Patterns of top-down control in a seagrass ecosystem: could a roving apex predator induce a behaviour-mediated trophic cascade?

1. The loss of large-bodied herbivores and/or top predators has been associated with large-scale changes in ecosystems around the world, but there remain important questions regarding the contexts in which such changes are most likely and the mechanisms through which they occur, particularly in marine ecosystems. 2. We used long-term exclusion cages to examine the effects of large grazers (sea cows, Dugong dugon; sea turtles Chelonia mydas) on seagrass community structure, biomass and nutrient dynamics. Experiments were conducted in habitats with high risk of predation (interior of shallow banks) and lower risk (edges of banks) to elucidate whether nonconsumptive (risk) effects of tiger sharks (Galeocerdo cuvier), a roving predator, structure herbivore impacts on seagrasses. 3. In lower-risk habitats, excluding large herbivores resulted in increased leaf length for Cymodocea angustata and Halodule uninervis. C. angustata shoot densities nearly tripled when released from herbivory, while H. uninervis nearly disappeared from exclusion cages over the course of the study. 4. We found no support for the hypothesis that grazing increases seagrass nutrient content. Instead, phosphorus content was higher in seagrasses within exclosures. This pattern is consistent with decreased light availability in the denser C. angustata canopies that formed in exclosures, and may indicate that competition for light led to the decrease in H. uninervis. 5. Impacts of large grazers were consistent with a behaviour-mediated trophic cascade (BMTC) initiated by tiger sharks and mediated by risk-sensitive foraging by large grazers. 6, Our results suggest that large-bodied grazers likely played important roles in seagrass ecosystem dynamics historically and that roving predators are capable of initiating a BMTC. Conservation efforts in coastal ecosystems must account for such interactions or risk unintended consequences.

[1]  Ransom A. Myers,et al.  Collapse and Conservation of Shark Populations in the Northwest Atlantic , 2003, Science.

[2]  W. Ripple,et al.  Are wolves saving Yellowstone's aspen? A landscape-level test of a behaviorally mediated trophic cascade: comment. , 2013, Ecology.

[3]  N. Marbà,et al.  Seagrass community metabolism: Assessing the carbon sink capacity of seagrass meadows , 2010 .

[4]  J. Laundré,et al.  Foraging in the ‘landscape of fear’ and its implications for habitat use and diet quality of elk Cervus elaphus and bison Bison bison , 2005 .

[5]  K. Bjorndal,et al.  Encouraging outlook for recovery of a once severely exploited marine megaherbivore , 2008 .

[6]  O. Schmitz Predators have large effects on ecosystem properties by changing plant diversity, not plant biomass. , 2006, Ecology.

[7]  M. Heithaus,et al.  Spatial pattern in seagrass stoichiometry indicates both N-limited and P-limited regions of an iconic P-limited subtropical bay , 2013 .

[8]  James W. Fourqurean,et al.  Phosphorus limitation of primary production in Florida Bay: Evidence from C:N:P ratios of the dominant seagrass Thalassia testudinum , 1992 .

[9]  O. J. Schmidt Behavior of predators and prey and links with population-level processes , 2005 .

[10]  Frederick T. Short,et al.  Accelerating loss of seagrasses across the globe threatens coastal ecosystems , 2009, Proceedings of the National Academy of Sciences.

[11]  Frederick T. Short,et al.  A Global Crisis for Seagrass Ecosystems , 2006 .

[12]  Cole,et al.  Trophic cascades revealed in diverse ecosystems. , 1999, Trends in ecology & evolution.

[13]  A. Frid,et al.  Behavioral Indicators in Marine Conservation: Lessons from a Pristine Seagrass Ecosystem , 2007 .

[14]  G. De’ath,et al.  HISTORICAL MARINE POPULATION ESTIMATES: TRIGGERS OR TARGETS FOR CONSERVATION? THE DUGONG CASE STUDY , 2005 .

[15]  Ivan R. Lawler,et al.  Distribution and Abundance of Dugongs, Turtles, Dolphins and other Megafauna in Shark Bay, Ningaloo Reef and Exmouth Gulf, Western Australia , 1997 .

[16]  L. Dill,et al.  Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. , 2009, The Journal of animal ecology.

[17]  S. V. Smith,et al.  Phosphorus limitation of net production in a confined aquatic ecosystem , 1984, Nature.

