Skip to main content

Advertisement

SpringerLink
Log in

Global Patterns in Seagrass Herbivory: Why, Despite Existing Evidence, There Are Solid Arguments in Favor of Latitudinal Gradients in Seagrass Herbivory

  • Special Issue: Seagrasses Tribute to Susan Williams
  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

The ecological paradigm that biological interactions are more intense in the tropics than in temperate or polar regions has existed since the mid-twentieth century, but several recent meta-analyses have provided scant evidence for latitudinal gradients in the intensity of herbivory. This contradictory evidence led us to carefully review the data and results of several of those papers that failed to find latitudinal gradients in rates of seagrass herbivory. To re-evaluate the arguments around the presence or absence of latitudinal gradients in herbivory in seagrass, we began by expanding the selection criteria to include more studies to compare the published latitudinal range of seagrass occurrences with the latitudes in which seagrass herbivory has been studied. We also compared the latitudinal range of known seagrass herbivores with the distribution of studies on seagrass herbivory. Finally, we investigated studies that provided seasonal data on net primary production and standing stock of seagrasses, which allowed an assessment of the relative amounts of production that could enter the seagrass grazing food web among latitudes and climatic regimes. Consistent with recent meta-analyses, we found little latitudinal effect on grazing rates. However, we argue that the following factors are likely to confound these findings and potentially mask latitudinal trends in seagrass herbivory: (1) the paucity of data available to test latitudinal trends in grazing rates at high latitudes; (2) the mismatch between the geographic distribution of important grazers and studies on seagrass herbivory; (3) the paucity of experimental studies from areas with little or no herbivory because few researchers would initiate a study on something not observed to be occurring; (4) the high level of seasonality in seagrass production in high latitudes, where seagrass production is very low or nonexistent in winter months; (5) the fact that temperate areas with Mediterranean climates behave very differently than temperate areas at similar latitudes with much greater seasonality, thereby making latitude a much less informative independent variable than annual range in temperature; and (6) anthropogenic disturbances, including the overharvesting to functional extinction of large seagrass herbivores in both temperate and tropical regions. Thus, while we currently cannot discount the lack of a latitudinal gradient in grazing intensity, we argue that the intensity of grazing is likely to be greater in the tropics than high-latitude regions where the carrying capacity of seagrass meadows is far less stable. Either way, there are clear gaps in our knowledge and ability to evaluate the role of grazing in seagrass ecosystems and inform future efforts to conserve and restore these extraordinarily valuable ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bakker, E.S., K.A. Wood, J.F. Pages, G.F. Veen, M.J.A. Christianen, L. Santamarina, B.A. Nolet, and S. Hilt. 2016. Herbivory on freshwater and marine macrophytes: a review and perspective. Aquatic Botany 135: 18–36.

    Google Scholar 

  • Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67 (1): 1–48.

    Google Scholar 

  • Baum, J.O., R.A. Myers, D.G. Kehler, B. Worm, S.J. Harley, and P.A. Doherty. 2003. Collapse and conservation of shark populations in the Northwest Atlantic. Science 299 (5605): 389–391.

    CAS  Google Scholar 

  • Beca-Carretero, P., C.S. Stanschewski, M. Julia-Miralles, A. Sanchez-Gallego, and D.B. Stengel. 2019. Temporal and depth-associated changes in the structure, morphometry and production of near-pristine Zostera marina meadows in western Ireland. Aquatic Botany 155: 5–17.

    Google Scholar 

  • Bennett, S., and D.R. Bellwood. 2011. Latitudinal variation in macroalgal consumption by fishes on the Great Barrier Reef. Marine Ecology Progress Series 426: 241–252.

    Google Scholar 

  • Bertness, M.W., S.D. Gaines, and S.C. Levings. 1981. Predation pressure and gastropod foraging: a tropical-temperate comparison. Evolution 35 (5): 995–1007.

    Google Scholar 

  • Cheng, B.S., G.M. Ruiz, A.H. Altieri, and M.E. Torchin. 2019. The biogeography of invasion in tropical and temperate seagrass beds: interactive effects of predation and propagule pressure. Diversity and Distribution 2019: 285–297.

    Google Scholar 

  • Colloca, F., M. Cardinale, F. Maynou, M. Giannoulaki, G. Scarcella, K. Jenko, J.M. Bellido, and F. Fiorentino. 2013. Rebuilding Mediterranean fisheries: a new paradigm for ecological sustainability in single species population models. Fish and Fisheries 14 (1): 89–109.

