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Sci Rep
2020 Mar 20;101:5103. doi: 10.1038/s41598-020-61753-1.
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Resistance of seagrass habitats to ocean acidification via altered interactions in a tri-trophic chain.
Martínez-Crego B
,
Vizzini S
,
Califano G
,
Massa-Gallucci A
,
Andolina C
,
Gambi MC
,
Santos R
.
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Despite the wide knowledge about prevalent effects of ocean acidification on single species, the consequences on species interactions that may promote or prevent habitat shifts are still poorly understood. Using natural CO2 vents, we investigated changes in a key tri-trophic chain embedded within all its natural complexity in seagrass systems. We found that seagrass habitats remain stable at vents despite the changes in their tri-trophic components. Under high pCO2, the feeding of a key herbivore (sea urchin) on a less palatable seagrass and its associated epiphytes decreased, whereas the feeding on higher-palatable green algae increased. We also observed a doubled density of a predatory wrasse under acidified conditions. Bottom-up CO2 effects interact with top-down control by predators to maintain the abundance of sea urchin populations under ambient and acidified conditions. The weakened urchin herbivory on a seagrass that was subjected to an intense fish herbivory at vents compensates the overall herbivory pressure on the habitat-forming seagrass. Overall plasticity of the studied system components may contribute to prevent habitat loss and to stabilize the system under acidified conditions. Thus, preserving the network of species interactions in seagrass ecosystems may help to minimize the impacts of ocean acidification in near-future oceans.
Figure 1. Trophic structure of consumer populations based on isotopic signatures at off-vent and vent sites. (a) δ13C vs. δ15N of consumers (single replicates) with solid lines enclosing the corrected standard ellipse areas (=isotopic niche widths) of urchin populations, where the diversity of resources exploited (δ13C range), the trophic niche redundancy (packing) and length (δ15N range), as well as the position of the niche centroid (which changes indicates trophic plasticity), are visualized for off-vent to south-vent and north-vent replicates. (b) δ13C vs. δ15N of basal resources and consumers (‰, mean ± standard deviation). Resources are indicated as follows: Asp, Asparagopsis armata; Clado, Cladophora prolifera; Cla, Cladophora spp.; Dic, Dictyota spp.; Epi, Epiphytes Fla, Flabellia petiolata; Halo, Halopteris scoparia; Jan, Jania rubens; Pey, Peyssonnelia spp.; Posi: Posidonia oceanica. Data on other invertebrate (Invert) obtained from Ricevuto et al.43 in the same sites and season were used exclusively as basal resources for wrasses in the SIA-based calculations. Values of the metrics of trophic structure and statistical comparison among sites are shown in Supplementary Table S4 (sea urchins) and S5 (wrasses). Statistical differences in isotopic signatures are shown in Supplementary Tables S6 (resources) and S7 (consumers).
Figure 2. C:N:P stoichiometry (a) and trophic position (b) of consumers at off-vent and vent sites (mean ± standard deviation). Trophic positions (TP) were obtained using methods based on diet composition (left graph) and stable isotopes (right graph). Different letters above bars or symbols denote significant differences among sites based on post hoc comparisons from one-way PERMANOVAs. Elemental contents are shown in Supplementary Fig. S1 and detailed statistical results in Supplementary Tables S8 (stoichiometry) and S9 (TP).
Figure 3. Mean diet composition of consumers at off-vent and vent sites. For illustrative purposes food items were grouped as detailed in SIMPER results shown in Supplementary Tables S10 (sea urchins) and S11 (wrasses). Abbreviations are as follows: Non-calcified benthic invertebrates (NC invert); Less calcified benthic invertebrates (LC invert); Heavily calcified benthic invertebrates (HC invert); Unidentified material (Other). Colour legend of food items is shown in one pie chart for each consumer species. The number of replicates is indicated in the parentheses. Data of P. lividus diet obtained from Nogueira et al.24. Statistical differences in diet composition, which are indicative of consumer trophic plasticity, are shown in Supplementary Table S12. Consumer images are courtesy of the Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/symbols/).
Figure 4. Feeding preference of sea urchins toward resources from off-vent versus vent sites (mean ± 95% CI). Effects are significantly different from zero if CIs do not overlap with zero. Negative values indicate preference for off-vent material, while positive values illustrate significant preference for vent material. The number of assays used in each estimate is indicated in the parentheses. Resources are indicated as follows: Posi: Posidonia oceanica; Posi-Epi, Posidonia with epiphytes, Fla, Flabellia petiolata; Pey, Peyssonnelia spp.; Jan, Jania rubens; Halo, Halopteris scoparia. Detailed consumptions are shown in Supplementary Fig. S2. Images were courtesy of the Integration and Application Network (ian.umces.edu/symbols/) or generated by BMC using SigmaPlot v11.1.
Figure 5. Nutritional, chemical and structural quality of the most abundant resources available to herbivores at off-vent (black) and vents (dark grey: south-vent, light grey: north-vent). Data are mean ± standard deviation (n = 4, except n = 5 for Posidonia and Peyssonnelia phenolics). Significant effects from PERMANOVAs are shown within the parenthesis. Different letters next to bars denote significant differences among sites for a given resource or for each Posidonia structural trait. Statistics are detailed in Supplementary Tables S13 and S14, and elemental contents in Supplementary Fig. S1.
Figure 6. Consumer abundances (a), fish herbivory (b), habitat structure (c) and refuge provision (d) at off-vent and vent sites. Data are mean ± standard deviation. PERMANOVA significant effects are shown within the parenthesis. Lowercase letters denote significant differences among sites. Capital letters denote significant differences between urchin and wrasse abundances within each site following the colour legend shown in the pictures. Statistics are detailed in Supplementary Tables S15 and S16. Pictures show the contrasting habitat structural complexity at vents (low canopy height due to an intense fish herbivory) and off-vent (regular canopy height). Mean seagrass density (shoots m−2), used to estimate indicators of refuge provision, is indicated in the parentheses within each site picture. Consumer images are courtesy of the Integration and Application Network (ian.umces.edu/symbols/).
Figure 7. Overview of the tri-trophic seagrass system under ambient (off-vent) and acidified (vent) conditions. The acidified conditions (vents) are characterized by an altered palatability of primary resources (with similar diversity and more abundant Cladophora and seagrass but with less epiphytes), with a subsequent adjusted herbivory by sea urchins that is reduced on a thicker seagrass and its epiphytes and amplified on the higher-palatable green algae Cladophora and Flabellia. Predatory fish populations double their abundances under acidified conditions. Lower habitat structural complexity at vents (i.e. lower seagrass canopy height due to an intense fish herbivory, and lower rhizome layer) is counteracted by a higher shoot density in terms of refuge provision. No change in sea urchin abundance is detected. Arrows represent direct trophic interactions (solid lines numbered as 1: herbivory, 2: predation) and indirect interactions (dashed line numbered as 3: fish herbivory as modifier of habitat structure, namely the seagrass canopy height), being the width of the arrow proportional to the strength of the interaction. Altered interactions (numbers and arrows) in acidified conditions are highlighted in red. Images were courtesy of the Integration and Application Network (ian.umces.edu/symbols/) or generated by BMC using SigmaPlot v11.1.
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