossRefGoogle Scholar
  228. Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJ, Poloczanska ES, Connell SD (2011b) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832PubMedCrossRefPubMedCentralGoogle Scholar
  229. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, De Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78–82CrossRefGoogle Scholar
  230. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  231. Whalen MA, Duffy JE, Grace JB (2013) Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology 94:510–520PubMedCrossRefGoogle Scholar
  232. White WT, Potter IC (2004) Habitat partitioning among four elasmobranch species in nearshore, shallow waters of a subtropical embayment in Western Australia. Mar Biol 145:1023–1032CrossRefGoogle Scholar
  233. White KS, Westera MB, Kendrick GA (2011) Spatial patterns in fish herbivory in a temperate Australian seagrass meadow. Estuar Coast Shelf Sci 93:366–374CrossRefGoogle Scholar
  234. Willette DA, Chalifour J, Debrot AOD, Engel MS, Miller J, Oxenford HA, Short FT, Steiner SCC, Védie F (2014) Continued expansion of the trans-Atlantic invasive marine angiosperm Halophila stipulacea in the Eastern Caribbean. Aquat Bot 112:98–102CrossRefGoogle Scholar
  235. Williams SL (2007) Introduced species in seagrass ecosystems: status and concerns. J Exp Mar Biol Ecol 350:89–110CrossRefGoogle Scholar
  236. Williams SL, Heck KL, Jr (2001) Seagrass community ecology. Marine Commun Ecol 317–337Google Scholar
  237. Wirsing AJ, Heithaus MR, Dill LM (2007a) Can you dig it? Use of excavation, a risky foraging tactic, by dugongs is sensitive to predation danger. Anim Behav 74:1085–1091CrossRefGoogle Scholar
  238. Wirsing AJ, Heithaus MR, Dill LM (2007b) Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)? Oecologia 153:1031–1040PubMedCrossRefGoogle Scholar
  239. Wirsing AJ, Heithaus MR, Dill LM (2007c) Living on the edge: dugongs prefer to forage in microhabitats that allow escape from rather than avoidance of predators. Anim Behav 74:93–101CrossRefGoogle Scholar
  240. Wirsing AJ, Cameron KE, Heithaus MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79:531–537CrossRefGoogle Scholar
  241. Worm B, Lotze HK (2006) Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnol Oceanogr 51:569–579CrossRefGoogle Scholar
  242. Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman D, Heithaus MR, Kessel ST, Gruber SH (2013) Global catches, exploitation rates, and rebuilding options for sharks. Marine Policy 40:194–204CrossRefGoogle Scholar
  243. Wressnig A, Booth DJ (2007) Feeding preferences of two seagrass grazing monacanthid fishes. J Fish Biol 71:272–278CrossRefGoogle Scholar
  244. Wu L, Cai W, Zhang L, Nakamura H, Timmermann A, Joyce T, McPhaden MJ, Alexander M, Qiu B, Visbeck M et al (2012) Enhanced warming over the global subtropical western boundary currents. Nat Clim Change 2:161–166CrossRefGoogle Scholar
  245. Zarnetske PL, Skelly DK, Urban MC (2012) Biotic multipliers of climate change. Science 336:1516–1518PubMedCrossRefPubMedCentralGoogle Scholar
  246. Zimmerman RC, Kohrs DG, Alberte RS (1996) Top-down impact through a bottom-up mechanism: the effect of limpet grazing on growth, productivity and carbon allocation of Zostera marina L. (eelgrass). Oecologia 107:560–567PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Robert J. Nowicki
    • 1
    • 2
  • James W. Fourqurean
    • 1
    • 3
  • Michael R. Heithaus
    • 1
    • 4
  1. 1.Department of BiologyFlorida International UniversityMiamiUSA
  2. 2.Elizabeth Moore International Center for Coral Reef Research and RestorationMote Marine LaboratorySummerland KeyUSA
  3. 3.School of the Environment, Arts and Society, OE 227, MMCFlorida International UniversityMiamiUSA
  4. 4.College of Arts, Sciences & Education, ECS 450, MMCFlorida International UniversityMiamiUSA

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