    Google Scholar 

  • Dobzhansky, T. 1950. Evolution in the tropics. American Scientist 38: 209–221.

    Google Scholar 

  • Domning, D.P. 2001. Sirenians, seagrasses, and Cenozoic ecological change in the Caribbean. Paleogeography, Paleoclimatology and Paleoecology 166 (1-2): 27–50.

    Google Scholar 

  • Eklof, J.S., M. de la Torre-Castro, M. Gullstrom, J. Uke, N. Muthiga, T. Lyimos, and O. Bandeira. 2008. Sea urchin overgrazing of seagrasses: A review of current knowledge on causes, consequences, and management. Estuarine Coastal and Shelf Science 79 (4): 569–580.

    Google Scholar 

  • Estes, J.A., 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, R.J. Marquis, L. Oksanen, T. Oksanen, R.T. Paine, E.K. Pikitch, W.J. Ripple, S.A. Sandin, M. Scheffer, T.W. Schoener, J.B. Shurin, A.R.E. Sinclair, M.E. Soulé, R. Virtanen, and D.A. Wardle. 2011. Trophic downgrading of planet earth. Science 333 (6040): 301–306.

    CAS  Google Scholar 

  • Farina, S., F. Tomas, P. Prado, J. Romero, and T. Alcoverro. 2009. Seagrass meadow structure alters interactions between the sea urchin Paracentrotus lividus and its predators. Marine Ecology Progress Series 377: 131–137.

    Google Scholar 

  • Floeter, S.R., M.D. Behrens, C.E.L. Ferreira, M.J. Paddack, and M.H. Horn. 2005. Geographical gradients of marine herbivorous fishes: patterns and processes. Marine Biology 147 (6): 1435–1447.

    Google Scholar 

  • Fox, A.D., Ebbinge, B.S., Mitchell, C., Heinicke, T., Aarvark, T., Colhoun, K., Clausen,P., Dereliev, S., Farago, S., Koffijberg, K., Kruckenberg, H., Loonen, M.J.J.E., Madsen, J., Mooij, J., Musil, P., Nilsson, L., Pihl, S., & van der Jeugd, H. (2010). Current estimates of goose population sizes in western Europe, a gap analysis and an assessment of trends. OrnisSvec 20: 115–127.

  • Freestone, A.L., R.W. Osman, G. Ruiz, and M.E. Torchin. 2011. Stronger predation in the tropics shapes species richness patterns in marine communities. Ecology 92 (4): 983–993.

    Google Scholar 

  • Froese, R., and D. Pauly (eds.) 2019. Fish base. World Wide Web Electronic Publication. http://www.fishbase.de.

  • Green, E.P., and F.T. Short. 2003. World atlas of seagrasses, 298 pp. Berkeley, AA: University of California Press.

    Google Scholar 

  • Heck, K.L., Jr., and T.A. Thoman. 1981. Experiments on predator prey interactions in vegetated aquatic habitats. Journal of Experimental Marine Biology and Ecology 53: 124–134.

    Google Scholar 

  • Heck, K.L., Jr., and J.F. Valentine. 2006. Plant-herbivore interactions in seagrass meadows. Journal of Experimental Marine Biology and Ecology 330: 420–436.

    Google Scholar 

  • Hyndes, G.A., K.L. Heck, A. Verges, E.S. Harvey, G.A. Kendrick, P.S. Lavery, et al. 2016. Accelerating tropicalization and the transformation of temperate seagrass meadows. Bioscience 66 (11): 938–948.

    Google Scholar 

  • Jackson, J. (1997). Reefs since Columbus Coral Reefs 16, Supplement: S23-S32.

  • Jackson, J.B.C., M.X. Kirby, W.H. Berger, K.A. Bjorndal, L.W. Botsford, B.J. Bourque, et al. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293 (5530): 629–637.

    CAS  Google Scholar 

  • Longo, G.O., M.E. Hay, C.E.L. Ferreirra, and S.R. Floeter. 2018. Trophic interactions across 61 degrees of latitude in the Western Atlantic. Global Ecology and Biogeography 2018: 1–11.

    Google Scholar 

  • MacArthur, R.H. 1972. Geographical ecology. NY: Harper and Row.

    Google Scholar 

  • MacArthur, L.D., and G.A. Hyndes. 2007. Varying foraging strategies of Labridae in seagrass habitats: Herbivory in temperate seagrass meadows? Journal of Experimental Marine Biology and Ecology 340 (2): 247–258.

