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Physiological tipping points to light reduction underlie seagrass population collapse and abrupt shift in a shallow coastal lagoon

Lazaro Marín-Guirao1*, Jaime Bernardeau-Esteller1, Maria Dolores Belando1, Ismael Cerezo1, Emilio Pérez1, Aranzazu Ramos1, Rocio G. Muñoz1 and Juan Manuel Ruiz1
  • 1 Oceanographic Center of Murcia, Spanish Institute of Oceanography, Spain

Tipping points are events where small changes in environmental conditions cause rapid and extensive ecological change. These ecological phase-shifts generally occur when environmental control variables exceed some thresholds, but the actual mechanisms driving this abrupt changes are often unknown (Scheffer et al., 2001). At the ecosystem level, feedback mechanisms play a major role in nonlinear responses of natural systems to environmental changes. Positive and negative feedback mechanisms can stabilize and destabilize ecosystems, which create potential for alternative and potentially stable states. At the organismal level, phenotypic plasticity could also be important for buffering ecological tipping points, although current discussions of the concept of tipping points seldom incorporate the physiological performance of the constituent organisms (Harley et al., 2017). These physiological approaches are particularly relevant in ecosystems dominated by habitat-forming species, since the extinction of a single species has an overall impact on the functioning of the ecosystem and its integrity. The Mar Menor is one of the biggest coastal lagoons in the Mediterranean area. The lagoon underwent a recent phase-shift, where a clear-water, macrophyte-dominated state gave way to a turbid-water, plankton-dominated state via eutrophication (Pérez-Ruzafa et al., 2019). In the spring 2016, an abrupt increase in nutrients and chlorophyll a concentration was detected, producing a dramatic loss of water transparency. These abnormal turbidity conditions remained for at least one year, resulting, after several months, in the massive die-off of the benthic vegetation dominated by the macrophytes Cymodocea nodosa and Caulerpa prolifera (Belando et al. 2017). In this study, we aimed to explore the physiological basis underlying the ecological regime shift in the Mar Menor by studying the phenotypic plasticity of the dominant species C. nodosa to the loss of water transparency. The hypothesis is that the observed ecological tipping point in the lagoon is explained by nonlinearities in how light reduction is translated into physiological responses, and how those drive population dynamics that affect ecosystem-level patterns. We used a field gradient design experiment to capture nonlinearities of the physiological responses in the species (Kreyling et al., 2018). Nine shading treatments were applied to a shallow (1 m depth) C. nodosa meadow by using neutral density screens. The selected light treatments encompassed a broad range of light availabilities: from 26% of subsurface irradiance (I0; 29.9 mol quanta m-2 d-1) in controls to 96% of I0(2.3 mol quanta m-2 d-1) in the most intense treatment. Changes in meadow structure (shoot density, meadow cover and plant biomass) were followed for the six-month duration of the experiment to characterize nonlinear population responses and the level of light reduction at which C. nodosa population start to decline. Morphological and (photo-)physiological plant responses were analyzed after two months of experimental shading for detecting and quantifying nonlinear trait responses that may underlie population collapse and ecological abrupt phase transition. Our results revealed that Cymodocea nodosa is able to maintain high plant density and biomass up to a light reduction of about 75% of subsurface irradiance (Figure 1), thanks to the activation of physiological mechanisms for plant acclimation to low light. Plastic plant traits contributing to this “homeostatic” population response included changes in canopy height, leaf concentration of photosynthetic pigments and reduction in the saturation irradiance (Ek) of shaded plants, among others. The integration of such complex responses resulted in an almost unaltered daily carbon balance of shaded plants, which favored the preservation of their energy reserves (i.e. total non-structural carbohydrates concentration in rhizomes; Figure 2). Figure 1. Shoot density (B) and total plant biomass (C) in each of the nine light reduction treatments at the end of the experiment. Further light reductions (>75%I0), however, drastically reduced the standing biomass of the population and significantly increased plant mortality rates (Figure 1), most likely due to the nonlinearity of some physiological responses. Gross-photosynthesis slowly decreased with decreasing irradiance, but this trend was four times stronger when light reduction exceeded this light threshold. Respiration was another key physiological trait, and showed a strong reduction at the same light threshold, which allowed plants to maintain their daily carbon balance unaltered (Figure 2). However, respiration cannot be further reduced under more intense shading, with direct consequences on the plant carbon balance and hence, on the energetic status of plants (Figure 2). Figure 2. Respiratory rates (B) and total non-structural carbohydrates concentration in rhizomes of C. nodosa from the nine light reduction treatments of the experiment. Our findings evidenced that the nonlinear physiological responses of C. nodosa to turbidity may be underlying the regime shift in this coastal ecosystem. The high phenotypic plasticity of C. nodosa to light reduction is one of the main mechanisms that would explain the high resilience of the coastal lagoon to decades of eutrophication. Plants are able to activate successful acclimative (homeostatic) mechanisms to buffer population responses (e.g. shoot density, plant biomass) to light reductions up to 75% of the natural/undisturbed levels. However, higher light reductions exceed the limits of physiological plasticity in the species, when plants revealed a marked steeping in their responses and where small increments in light reduction provoked profound changes in the population structure. We concluded that, understanding the mechanisms underlying the complex interaction between changes in the environment (e.g. light reduction) and organismal (physiological) and ecological (community) responses is critical if we are to predict ecosystem tipping points, mainly in those systems dominated by foundation species.

