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Herbivore effects increase with latitude across the extent of a foundational seagrass

Nature Ecology & Evolution volume 8, pages 663–675 (2024)Cite this article

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Abstract

Climate change is altering the functioning of foundational ecosystems. While the direct effects of warming are expected to influence individual species, the indirect effects of warming on species interactions remain poorly understood. In marine systems, as tropical herbivores undergo poleward range expansion, they may change food web structure and alter the functioning of key habitats. While this process (‘tropicalization’) has been documented within declining kelp forests, we have a limited understanding of how this process might unfold across other systems. Here we use a network of sites spanning 23° of latitude to explore the effects of increased herbivory (simulated via leaf clipping) on the structure of a foundational marine plant (turtlegrass). By working across its geographic range, we also show how gradients in light, temperature and nutrients modified plant responses. We found that turtlegrass near its northern boundary was increasingly affected (reduced productivity) by herbivory and that this response was driven by latitudinal gradients in light (low insolation at high latitudes). By contrast, low-latitude meadows tolerated herbivory due to high insolation which enhanced plant carbohydrates. We show that as herbivores undergo range expansion, turtlegrass meadows at their northern limit display reduced resilience and may be under threat of ecological collapse.

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Fig. 1: Map of study area and representative photos of simulated grazing.
Fig. 2: Grazing effects on seagrass productivity across latitude and light gradients.
Fig. 3: Standardized coefficients from the ‘latitude’ model of seagrass productivity.
Fig. 4: Grazing effects on rhizome non-structural carbohydrates.
Fig. 5: Standardized coefficients from the ‘light/temperature’ model of seagrass productivity.

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Data availability

All data used in this study are available at the FigShare repository (https://doi.org/10.6084/m9.figshare.24649641.v1).

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Acknowledgements

We are greatly indebted to the many staff, students and volunteers who helped with fieldwork and processing in the lab. We thank those at the Smithsonian Marine Station: S. Jones, Z. Foltz, S. Carlson, I. Segura-Garcia, M. Johnson, A. Looby, O. Carmack and D. Branson. We also thank L Spiers, J. Kuehl and J. Clamp at the Central Caribbean Marine Institute (CCMI) in Little Cayman; A. E. MacDonald at the Galveston site; K. Coates at the Bermuda site; A. John, A. Safryghin, J. Reinhart, K. Malinowski, L. Woodlee, M. Speegle, M, England, S. Glew, T. Leon and N. Knight at the Andros, Bahamas site; S. Engel and J. van Duijnhoven at the Bonaire site; S. Alford, T. Gruninger, A. Looby (again), C. Sullivan, S. Downey, P. Saldana, W. Scheffel, J. Roth and T. Jones at the Crystal River site; T. Gluckman, C. Raguse, I. Primrose Hartman, W. F. Bigelow and M. Albury at the Eleuthera, Bahamas site; and M. Guadalupe Barba Santos at the Puerto Morelos site. We also thank M. Sarsich and the Blue Carbon Analysis Laboratory at Florida International University for assistance with the nutrient analyses. Special thanks to E. Duffy, the Smithsonian MarineGEO program and the Zostera Experimental Network for key insights and inspiration behind this network. This work was conducted under the following permits: at Eleuthera under permit numbers MAMR/FIS/17 and MAMR/FIS/9 issued by the Department of Marine Resources; at Bonaire under permit number 558/2015‐2015007762 issued by Openbaar Lichaam Bonaire; at Belize under permit number 0004-18 issued by the Belize Fisheries Department; at Panama under permit numbers SE/AP-23-17 and SE/AO-1-19 issued by the Ministerio de Ambiente de la Republica de Panama; at Andros by permits issued by The Bahamas National Trust and the Bahamas Environment, Science and Technology Commission; and at Cayman Islands by a permit issued by the Department of Environment. This is contribution #1679 from the Coastlines and Oceans Division of the Institute of Environment at Florida International University, contribution #1213 from the Smithsonian Marine Station and contribution #1077 from the Caribbean Coral Reef Ecosystems Program. Funding for this project was provided by the US National Science Foundation (OCE-1737247 to J.E.C., A.H.A. and VJP; OCE-2019022 to J.E.C.; OCE-1737144 to K.L.H.; and OCE-1737116 to J.G.D.). M.J.A.C. was supported by I-Veni grant 181.002.

