Eelgrass structural complexity mediates mesograzer herbivory on epiphytic algae

Abstract

Structural complexity mediates ecological processes such as predation, competition, and recruitment in marine systems, but relatively little is known about its effects on herbivory. In temperate seagrasses, such as eelgrass (Zostera marina), the primary herbivores are small crustacean and gastropod mesograzers that promote seagrass persistence by preferentially consuming competing epiphytic algae. We used a laboratory grazing experiment, a field colonization experiment, and stable isotope analysis to determine whether one component of eelgrass structural complexity, shoot density, dictates the strength of mesograzer top-down effects on epiphytic algae, and whether this is influenced by mesograzer community composition. Our results suggest that increasing structural complexity shifted eelgrass communities from a bottom-up to a top-down controlled system. In the lab, mesograzers reduced epiphyte standing stock only in high-shoot density experimental communities, though grazing impact varied among different combinations of dominant mesograzer taxa. In our field experiment, epiphyte biomass was inversely correlated with mesograzer density in high but not in low-shoot density eelgrass plots. High-shoot density plots contained lower epiphyte biomass despite housing lower densities of mesograzers, when compared to low-density plots, suggesting potential effects of mesograzer behavior, community composition, or self-shading on epiphyte growth. Our results suggest that structural complexity can strongly influence rates of top-down and bottom-up processes in eelgrass habitat, and should be incorporated into future experiments on the role of herbivores in seagrass ecosystems.

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References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Article  Google Scholar 

  2. Barry CK (1974) Role of form vision in habitat selection of the grass shrimp Hippolyte californiensis. Mar Biol 26:261–270

    Article  Google Scholar 

  3. Bell JD, Westoby M (1986) Abundance of macrofauna in dense seagrass is due to habitat preference, not predation. Oecologia 68:205–209

    Article  Google Scholar 

  4. Best RJ, Stachowicz JJ (2012) Trophic cascades in seagrass meadows depend on mesograzer variation in feeding rates, predation susceptibility, and abundance. Mar Ecol Prog Ser 456:29–42

    Article  Google Scholar 

  5. Boström C, Bonsdorff E (2000) Zoobenthic community establishment and habitat complexity-the importance of seagrass shoot-density, morphology and physical disturbance for faunal recruitment. Mar Ecol Prog Ser 205:123–138

    Article  Google Scholar 

  6. Bracken M, Dolecal RE, Long JD (2014) Community context mediates the top-down vs. bottom-up effects of grazers on rocky shores. Ecology 95:1458–1463

    Article  Google Scholar 

  7. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304

    Article  Google Scholar 

  8. Byrnes JE, Stachowicz JJ (2009) The consequences of consumer diversity loss: different answers from different experimental designs. Ecology 90(10):2879–2888

    Article  Google Scholar 

  9. Cebrian J, Stutes J, Christiaen B (2013) Effects of grazing and fertilization on epiphyte growth dynamics under moderately eutrophic conditions: implications for grazing rate estimates. Mar Ecol Prog Ser 474:121–133

    Article  Google Scholar 

  10. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER E Ltd, Plymouth

    Google Scholar 

  11. Crowder LB, Cooper WE (1982) Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63:1802–1813

    Article  Google Scholar 

  12. deMaintenon MJ (1999) Phylogenetic analysis of the Columbellidae (Mollusca: Neogastropoda) and the evolution of herbivory from carnivory. Invertebrate Biol 1:258–288

    Article  Google Scholar 

  13. Duarte CM, Middelburg JJ, Caraco N (2005) Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2:1–8

    CAS  Article  Google Scholar 

  14. Duarte CM, Marbà N, Gacia E et al (2010) Seagrass community metabolism: assessing the carbon sink capacity of seagrass meadows. Glob Biogeochem Cycles 24:GB4032

    Article  Google Scholar 

  15. Duffy JE (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7:437–444

    Article  Google Scholar 

  16. Duffy JE, Harvilicz AM (2001) Species-specific impacts of grazing amphipods in an eelgrass-bed community. Mar Ecol Prog Ser 223:201–211

    Article  Google Scholar 

  17. Duffy JE, Macdonald KS, Rhode JM, Parker JD (2001) Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology 82:2417–2434

    Article  Google Scholar 

  18. Duffy JE, Paul Richardson J, Canuel EA (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6:637–645

    Article  Google Scholar 

  19. Duffy JE, Paul Richardson J, France KE (2005) Ecosystem consequences of diversity depend on food chain length in estuarine vegetation. Ecol Lett 8:301–309

    Article  Google Scholar 

  20. Duffy JE, Reynolds PL, Boström C et al (2015) Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach. Ecol Lett 18:696–705

    Article  Google Scholar 

  21. Edgar GJ (1990) The use of the size structure of benthic macrofaunal communities to estimate faunal biomass and secondary production. J Exp Mar Biol Ecol 137:195–214

    Article  Google Scholar 

  22. Edgar GJ, Shaw C (1995) The production and trophic ecology of shallow-water fish assemblages in southern Australia III. General relationships between sediments, seagrasses, invertebrates and fishes. J Exp Mar Biol Ecol 194:107–131