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Acknowledgements

This study is part of the UMBRAL project (Ref. CTM2017-86695-C3-2-R)funded by the National Research Programme of the Spanish Ministry of Science, Innovation and University.

References

Belando, M.D., Bernardeau-Esteller, J., García-Muñoz, R., Ramos-Segura, A., Santos-Echeandía, J., García-Moreno, P., Carreño, F. y Ruiz, J.M. 2017. Evaluación del estado de conservación de las praderas de Cymodoceanodosa en la laguna costera del Mar Menor. 2014-2016. Informe del Instituto Español de Oceanografía y la Asociación de Naturalistas del Sureste. Murcia. 157pp. Harley C.D.G., Connell S.D., Doubleday Z.A., Kelaher, B., Russell, B.D., Sarà, G., Helmuth, B. 2017. Conceptualizing ecosystem tipping points within a physiological framework. Ecology and Evolution, 7:6035–6045. https://doi.org/10.1002/ece3.3164 Kreyling, J., Schweiger, A.H., Bahn, M., Ineson, P., Migliavacca, M., Morel‐Journel, T., Christiansen, J.R., Schtickzelle, N., Larsen, K.S. 2018. To replicate, or not to replicate – that is the question: how to tackle nonlinear responses in ecological experiments. EcologyLetters, 21: 1629-1638. doi:10.1111/ele.13134 Pérez-Ruzafa, A., Campillo, S., Fernández-Palacios, J.M. et al. 2019. Long-term dynamic in nutrients, chlorophyll a, and water quality parameters in a coastal lagoon during a process of eutrophication for decades, a sudden break and a relatively rapid recovery. Frontiers in Marine Science, 6:26. https://doi.org/10.3389/fmars.2019.00026 Scheffer, M., Carpenter, S., Foley, J.A., Folke, C., Walker, B. 2001. Catastrophic shifts in ecosystems. Nature, 413, 591–596.https://doi.org/10.1038/35098000

Keywords: Critical transition, Nonlinear responses, turbidity, foundation species, Cymodocea nososa

Conference: XX Iberian Symposium on Marine Biology Studies (SIEBM XX) , Braga, Portugal, 9 Sep - 12 Sep, 2019.

Presentation Type: Poster Presentation

Topic: Ecology, Biodiversity and Vulnerable Ecosystems

Citation: Marín-Guirao L, Bernardeau-Esteller J, Belando M, Cerezo I, Pérez E, Ramos A, Muñoz RG and Ruiz J (2019). Physiological tipping points to light reduction underlie seagrass population collapse and abrupt shift in a shallow coastal lagoon. Front. Mar. Sci. Conference Abstract: XX Iberian Symposium on Marine Biology Studies (SIEBM XX) . doi: 10.3389/conf.fmars.2019.08.00181

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Received: 19 May 2019; Published Online: 27 Sep 2019.

* Correspondence: Dr. Lazaro Marín-Guirao, Oceanographic Center of Murcia, Spanish Institute of Oceanography, Murcia, Spain, maringuirao@gmail.com