Author information

Authors and Affiliations

  1. Institute of Environment, Coastlines and Oceans Division, and Department of Biological Sciences, Florida International University, Miami, FL, USA

    Justin E. Campbell, O. Kennedy Rhoades, Calvin J. Munson, James W. Fourqurean, Janelle A. Goeke, Rancel Grana-Valdes, Clare Peabody & William L. Wied

  2. Smithsonian Marine Station, Fort Pierce, FL, USA

    Justin E. Campbell, O. Kennedy Rhoades, Valerie J. Paul, Enrique Bethel, Grace Dodillet, Katrina Dutton, Bethany M. Gaffey, Rachael Glazner, Janelle A. Goeke, Victoria J. Jenkins, Olivier A. A. Kramer, Isis G. Martinez Lopez, Vivienne A. Main, Duncan A. O’Brien, Amanda Sang, Khalil Smith, Uriah Sun, Jamie E. Thompson & William L. Wied

  3. Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, British Columbia, Canada

    O. Kennedy Rhoades

  4. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, USA

    Calvin J. Munson

  5. Department of Environmental Engineering Sciences, University of Florida, Gainesville, FL, USA

    Andrew H. Altieri

  6. Smithsonian Tropical Research Institute, Panama City, Republic of Panama

    Andrew H. Altieri

  7. The Water School, Florida Gulf Coast University, Fort Myers, FL, USA

    James G. Douglass & Amanda Sang

  8. Dauphin Island Sea Lab and University of South Alabama, Dauphin Island, AL, USA

    Kenneth L. Heck, Samantha T. Linhardt, Charles W. Martin, Candela Marco-Méndez & Alex Rodriguez

  9. Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX, USA

    Anna R. Armitage, Rachael Glazner, Janelle A. Goeke & Jamie E. Thompson

  10. UF|IFAS Nature Coast Biological Station, University of Florida, Cedar Key, FL, USA

    Savanna C. Barry & Ashley M. McDonald

  11. The Centre for Ocean Research and Education (CORE), Gregory Town, Bahamas

    Enrique Bethel, Duncan A. O’Brien & Owen R. O’Shea

  12. International Field Studies, Inc., Forfar Field Station, Blanket Sound, Bahamas

    Lindsey Christ

  13. Aquatic Ecology and Water Quality Management Group, Wageningen University & Research, Wageningen, The Netherlands

    Marjolijn J. A. Christianen & Fee O. H. Smulders

  14. CSA Ocean Sciences Inc., Stuart, FL, USA

    Grace Dodillet

  15. College of Marine Science, University of South Florida, St. Petersburg, FL, USA

    Thomas K. Frazer

  16. Florida Cooperative Fish and Wildlife Research Unit, School of Forest, Fisheries, and Geomatics Sciences, University of Florida, Gainesville, FL, USA

    Bethany M. Gaffey

  17. Texas A&M University-Corpus Christi, Corpus Christi, TX, USA

    Victoria J. Jenkins

  18. Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Puerto Morelos, Mexico

    Isis G. Martinez Lopez & Brigitta van Tussenbroek

  19. Soil and Water Sciences Department, University of Florida, Gainesville, FL, USA

    Ashley M. McDonald & Laura K. Reynolds

  20. Department of Plant and Soil Sciences, College of Agriculture, Food and Environment, University of Kentucky, Lexington, KY, USA

    Vivienne A. Main

  21. Department of Environment and Natural Resources, Government of Bermuda, ‘Shorelands’, Hamilton Parish, Bermuda

    Sarah A. Manuel & Khalil Smith

  22. CEAB (CSIC), Girona, Spain

    Candela Marco-Méndez

  23. Coastal and Ocean Processes Section, Virginia Institute of Marine Sciences, William & Mary, Gloucester Point, VA, USA

    Christopher J. Patrick

  24. King Abdullah University of Science and Technology, Thuwal, Saudi Arabia

    Lucia M. Rodriguez Bravo

  25. Bermuda Institute of Ocean Sciences (BIOS), St. George’s, Bermuda

    Yvonne Sawall

Authors
  1. Justin E. Campbell
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  2. O. Kennedy Rhoades
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  3. Calvin J. Munson
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Contributions

J.E.C., O.K.R., A.H.A., J.G.D., K.L.H. and V.J.P. designed the research; J.E.C., O.K.R., A.H.A., J.G.D., K.L.H., V.J.P., A.R.A., S.C.B., E.B., L.C., M.J.A.C., G.D., K.D., J.W.F., T.K.F., B.M.G., R.G., J.A.G., R.G.-V., V.J.J., O.A.A.K., S.T.L., C.W.M., I.G.M.L., A.M.M., V.A.M., S.A.M., C.M.-M., D.A.O’B., O.R.O’S., C.J.P., C.P., L.K.R., A.R., L.M.R.B., A.S., Y.S., K.S., F.O.H.S., U.S., J.E.T., B.V.T. and W.L.W. performed the research; J.E.C. analysed the data with contributions from C.J.M. and O.K.R.; and J.E.C. wrote the paper with contributions from all authors.

Corresponding author

Correspondence to Justin E. Campbell.