    Google Scholar 

  • Madsen, L. 1998. Experimental refuges for migratory waterfowl in Danish wetlands. I. Baseline assessment of the disturbance effects of recreational activities. Journal of Applied Ecology 35: 386–397.

    Google Scholar 

  • Marco-Méndez, C., L.M. Ferrero-Vicente, P. Prado, K.L. Heck, J. Cebrián, and J.L. Sánchez-Lizaso. 2015. Epiphyte presence and seagrass species identity influence rates of herbivory in Mediterranean seagrass meadows. Estuarine, Coastal and Shelf Science 154: 94–101.

    Google Scholar 

  • Marsh, H., T. O’Shea, and J.E.I. Reynolds (eds.). 2011. Ecology and conservation of the sirenia: dugongs and manatees. Cambridge, UK: Cambridge University Press.

  • Moles, A.T., S.P. Bonser, A.G.B. Poore, I.R. Wallis, and W.J. Foley. 2011. Assessing the evidence for latitudinal gradients in plant defence and herbivory. Functional Ecology 25 (2): 380–388.

    Google Scholar 

  • Nacken, M., and K. Reise. 2000. Effects of herbivorous birds on intertidal seagrass beds in the northern Waddeen Sea. Helgoland Marine Research 54: 87–94.

    Google Scholar 

  • Olesen, B., D. Krause-Jensen, N. Marba, and P.B. Christensen. 2015. Eelgrass Zostera marina in subarctic Greenland: Dense meadows with slow biomass turnover in cold waters. Marine Ecology Progress Series 518: 107–121.

    Google Scholar 

  • Pennings, S.C., E.L. Siska, and M.D. Bertness. 2001. Latitudinal differences in plant palatability in Atlantic coast salt marshes. Ecology 82: 1344–1359.

    Google Scholar 

  • Pennings, S.C., C.K. Ho, C.S. Salgado, K. Wieski, N. Dave, A.E. Kunza, and E.L. Wason. 2009. Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes. Ecology 90 (1): 183–195.

    Google Scholar 

  • Pinna, S., A. Pais, L. Chessa, N. Sechi, and G. Ceccherelli. 2009. Leaf partitioning of the seagrass Posidonia oceanica between two herbivores: is Sarpa salpa herbivory underestimated because of Paracentrotus lividus grazing? Estuarine, Coastal and Shelf Science 84 (1): 21–27.

    Google Scholar 

  • Poore, A.G.B., A.H. Campbell, R.A. Coleman, G.J. Edgar, V. Jormalainen, P.A. Reynolds, et al. 2012. Global patterns in the impact of marine herbivores on benthic primary producers. Ecology Letters 15 (8): 912–922.

    Google Scholar 

  • Portig, A.A., R.G. Mathers, W.I. Montgomery, and R.N. Govier. 1994. The distribution and utilisation of Zostera species in Strangford Lough, Northern Ireland. Aquatic Botany 47 (3-4): 317–328.

    Google Scholar 

  • Prado, P., F. Tomas, T. Alcoverro, and J. Romero. 2007. Extensive direct measurements of Posidonia oceania defoliation confirm the importance of herbivory in temperate seagrass meadows. Marine Ecology Progress Series 340: 63–71.

    Google Scholar 

  • Prado, P., J. Romero, and T. Alcoverro. 2010. Nutrient status: plant availability and seasonal forcing mediate fish herbivory in temperate seagrass beds. Marine Ecology Progress Series 409: 229–239.

    Google Scholar 

  • Robertson, A.I., and K.H. Mann. 1984. Disturbance by ice and life-history adaptations of the seagrass Zostera marina. Marine Biology 80 (2): 131–141.

    Google Scholar 

  • Tomas, F., X. Turon, and J. Romero. 2005. Seasonal and small-scale spatial variability of herbivory pressure on the temperate seagrass Posidonia oceanica. Marine Ecology Progress Series 301: 95–107.

    Google Scholar 

  • UNEP-WCMC, Short, F.T. (2017). Global distribution of seagrasses (version 6.0). Sixth update to the data layer used in Green and Short (2003). Cambridge (UK): UN Environment World Conservation Monitoring Centre. URL: http://data.unepwcmc.org/datasets/7.

  • Valentine, J.F., and K.L. Heck Jr. 1999. Seagrass herbivory: evidence for the continued grazing of marine grasses. Marine Ecology Progress Series 176: 291–302.