[18]  J. Brodie,et al.  Are wolves saving Yellowstone's aspen? A landscape-level test of a behaviorally mediated trophic cascade. , 2010, Ecology.

[19]  E. Meelis,et al.  Seagrass distribution and seasonal biomass changes in relation to dugong grazing in the Moluccas, East Indonesia , 1995 .

[20]  L. Dill,et al.  Can measures of prey availability improve our ability to predict the abundance of large marine predators? , 2007, Oecologia.

[21]  S. Creel Toward a predictive theory of risk effects: hypotheses for prey attributes and compensatory mortality. , 2011, Ecology.

[22]  James W. Fourqurean,et al.  Seagrass ecosystems as a globally significant carbon stock , 2012 .

[23]  M. Heithaus,et al.  Feeding preferences of herbivores in a relatively pristine subtropical seagrass ecosystem , 2012 .

[24]  O. Schmitz Effects of predator functional diversity on grassland ecosystem function. , 2009, Ecology.

[25]  L. Dill,et al.  Can you dig it? Use of excavation, a risky foraging tactic, by dugongs is sensitive to predation danger , 2007, Animal Behaviour.

[26]  Susan L. Williams,et al.  Role of larger herbvores in seagrass communities , 1984 .

[27]  William J. Foley,et al.  Dugong grazing and turtle cropping: grazing optimization in tropical seagrass systems? , 2006, Oecologia.

[28]  B. Godley,et al.  Fidelity and over-wintering of sea turtles , 2007, Proceedings of the Royal Society B: Biological Sciences.

[29]  D. Bolnick,et al.  SCARED TO DEATH? THE EFFECTS OF INTIMIDATION AND CONSUMPTION IN PREDATOR–PREY INTERACTIONS , 2005 .

[30]  L. Dill,et al.  Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)? , 2007, Oecologia.

[31]  T. Williams,et al.  Complex trophic interactions in kelp forest ecosystems , 2004 .

[32]  C. Johnson,et al.  Effects of simulated green turtle regrazing on seagrass abundance, growth and nutritional status in Moreton Bay, south-east Queensland, Australia , 2007 .

[33]  Lemnuel V. Aragones,et al.  Impact of Dugong grazing and turtle cropping on tropical seagrass communities , 1999 .

[34]  S. Creel,et al.  Relationships between direct predation and risk effects. , 2008, Trends in ecology & evolution.

[35]  A. Frid,et al.  Predicting ecological consequences of marine top predator declines. , 2008, Trends in ecology & evolution.

[36]  J. Valentine,et al.  Plant-herbivore interactions in seagrass meadows , 2006 .

[37]  Ransom A. Myers,et al.  Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico , 2004 .

[38]  J. Shurin,et al.  The strength of trophic cascades across ecosystems: predictions from allometry and energetics , 2005 .

[39]  D. Wise,et al.  Terrestrial Trophic Cascades: How Much Do They Trickle? , 2001, The American Naturalist.

[40]  Dharmadi,et al.  Elasmobranchs in southern Indonesian fisheries: the fisheries, the status of the stocks and management options , 2009, Reviews in Fish Biology and Fisheries.

[41]  S. Creel,et al.  Elk alter habitat selection as an antipredator response to wolves , 2005 .

[42]  W. Ripple,et al.  Restoring Yellowstone’s aspen with wolves , 2007 .

[43]  E. K. Pikitch,et al.  Trophic Downgrading of Planet Earth , 2011, Science.

[44]  G. Kendrick,et al.  The distribution of seagrass species in shark bay, Western Australia, with notes on their ecology , 1988 .

[45]  A. Frid,et al.  State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. , 2007, The Journal of animal ecology.

[46]  K. Bjorndal,et al.  Historical Overfishing and the Recent Collapse of Coastal Ecosystems , 2001, Science.

[47]  Boris Worm,et al.  Patterns and ecosystem consequences of shark declines in the ocean. , 2010, Ecology letters.

[48]  M. Heithaus,et al.  Diversity in trophic interactions of green sea turtles Chelonia mydas on a relatively pristine coastal foraging ground , 2011 .

[49]  J. Winnie Predation risk, elk, and aspen: tests of a behaviorally mediated trophic cascade in the Greater Yellowstone Ecosystem. , 2012, Ecology.

[50]  J. Fourqurean,et al.  Effects of excluding sea turtle herbivores from a seagrass bed: Overgrazing may have led to loss of seagrass meadows in Bermuda , 2010 .