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Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Guilherme Longo and Jordi Pagès for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Graphical representation of treatments established at each site.

Plots (0.25m2) were established at each site manipulating (1) herbivory intensity (via leaf clipping) and (2) nutrient availability (via Osmocote nutrient bags attached center plot), for a total of 10 treatments (n = 5/site). Mesh cages were established around the clipped treatments to control variation in natural grazing. Partial cages and open plots were also established, but these treatments did not receive leaf clipping. Lower panel displays the gridded plot arrangement at each site. Photographs display plot / cage placement (upper) and Osmocote fertilizer bag (lower).

Extended Data Fig. 2 Winter effects of grazing on leaf productivity across latitude.

Lines represent linear fits plus 95% confidence intervals for the severe grazing (red), moderate grazing (blue) and no grazing (black) treatments. Points represent individual plots and are jittered for clarity (n = 50 plots/site).

Extended Data Fig. 3 Light and temperature trends across latitude.

Site means for light (daily photosynthetically active radiation, µmol photons m−2 s−1) and temperature across latitude (ºN). Data have been divided into two seasons based on sampling timeline. ‘Summer’ represents measurements recorded from approximately Apr 2018 - Sept 2018, and ‘Winter’ represents measurements recorded from approximately Sept 2018 – Apr 2019. Trend lines represent fits of generalized additive models (GAMs) and grey shading displays 95% confidence intervals. Significant tests were two-sided. Sites are labeled: Lac Bay, Bonaire (BONA), Carrie Bow Cay, Belize (CARR), Little Cayman, Cayman Islands (CAYM), Puerto Morelos, Mexico (PUER), Andros, Bahamas (ANDR), Eleuthera, Bahamas (ELEU), Naples, Florida (NAPL), Crystal River, Florida (CRYS), Galveston, Texas (GALV), St. Joseph Bay, Florida (JOES), Riddell’s Bay, Bermuda (BERM). Note that BOCA was an outlier for light levels and was excluded from the analysis (see Methods) to understand trends across the broader network.

Extended Data Fig. 4 Temperature density distributions across sites.

Plots display frequency distributions of recorded temperatures at each site during the summer and winter seasons. Sites have been ordered from top to bottom in order of decreasing latitude.

Extended Data Fig. 5 Latitudinal trends in grazing.

Rates of seagrass grazing across latitude (ºN). Total grazing rate (left panel) represents the proportion of examined shoots with evidence of any grazing mark. Grazing rate – Fish only (right panel) represents the proportion of shoots with only characteristic fish grazing marks (crescent shaped bite marks). Grazing rates were averaged across seasons. Trend lines represent fits of generalized additive models (GAMs) and grey shading displays 95% confidence intervals. Significance tests were two-sided.

Extended Data Fig. 6 Main effects of simulated grazing on belowground non-structural carbohydrates.

Grazing effects (no clip vs full clip, only) on rhizome total non-structural carbohydrates. Samples were collected at the experiment end after the winter season. Points represent individual plots and are jittered for clarity (n = 10 plots/site). Description: vertical heavy lines (medians); solid boxes (interquartile range); whiskers (range of non-outlier data).

Extended Data Fig. 7 Trends in leaf productivity, shoot density and leaf width across sites.

Boxplots of seagrass metrics measured in unmanipulated, open control plots (n = 5 plots/site) after the summer (upper panels) and winter (lower panels) seasons. Sites decline in latitude from top to bottom. Description: vertical heavy lines (medians); solid boxes (interquartile range); whiskers (range of non-outlier data).

Extended Data Fig. 8 Rhizome non-structural carbohydrates.

Boxplot of rhizome carbohydrates measured in control plots (n = 5 plots/site). Sites decline in latitude from top to bottom. Description: vertical heavy lines (medians); solid boxes (interquartile range); whiskers (range of non-outlier data).

Extended Data Fig. 9 Trends in leaf tissue nutrient content across latitude.

Values represent means of leaf tissue nitrogen (N) and phosphorus (P) content from the control, unmanipulated plots at each site across latitude (°N) (data previously published86). The limitation index (LI) was calculated for each site (see Methods). Note, higher LI values indicate seagrasses that are more nutrient-limited, thus a lower availability of ambient nutrients. For comparison, dashed red and black lines represent mean values from the enriched and unenriched open plots, respectively.

Extended Data Table 1 Site locations, codes, and environmental parameters
Full size table

Supplementary information

Supplementary Information

Supplementary Figs. 1–8 and Supplementary Tables 1–13.

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Campbell, J.E., Kennedy Rhoades, O., Munson, C.J. et al. Herbivore effects increase with latitude across the extent of a foundational seagrass. Nat Ecol Evol 8, 663–675 (2024). https://doi.org/10.1038/s41559-024-02336-5

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