    Google Scholar 

  • Valentine, J.F., and J.E. Duffy. 2006. The central role of grazing in seagrass ecology. In Seagrasses: Biology, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 463–501. NY: Ecology and Conservation. Springer.

    Google Scholar 

  • Vasilakopoulos, P., C.D. Maravelias, and G. Tserpes. 2014. The alarming decline of Mediterranean fish stocks. Current Biology 24: 14.

    Google Scholar 

  • Velez-Juarbe, J. D.P. Domning & A.D. Pyenson. (2013). Iterative evolution of sympatric seacow (Dugongidae, Sirenia) assemblages during the past ,26 Million years. PLoS One 7: e31294.

  • Vergés, A., M.A. Becerro, T. Alcoverro, and J. Romero. 2007. Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant-herbivore interactions. Oecologia 151 (4): 675–686.

    Google Scholar 

  • Verges, A., P.D. Steinberg, N.E. Hay, A.G.B. Poore, A.H. Campbell, E. Ballesteros, et al. 2014. The tropicalizationof temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society B. 281 (1789): 20140846.

    Google Scholar 

  • Verges, A., C. Doroupoulos, R. Czarnik, K. McMahon, N. Llonch, and A.G.B. Poore. 2018. Latitudinal variation in seagrass herbivory: global pattern and explanatory mechanisms. Global Ecology and Biogeography 27 (9): 1068–1079.

    Google Scholar 

  • Vermeij, G.J. 1987. Evolution and escalation: an ecological history of life. Princeton, NJ: Princeton University Press (527 pp).

    Google Scholar 

  • Wernberg, T., D.A. Smale, F. Tuya, M.S. Thomsen, T.J. Langlois, T. de Bettignies, S. Bennett, and C.S. Rousseaux. 2013. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change 3 (1): 78–82.

    Google Scholar 

  • Wernberg, T., S. Bennett, R.C. Babcock, T. de Bettignies, K. Cure, M. Depczynski, et al. 2016. Climate driven regime shift of a temperate marine ecosystem. Science 353: 68–72.

    Google Scholar 

  • White, K.S., M.B. Westera, and G.A. Kendrick. 2011. Spatial patterns in fish herbivory in a temperate Australian seagrass meadow. Estuarine, Coastal and Shelf Science 93 (4): 366–374.

    Google Scholar 

  • 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, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106 (30): 12377–12381.

    CAS  Google Scholar 

  • Wood, K.A., M.T. O'Hare, C. McDonald, K.R. Searle, F. Daunt, and R.T. Stillman. 2016. Herbivore regulation of plant abundance in aquatic ecosystems. Biological Reviews 92: 1128–1141.

    Google Scholar 

  • Wressnig, A., and D.J. Booth. 2007. Feeding preferences of two seagrass grazing monacanthid fishes. Journal of Fish Biology 7: 272–278.

    Google Scholar 

Download references

Acknowledgments

We thank Adriana Verges for the early discussions and provision of a subset of the data. We also thank Edith Cowan University for providing the funds for KH to visit Edith Cowan University to initiate and develop the paper and Casper Avenant for the final edits on the manuscript.

Author information

Author notes

  1. Authors K. L. Heck, Jr and G. A. Hyndes contributed equally to the preparation of this paper

Authors and Affiliations

  1. Dauphin Island Sea Lab, Dauphin Island, AL, USA

    K. L. Heck Jr

  2. University of South Alabama, Dauphin Island, AL, USA

    K. L. Heck Jr

  3. Centre for Marine Ecosystems Research, School of Science, Edith Cowan University, Joondalup, WA, Australia

    M. Samsonova & G. A. Hyndes

  4. Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW, Australia

    A. G. B. Poore

Authors
  1. K. L. Heck Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Samsonova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. G. B. Poore
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. A. Hyndes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. L. Heck Jr.

Additional information

Communicated by Just Cebrian

Electronic Supplementary Material

ESM 1

(DOCX 55 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Heck, K.L., Samsonova, M., Poore, A.G.B. et al. Global Patterns in Seagrass Herbivory: Why, Despite Existing Evidence, There Are Solid Arguments in Favor of Latitudinal Gradients in Seagrass Herbivory. Estuaries and Coasts 44, 481–490 (2021). https://doi.org/10.1007/s12237-020-00833-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-020-00833-x

Keywords

Search

Navigation