    Article  Google Scholar 

  23. Eggleston DB, Etherington LL, Elis WE (1998) Organism response to habitat patchiness: species and habitat-dependent recruitment of decapod crustaceans. J Exp Mar Biol Ecol 223:111–132

    Article  Google Scholar 

  24. Ellison AM, Bank MS, Clinton BD et al (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486

    Article  Google Scholar 

  25. Fonseca MS, Bell SS (1998) Influence of physical setting on seagrass landscapes near Beaufort, North Carolina, USA. Marine Ecol Prog Ser 171:109

    Article  Google Scholar 

  26. Fonseca MS, Fisher JS (1986) A comparison of canopy friction and sediment movement between four species of seagrass with reference to their ecology and restoration. Mar Ecol Prog Ser 29:15–22

    Article  Google Scholar 

  27. Heck KL Jr, Crowder LB (1991) Habitat structure and predator-prey interactions in vegetated aquatic systems. Habitat structure. Springer, Dordrecht, pp 281–299

    Google Scholar 

  28. Heck KL Jr, Orth RJ (2006) Predation in seagrass beds. Seagrasses: biology, ecology, and conservation. Springer, Dordrecht, pp 537–550

    Google Scholar 

  29. Hooper DU, Chapin Iii FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  30. Hovel KA, Warneke AM, Virtue-Hilborn SP, Sanchez AE (2016) Mesopredator foraging success in eelgrass (Zostera marina): relative effects of epiphytes, shoot density, and prey abundance. J Exp Mar Biol Ecol 474:142–147

    Article  Google Scholar 

  31. Hughes AR, Bando KJ, Rodriguez LF, Williams SL (2004) Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Mar Ecol Prog Ser 282:87–99

    Article  Google Scholar 

  32. Hughes TP, Graham NAJ, Jackson JBC et al (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642

    Article  Google Scholar 

  33. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732

    Google Scholar 

  34. Irlandi EA (1997) Seagrass patch size and survivorship of an infaunal bivalve. Oikos 78:511

    Article  Google Scholar 

  35. Jaschinski S, Sommer U (2008) Functional diversity of mesograzers in an eelgrass–epiphyte system. Mar Biol 154:475–482

    Article  Google Scholar 

  36. Jaschinski S, Sommer U (2010) Positive effects of mesograzers on epiphytes in an eelgrass system. Mar Ecol Prog Ser 401:77–85

    Article  Google Scholar 

  37. Jaschinski S, Aberle N, Gohse-Reimann S et al (2008) Grazer diversity effects in an eelgrass–epiphyte–microphytobenthos system. Oecologia 159:607–615

    Article  Google Scholar 

  38. Larkum AWD, Orth RJ, Duarte CM (2006) Seagrasses: biology, ecology, and conservation. Springer, Dordrecht

    Google Scholar 

  39. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  40. Loreau M (1998) Biodiversity and ecosystem functioning: a mechanistic model. Proc Natl Acad Sci 95:5632–5636

    CAS  Article  Google Scholar 

  41. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    CAS  Article  Google Scholar 

  42. Loreau M, Naeem S, Inchausti P (2002) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford

    Google Scholar 

  43. McCoy ED, Bell SS (1991) Habitat structure: the evolution and diversification of a complex topic. Habitat structure: the physical arrangement of objects in space. Chapman and Hall, London, pp 3–27

    Google Scholar 

  44. Michel L, Dauby P, Dupont A, Gobert S (2015) Selective top-down control of epiphytic biomass by amphipods from Posidonia oceanica meadows: implications for ecosystem functioning. Belgian J Zool 145:83–93

    Google Scholar 

  45. Moore EC, Hovel KA (2010) Relative influence of habitat complexity and proximity to patch edges on seagrass epifaunal communities. Oikos 119:1299–1311

    Article  Google Scholar 

  46. Nelson WG (1979) Experimental studies of selective predation on amphipods: consequences for amphipod distribution and abundance. J Exp Mar Biol Ecol 38:225–245

    Article  Google Scholar 

  47. Norberg J (2000) Resource-niche complementarity and autotrophic compensation determines ecosystem-level responses to increased cladoceran species richness. Oecologia 122:264–272

    CAS  Article  Google Scholar 

  48. Orth RJ, Heck KL Jr (1980) Structural components of eelgrass (Zostera marina) meadows in the lower Chesapeake Bay-fishes. Estuaries Coasts 3:278–288

    Article  Google Scholar 

  49. Orth RJ, Heck KL Jr, Van Montfrans J (1984) Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries Coasts 7:339–350

    Article  Google Scholar 

  50. Orth RJ, Carruthers TJB, Dennison WC et al (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

    Article  Google Scholar 

  51. Paine RT (1992) Food-web analysis through field measurement of per capita interaction strength. Nature 355:73–75

    Article  Google Scholar 

  52. Perez-Matus A, Shima JS (2010) Density- and trait-mediated effects of fish predators on amphipod grazers: potential indirect benefits for the giant kelp Macrocystis pyrifera. Mar Ecol Prog Ser 417:151–U168. https://doi.org/10.3354/meps08820

