Elsevier

Marine Pollution Bulletin

Volume 134, September 2018, Pages 14-26
Marine Pollution Bulletin

Interactive effect of temperature, acidification and ammonium enrichment on the seagrass Cymodocea nodosa

https://doi.org/10.1016/j.marpolbul.2018.02.029Get rights and content

Highlights

  • A significant synergy can occur when several environmental factors interact.

  • Warming positively affect plant production but at expense of reducing carbon reserves.

  • Loss leaf rates increased with ammonium supply

  • CO2 increase did not produce significant effects.

  • Future scenarios may benefit to C. nodosa improving their growth and carbon reserves.

Abstract

Global (e.g. climate change) and local factors (e.g. nutrient enrichment) act together in nature strongly hammering coastal ecosystems, where seagrasses play a critical ecological role. This experiment explores the combined effects of warming, acidification and ammonium enrichment on the seagrass Cymodocea nodosa under a full factorial mesocosm design. Warming increased plant production but at the expense of reducing carbon reserves. Meanwhile, acidification had not effects on plant production but increased slightly carbon reserves, while a slight stimulation of net production and a slight decrease on carbon reserves under ammonium supply were recorded. When all the factors were combined together improved the production and carbon reserves of Cymodocea nodosa, indicating that acidification improved ammonium assimilation and buffered the enhanced respiration promoted by temperature. Therefore, it could indicate that this temperate species may benefit under the simulated future scenarios, but indirect effects (e.g. herbivory, mechanical stress, etc.) may counteract this balance.

Introduction

In the last century, human activities have triggered changes at a global scale that are affecting ecosystems worldwide, with coastal vegetated ecosystems being one of the most threatened (Large, 2009). These ecosystems are expected to come under increased pressure from climate change and direct anthropogenic factors in the next decades, (Nicholls et al., 2007). In coastal vegetated habitats worldwide, seagrasses (i.e. marine flowering plants) form extensive meadows in intertidal and subtidal environments. These habitats are increasingly recognised for their ecological function and provisioning of human services, including nutrient regeneration (Costanza et al., 1997), water quality improvement (Waycott et al., 2005), reduction in human and wildlife pathogens (Lamb et al., 2017; Sullivan et al., 2017), shoreline protection (Bos et al., 2007; Christianen et al., 2013), suitable breeding habitats (including those for economically relevant species; Cullen-Unsworth et al., 2014), biodiversity hotspots (Duffy, 2006; González-Ortiz et al., 2014a) and carbon sequestration (Fourqurean et al., 2012). These keystone habitats thus are considered one of the richest and most relevant ecosystems worldwide (Ruiz-Frau et al., 2017; Short et al., 2011), with high economic value for humans (e.g. Campagne et al., 2014). This importance is recognised worldwide by different legislations and international conventions like the Convention on Biological Diversity (1992) or the European Habitats Directive (92/43/EEC). Favoured by this legislative framework, seagrass habitats have been specifically targeted for conservation and restoration (Green and Short, 2004). Regrettably, the proximity of seagrasses to anthropogenic littoral impacts and their shallow distribution in estuarine and coastal areas have led to widespread seagrass losses, with a global decline of 7% yr−1 (Waycott et al., 2009) and almost 14% of all seagrass species currently endangered (Short et al., 2011). Therefore, it is crucial to understand the responses of these ecosystems to multiple co-stressors in order to provide sound advice on managing for possible future trajectories (Brierley and Kingsford, 2009; Hoegh-Guldberg and Bruno, 2010; Unsworth et al., 2014).

Climatic change effects (e.g. increase in temperature, seawater acidification, frequency of storms, sea level rise, etc.) in combination with coastal anthropogenic and natural stressors (e.g. nutrient load, changes in salinity and littoral current, diseases, etc.) act together in coastal areas, and their effects are expected to increase in the near future (Halpern, 2014; Nicholls et al., 2007). Increased CO2 concentration in the air and subsequent solubility in seawater reduces pH and modifies the balance of the different dissolved carbonate species (Zeebe and Wolf-Gladrow, 2001; Koch et al., 2013). Partial pressure of carbon dioxide in water is raised under such conditions, which can benefit seagrass primary production as seagrass photosynthesis is generally considered to be carbon limited (Beer et al., 1980; Beardall et al., 1998; Beer and Koch, 1996; Invers et al., 2001). Thus, higher CO2 is predicted to lead to higher photosynthesis, growth rates, biomass (Hall-Spencer et al., 2008; Jiang et al., 2010; Palacios and Zimmerman, 2007; Short and Neckles, 1999; Takahashi et al., 2016; Zimmerman et al., 1997) and internal non-structural carbohydrates (NSC) concentrations (Campbell and Fourqurean, 2013; Egea et al., 2018; Garrard and Beaumont, 2014; Zimmerman et al., 1997), in the absence of other factors limiting the growth (e.g. nutrients, light). However, it is important to note that extrapolating laboratory results to predict long-term responses in seagrasses is not always easy, since some long-term experiments have shown no significant changes in biomass, shoot density and/or growth rates under CO2 enrichment (Alexandre et al., 2012; Campbell and Fourqurean, 2013; Cox et al., 2016; Palacios and Zimmerman, 2007).

