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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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.
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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.
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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.
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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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DOI: https://doi.org/10.1038/s41559-024-02336-5
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