    Article  Google Scholar 

  53. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 128:304

    Article  Google Scholar 

  54. Reynolds PL, Sotka EE (2011) Non-consumptive predator effects indirectly influence marine plant biomass and palatability. J Ecol 99:1272–1281

    Article  Google Scholar 

  55. Reynolds PL, Richardson JP, Duffy JE (2014) Field experimental evidence that grazers mediate transition between microalgal and seagrass dominance. Limnol Oceanogr 59:1053–1064

    Article  Google Scholar 

  56. Ruppert JLW, Travers MJ, Smith LL et al (2013) Caught in the middle: combined impacts of shark removal and coral loss on the fish communities of coral reefs. PLoS One 8:e74648

    CAS  Article  Google Scholar 

  57. Sanders D, Nickel H, Grützner T, Platner C (2008) Habitat structure mediates top–down effects of spiders and ants on herbivores. Basic Appl Ecol 9:152–160

    Article  Google Scholar 

  58. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Article  Google Scholar 

  59. Sirota L, Hovel KA (2006) Simulated eelgrass Zostera marina structural complexity: effects of shoot length, shoot density, and surface area on the epifaunal community of San Diego Bay, California, USA. Mar Ecol Prog Ser 326:115–131

    Article  Google Scholar 

  60. Sommer U (1999) The impact of herbivore type and grazing pressure on benthic microalgal diversity. Ecol Lett 2:65–69

    Article  Google Scholar 

  61. Stachowicz JJ, Best RJ, Bracken MES, Graham MH (2008) Complementarity in marine biodiversity manipulations: reconciling divergent evidence from field and mesocosm experiments. Proc Natl Acad Sci 105:18842–18847

    CAS  Article  Google Scholar 

  62. Stoner AW (1980) Perception and choice of substratum by epifaunal amphipods associated with seagrasses. Mar Ecol Prog Ser 3:105–111

    Article  Google Scholar 

  63. Tait KJ, Hovel KA (2012) Do predation risk and food availability modify prey and mesopredator microhabitat selection in eelgrass (Zostera marina) habitat? J Exp Mar Biol Ecol 426–427:60–67

    Article  Google Scholar 

  64. Trussell GC, Ewanchuk PJ, Matassa CM (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252

    Article  Google Scholar 

  65. Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum AWD et al (eds) Seagrasses: biology, ecology, and conservation. Springer, Dordrecht, pp 463–501

    Google Scholar 

  66. Van Montfrans J, Wetzel RL, Orth RJ (1984) Epiphyte-grazer relationships in seagrass meadows: consequences for seagrass growth and production. Estuaries 7:289

    Article  Google Scholar 

  67. Vergés A, Vanderklift MA, Doropoulos C, Hyndes GA (2011) Spatial patterns in herbivory on a coral reef are influenced by structural complexity but not by algal traits. PLoS One 6:e17115

    Article  Google Scholar 

  68. Warfe DM, Barmuta LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Oecologia 141:171–178 (d)

    Article  Google Scholar 

  69. Waycott M, Duarte CM, Carruthers TJB et al (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci 106:12377–12381

    CAS  Article  Google Scholar 

  70. Whalen MA, Duffy JE, Grace JB (2013) Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology 94:510–520

    Article  Google Scholar 

  71. Williams SL, Heck KL Jr (2001) Seagrass community ecology. Marine Community Ecology. Sinauer Associates Inc, Sunderland, pp 317–337

    Google Scholar 

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Acknowledgements

We thank C. Bayne, J. Boucree, W. Dailey, R. Dunn, A. Harrington, S. Hengen, J. Jaeger, J. Joseph, J. Ledbetter, P. Shukla, and M. Yeager for their advice and assistance both in the laboratory and the field. We would also like to thank J. Long, A. Palacios, J.E. Duffy, J.J Stachowicz, P.L. Reynolds, and members of the Zostera Experimental Network (ZEN) for advice and guidance throughout the study. Our research was supported by a Segal Americorps Education Award, a San Diego State University Harold and June Grant Memorial Scholarship, a CSU COAST Graduate Student Award for Marine Science Research, a Lerner-Grey Grant for Marine Research, and a National Science Foundation grant (OCE- 1336905) to K. Hovel. This is contribution number 62 from the San Diego State University Coastal and Marine Institute.

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EPV and KAH conceived of and designed the experiments. EPV performed the experiments and analyzed the data. EPV and KAH wrote the manuscript.

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Correspondence to Erin P. Voigt.

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Communicated by Ulrich Sommer.

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Voigt, E.P., Hovel, K.A. Eelgrass structural complexity mediates mesograzer herbivory on epiphytic algae. Oecologia 189, 199–209 (2019). https://doi.org/10.1007/s00442-018-4312-2

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Keywords

  • Grazing
  • Habitat structure
  • Seagrass
  • Shoot density
  • Stable isotope