Several studies have highlighted the importance of temperature in the seagrass metabolism and in the maintenance of a positive carbon balance, since warmer temperatures favour photosynthesis and respiration through their effects on kinetic reactions and metabolism (Evans et al., 1986; Pérez and Romero, 1992; Zimmerman et al., 1989). Some previous experiments have demonstrated that warmer temperature may benefit the flowering (Ruiz et al., 2017), growth and biomass of seagrass species (under high saturating light conditions; Bulthuis, 1987), while reducing the reserves of non-structural carbohydrates through enhancing respiration (Hernán et al., 2017). However, other studies have shown negative effects on plants (Collier and Waycott, 2014; Jordà et al., 2012; Moreno-Marin et al., 2018; Repolho et al., 2017). The final effect will depend on the thermal tolerance of a species and its optimal temperature for photosynthesis, respiration, and growth (Bulthuis, 1987; Collier et al., 2011; Masini and Manning, 1997; Short and Neckles, 1999).

In addition to these variables affected by climate change, the current increase in nutrient load in coastal waters has been identified as a key factor that has the potential to negatively impact seagrass meadows (Antón et al., 2011; Burkholder et al., 2007; Cabaço et al., 2008; Hughes et al., 2004). Several reports have indicated that moderate increases in nutrient load may stimulate seagrass production and biomass (Alcoverro et al., 1997; Jiménez-Ramos et al., 2017a; Pérez et al., 1991; Short, 1987; Udy et al., 1999). However, under conditions of high nitrogen availability, direct ammonium toxicity can curtail plant growth, biomass and survival (Brun et al., 2002; van Katwijk et al., 1997). As with temperature, the net outcome will depend on the effects of nutrient load on the photosynthesis rates and non-structural carbohydrate reserves, which are needed for a rapid ammonium assimilation (Brun et al., 2008; Villazán et al., 2013a).

These three factors directly affect photosynthetic rate, plant production, biomass and non-structural carbohydrate reserves. However, while CO2 enrichment may have either a positive effect or no effect on seagrasses, temperature and nutrient enrichment may cause positive or negative effects. The net response may depend on the species, the physiological status of the plants and, notably, the interaction between these factors. For instance, higher CO2 may benefit plants subject to higher temperatures because both the higher photosynthetic and respiration rates expected under higher temperature can benefit from elevated CO2 levels (e.g. reducing the carbon limitation; Ow et al., 2016; Zimmerman et al., 1997), higher levels of non-structural carbohydrates (e.g. needed for respiration processes; Campbell and Fourqurean, 2013) and higher biomass (e.g. more photosynthetic tissues; Jiang et al., 2010; Palacios and Zimmerman, 2007; Russell et al., 2013). In contrast, warmer temperature may have a detrimental effect on plants subjected to ammonium enrichment because of the decrease in non-structural carbohydrate reserves due to enhanced respiration rates, as demonstrated by van Katwijk et al. (1997) and Moreno-Marin et al. (2018). However, CO2 enrichment may counterbalance this negative interaction to some extent, because of its associated enhanced rates in photosynthetic and higher non-structural carbohydrate reserves, which are known to reduce ammonium toxicity symptoms (Brun et al., 2002, Brun et al., 2008). In addition, higher nutrient levels (mainly nitrogen) may be beneficial under elevated CO2 levels, since the resulting higher photosynthesis and growth rates increase the demand for nutrients (Coskun et al., 2016; Stitt and Krapp, 1999).

Therefore, while the plant response to a single factor can be well described and predicted, the combination of multiple factors acting together under natural conditions can induce a complex response difficult to predict, as plants may exhibit non-additive responses when exposed to multiple stressors (Gunderson et al., 2016; Moreno-Marin et al., 2018). Non-additive effects may be antagonistic (i.e. the combined effect is less than the expected additive effect) or synergistic (i.e. greater than the expected additive effect). Some previous works have found mainly non-additive responses when using a multifactorial design with some of the aforementioned stressors (warmer temperature, enhanced CO2, ammonium enrichment) (Brun et al., 2008; Burnell et al., 2013; Collier et al., 2011; De los Santos et al., 2010; Egea et al., 2018; Jiménez-Ramos et al., 2017b; Koch et al., 2013; La Nafie et al., 2012; Lee et al., 2007; Moreno-Marín et al., 2016, Moreno-Marin et al., 2018; Repolho et al., 2017; Salo and Pedersen, 2014; Villazán et al., 2013a). Therefore, if plants have a non-additive response, predicting the effects of environmental change from single factor experiments may under- or overestimate the combined effect of multiple stressors.