[51]  David W. Engel,et al.  Evidence for short-circuiting of the detritus cycle of seagrass beds by the green turtle, Chelonia mydas L. , 1982 .

[52]  K. Bjorndal,et al.  Simulated green turtle grazing affects structure and productivity of seagrass pastures , 2005 .

[53]  K. Bjorndal Nutrition and grazing behavior of the green turtle Chelonia mydas , 1980 .

[54]  Hiroshi Mukai,et al.  Impacts of dugong foraging on benthic animal communities in a Thailand seagrass bed , 2002, Ecological Research.

[55]  O. Schmitz,et al.  EFFECTS OF TOP PREDATOR SPECIES ON DIRECT AND INDIRECT INTERACTIONS IN A FOOD WEB , 2001 .

[56]  Stacy K. Hargrove,et al.  Ecosystem structure and processes at Kaloko Honoko - hau, focusing on the role of herbivores, including the green sea turtle Chelonia mydas, in reef resilience , 2010 .

[57]  A Preen,et al.  Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing , 1995 .

[58]  Oswald J. Schmitz,et al.  Effects of Predator Hunting Mode on Grassland Ecosystem Function , 2008, Science.

[59]  C. Duarte Allometric scaling of seagrass form and productivity , 1991 .

[60]  S. Peacor,et al.  A REVIEW OF TRAIT-MEDIATED INDIRECT INTERACTIONS IN ECOLOGICAL COMMUNITIES , 2003 .

[61]  J. Valentine,et al.  The primacy of top-down effects in shallow benthic ecosystems , 2007 .

[62]  James W. Fourqurean,et al.  Large-scale decline in offshore seagrass meadows in Bermuda , 2007 .

[63]  D. Walker The Seagrasses of Western Australia , 2003 .

[64]  L. Dill,et al.  Predator‐induced modifications to diving behavior vary with foraging mode , 2011 .

[65]  W. Ripple,et al.  Wolves and the Ecology of Fear: Can Predation Risk Structure Ecosystems? , 2004 .

[66]  J. Jackson,et al.  Reefs since Columbus , 1997, Coral Reefs.

[67]  M. Boyce,et al.  WOLVES INFLUENCE ELK MOVEMENTS: BEHAVIOR SHAPES A TROPHIC CASCADE IN YELLOWSTONE NATIONAL PARK , 2005 .

[68]  N. Marbà,et al.  Implications of conserving an ecosystem modifier: Increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadows , 2010 .

[69]  A. Frid,et al.  Biology of sea turtles under risk from tiger sharks at a foraging ground , 2005 .

[70]  Stephen R. Carpenter,et al.  The Trophic Cascade in Lakes , 1993 .

[71]  Lawrence M. Dill,et al.  Living on the edge: dugongs prefer to forage in microhabitats that allow escape from rather than avoidance of predators , 2007, Animal Behaviour.

[72]  G. Hays,et al.  Critical evaluation of the nursery role hypothesis for seagrass meadows , 2003 .

[73]  Lawrence M. Dill,et al.  The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem , 2012 .

[74]  L. Dill,et al.  Tiger shark (Galeocerdo cuvier) abundance and growth in a subtropical embayment: evidence from 7 years of standardized fishing effort , 2006 .

[75]  J. Ogden,et al.  Herbivory Effects on Thalassia testudinum Leaf Growth and Nitrogen Content , 1984 .

[76]  A. Mccomb,et al.  A Halodule-dominated community in a subtropical embayment: physical environment, productivity, biomass, and impact of dugong grazing , 2001 .

[77]  O. Schmitz,et al.  Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants , 2000, The American Naturalist.

[78]  W. Dennison,et al.  Physiological and morphological responses of the seagrass Zostera capricorni Aschers, to light intensity , 1994 .

[79]  S. L. Williams,et al.  Thalassia testudinum productivity and grazing by green turtles in a highly disturbed seagrass bed , 1988 .

[80]  Michael R. Heithaus,et al.  Spatial responses to predators vary with prey escape mode , 2010, Animal Behaviour.

[81]  M. Heithaus FISH COMMUNITIES OF SUBTROPICAL SEAGRASS MEADOWS AND ASSOCIATED HABITATS IN SHARK BAY, WESTERN AUSTRALIA , 2004 .