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Ecol Evol
2023 Mar 01;133:e9929. doi: 10.1002/ece3.9929.
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Nutrient conditions determine the strength of herbivore-mediated stabilizing feedbacks in barrens.
Illa-López L
,
Aubach-Masip À
,
Alcoverro T
,
Ceccherelli G
,
Piazzi L
,
Kleitou P
,
Santamaría J
,
Verdura J
,
Sanmartí N
,
Mayol E
,
Buñuel X
,
Minguito-Frutos M
,
Bulleri F
,
Boada J
.
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Abiotic environmental conditions can significantly influence the way species interact. In particular, plant-herbivore interactions can be substantially dependent on temperature and nutrients. The overall product of these relationships is critical for the fate and stability of vegetated ecosystems like marine forests. The last few decades have seen a rapid spread of barrens on temperate rocky reefs mainly as a result of overgrazing. The ecological feedbacks that characterize the barren state involve a different set of interactions than those occurring in vegetated habitats. Reversing these trends requires a proper understanding of the novel feedbacks and the conditions under which they operate. Here, we explored the role of a secondary herbivore in reinforcing the stability of barrens formed by sea urchin overgrazing under different nutrient conditions. Combining comparative and experimental studies in two Mediterranean regions characterized by contrasting nutrient conditions, we assessed: (i) if the creation of barren areas enhances limpet abundance, (ii) the size-specific grazing impact by limpets, and (iii) the ability of limpets alone to maintain barrens. Our results show that urchin overgrazing enhanced limpet abundance. The effects of limpet grazing varied with nutrient conditions, being up to five times more intense under oligotrophic conditions. Limpets were able to maintain barrens in the absence of sea urchins only under low-nutrient conditions, enhancing the stability of the depauperate state. Overall, our study suggests a greater vulnerability of subtidal forests in oligotrophic regions of the Mediterranean and demonstrates the importance of environment conditions in regulating feedbacks mediated by plant-herbivore interactions.
FIGURE 1. Map of the study locations (Mediterranean Sea). High‐nutrient regime surveys were conducted in (PSA) Punta Santa Anna (41.67286°N 2.80211°E), (SAG) S'Agulla Garbí (41.68192°N 2.81511°E) and (SAL) S'Agulla Llevant (41.68242°N 2.81725°E) in the Catalan coast (1), Spain (NW Mediterranean). Low‐nutrient regime surveys were conducted in (CP) Costa Paradiso (41.04980°N 8.93686°E), (TP) Torre Porticciolo (40.64287°N 8.18720°E) and (SC) Santa Caterina (40.10620°N 8.48231°E) in the west coast of Sardinia (2), Italy (NW Mediterranean) and in (OL) Old Limassol (34.70693°N 33.13508°E) in the south coast of Cyprus (3, Levantine Sea). Orange and turquoise dots in the upper panel represent the position of the surveyed sites within both high‐ and low‐nutrient conditions, respectively. Mean annual surface NPP map was produced using 2019 monthly series of the MedBFM model system obtained from CMEM's Mediterranean Sea Biochemistry Analysis and Forecast metadata (E.U. Copernicus Marine Service Information). Annual mean values were calculated from 2019 monthly averages using SeaDAS software from NASA (version 8.0.0).
FIGURE 2. (a) Sea urchin density and barren cover. Bubble plot with values for the combination of sea urchin density (ind/m2) and barren cover (%) under high‐ and low‐nutrient conditions. The size of the bubbles is proportional to the number of specific combinations between both variables in quadrats (data from high‐ and low‐nutrients conditions have been included; n = 289). (b) Barren cover and limpet density. Bubble plot and predicted values (according to GLMMs; solid line) plus confidence intervals (shaded gray area) for limpet density (ind/m2) to barren cover. The interaction between barren cover and nutrient regime is significant (p‐value < .001). Data from high‐ (orange trend, n = 125) and low‐ (green trend, n = 164) nutrient conditions are plotted together and predicted values come from independent models.
FIGURE 3. Effect of nutrient regime on limpet densities and grazing impact. (a) Box plots of the overall limpet densities (ind/m2 ± SE) presented in high‐ and low‐nutrient conditions. (b) Bar plot of mean limpet densities (ind/m2 ± SE) per size class in each nutrient condition. Significant differences are denoted by the symbol * (p‐value < .05). (c) Box plots depicting the effect of nutrient conditions on limpets grazing impact (ratio between halos and limpet shell areas) under high‐ (n = 48) and low‐ (n = 47) nutrient conditions, respectively. Significant differences are denoted by the *** (p‐value < .001). (d) Relationship between halos and limpet shell areas (cm2) for both nutrient conditions. Predicted values (solid line) and confidence interval (shaded area) are also shown. A significant trend between these variables is seen under both regimes (p‐value < .001).
FIGURE 4. Effects of sea urchin removal under contrasting nutrient conditions. Changes in mean macroalgae cover, including both shrub‐forming and turf strata (solid lines and dots; %±SE), and in the percentage of limpet density (dashed lines and dots; % from initial density±SE) after removing sea urchins under (a) high‐ and (b) low‐nutrient conditions. Significant differences over time are seen for macroalgae cover and limpet population in a high‐nutrient regime (p‐value < .001). Pink shading indicates the time when sea urchins were removed from the selected barren areas.
FIGURE 5. Diagram of the main findings explaining the dependence of reinforcing feedbacks to nutrient conditions. On the left, sea urchin overgrazing facilitates the presence of limpets by grazing on the macroalgal forests (1) and precipitating the formation of barrens (2). Differences in nutrient conditions determine the capacity of limpets to maintain barrens. In high‐nutrient conditions, limpets do not outcompete algae growth and turfs colonize the rock surface (3.1). Instead, in low‐nutrient conditions, limpet grazing is sufficient to maintain the barren state (3.2). On the right, the mechanisms underlying this feedback in both nutrient conditions are detailed (a) sea urchin facilitation of limpets, (b) slightly different limpet densities between nutrient regimes, (c) differential grazing impact according to nutrient conditions, and (d) increased limpet mortality related to the recovery of the macroalgae.
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