This work aims to study the response of a temperate seagrass (Cymodocea nodosa) to the forecasted global change factors (high temperature, CO2 increase and ammonium enrichment) using a multifactorial mesocosm experiment, testing whether the combined effects of these stressors are additive or non-additive. Based on previous studies, we hypothesize that the combination of the three factors will have a positive effect on plant production and biomass, while non-structural carbohydrates will be reduced because of their depletion by ammonium assimilation and the enhanced respiratory processes promoted by higher temperature. In addition, we predict that most of the factor combinations will produce non-additive responses.

Section snippets

Field plant collection

Individual shoots of Cymodocea nodosa (Ucria) Ascherson were randomly collected from a depth of 1–2 m in submerged seagrass meadows at Cadiz Bay (southern Spain, 36°29′19.79”N; 6°15′53.05″E). Healthy looking vertical shoots with intact rhizomes were transported to the laboratory within 2 h of collection in an ice chest. Once in the laboratory, a large pool of experimental shoots were selected bearing similar lengths, numbers of leaves and roots, and they were cleaned of visible epiphytes. They

Ammonium concentration in seawater

Generally, the added ammonium was effectively removed by the plants during the experiment under the control temperature and NH4+ enrichment treatment combinations (Fig. 2A). However, some ammonium did accumulate in the seawater in the treatment high temperature + control pH during the first days of the experiment. The highest accumulation level was recorded in the treatment high temperature + forecasted pH during the first two weeks of the experiment (4–6 μM NH4+; Fig. 2B).

Effects on plant production

No dead plants were

Discussion

Ecological experiments may target the integrated responses of individuals to experimental factors or seek underlying mechanisms to explain such responses (Irschick et al., 2013). In the present study, the response of Cymodocea nodosa to the assayed stressors was analysed using a set of response variables that integrated the final response at the plant level (i.e. survival, GPR, NPR and LLR) and some of the main indicators of responses at the physiological level (i.e. non-structural

Conclusions

Our study shows that although some of the environmental factors studied in this experiment may produce a limited response in Cymodocea nodosa when acting alone (CO2 increase and NH4+ enrichment), the combined effect of the three factors triggered a positive response of this seagrass specie. Overall productivity was improved in this species, as were NSC concentrations, which may improve plant resistance to other stressors. In this case, we predict a positive response of C. nodosa to the

Acknowledgments

This work was supported by the Excelence Project of the Junta Andalucia RNM-P12-3020 (PRODESCA), the Spanish national project CTM2011-24482 (SEA-LIVE), and the Spanish Ministry of Education [FPU12/05055 grant awarded to L.G. Egea]. We thank N. Garzón (CACYTMAR) for laboratory assistance.

References (131)

  • L.C. Cullen-Unsworth et al.

    Seagrass meadows globally as a coupled social-ecological system: implications for human wellbeing

    Mar. Pollut. Bull.

    (2014)
  • A.G. Dickson et al.

    A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media

    Deep Sea Res. Part A

    (1987)
  • E.A. Drew

    Factors affecting photosynthesis and its seasonal variation in the seagrasses Cymodocea nodosa (Ucria) archers. and Posidonia oceanica (L.) Delile in the Mediterranean

    J. Exp. Mar. Biol. Ecol.

    (1978)
  • A.S. Evans et al.

    Photosynthetic temperature acclimation in two coexisting seagrasses, Zostera marina L. and Ruppia maritima L

    Aquat. Bot.

    (1986)
  • S.L. Garrard et al.

    The effect of ocean acidification on carbon storage and sequestration in seagrass beds; a global and UK context

    Mar. Pollut. Bull.

    (2014)
  • V. González-Ortiz et al.

    Effects of two antagonistic ecosystem engineers on infaunal diversity

    Estuar. Coast. Shelf Sci.

    (2014)
  • O. Invers et al.

    Effects of pH on seagrass photosynthesis: a laboratory and field assessment

    Aquat. Bot.

    (1997)
  • O. Invers et al.

    Bicarbonate utilization in seagrass photosynthesis: role of carbonic anhydrase in Posidonia oceanica (L.) Delile and Cymodocea nodosa (Ucria) Ascherson

    J. Exp. Mar. Biol. Ecol.

    (1999)
  • O. Invers et al.

    Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation of bicarbonate use in species inhabiting temperate waters

    J. Exp. Mar. Biol. Ecol.

    (2001)
  • O. Invers et al.

    Effects of nitrogen addition on nitrogen metabolism and carbon reserves in the temperate seagrass Posidonia oceanica

    J. Exp. Mar. Biol. Ecol.

    (2004)
  • R. Jiménez-Ramos et al.

    Resistance to nutrient enrichment varies among components in the Cymodocea nodosa community

    J. Exp. Mar. Biol. Ecol.

    (2017)
  • K.S. Lee et al.

    Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review

    J. Exp. Mar. Biol. Ecol.

    (2007)
  • R.J. Masini et al.

    The photosynthetic responses to irradiance and temperature of four meadow-forming seagrasses

    Aquat. Bot.

    (1997)
  • M. Pérez et al.

    Photosynthetic response to light and temperature of the seagrass Cymodocea nodosa and the prediction of its seasonality

    Aquat. Bot.

    (1992)
  • T. Alcoverro et al.

    Spatial and temporal variations in nutrient limitation of seagrass Posidonia oceanica growth in the NW Mediterranean

    Mar. Ecol. Prog. Ser.

    (1997)
  • A. Alexandre et al.

    Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii

    Ecol. Evol.

    (2012)
  • A. Antón et al.

    Decoupled effects (positive to negative) of nutrient enrichment on ecosystem services

    Ecol. Appl.

    (2011)
  • T. Arnold et al.

    Ocean acidification and the loss of phenolic substances in marine plants

    PLoS One

    (2012)
  • J. Beardall et al.

    Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance

    Bot. Mar.

    (1998)
  • S. Beer et al.

    Photosynthesis of marine macroalgae and seagrasses in globally changing CO2 environments

    Mar. Ecol. Prog. Ser.

    (1996)
  • S. Beer et al.

    Carbon metabolism in seagrasses

    J. Exp. Bot.

    (1980)
  • C.E. Bower et al.

    A salicylate–hypochlorite method for determining ammonia in seawater

    Can. J. Fish. Aquat. Sci.

    (1980)
  • F.G. Brun et al.

    Assessing the toxicity of ammonium pulses to the survival and growth of Zostera noltii

    Mar. Ecol. Prog. Ser.

    (2002)
  • F.G. Brun et al.

    Effect of shading by Ulva rigida canopies on growth and carbon balance of the seagrass Zostera noltii

    Mar. Ecol. Prog. Ser.

    (2003)
  • F.G. Brun et al.

    Increased vulnerability of Zostera noltii to stress caused by low light and elevated ammonium levels under phosphate deficiency

    Mar. Ecol. Prog. Ser.

    (2008)
  • M.K. Burke et al.

    Non-structural carbohydrate reserves of eelgrass Zostera marina

    Mar. Ecol. Prog. Ser.

    (1996)
  • O.W. Burnell et al.

    Eutrophication offsets increased sea urchin grazing on seagrass caused by ocean warming and acidification

    Mar. Ecol. Prog. Ser.

    (2013)
  • C.S. Campagne et al.

    The seagrass Posidonia oceanica: ecosystem services identification and economic evaluation of goods and benefits

    Mar. Pollut. Bull.

    (2014)
  • J.E. Campbell et al.

    Effects of in situ CO2 enrichment on the structural and chemical characteristics of the seagrass Thalassia testudinum

    Mar. Biol.

    (2013)
  • M.J.A. Christianen et al.

    Low-canopy seagrass beds still provide important coastal protection services

    PLoS One

    (2013)
  • P. Ciais et al.

    Carbon and other biogeochemical cycles

  • C.J. Collier et al.

    Thermal tolerance of two seagrass species at contrasting light levels: implications for future distribution in the great barrier reef

    Limnol. Oceanogr.

    (2011)
  • Convention on Biological Diversity
  • D. Coskun et al.

    Measuring fluxes of mineral nutrients and toxicants in plants with radioactive tracers

    J. Vis. Exp.

    (2014)
  • R. Costanza et al.

    The value of the world's ecosystem services and natural capital

    Nature

    (1997)
  • T.E. Cox et al.

    Effects of in situ CO2 enrichment on structural characteristics, photosynthesis, and growth of the Mediterranean seagrass Posidonia oceanica

    Biogeosciences

    (2016)
  • E.S. Darling et al.

    Quantifying the evidence for ecological synergies

    Ecol. Lett.

    (2008)
  • C. De los Santos et al.

    Acclimation of seagrass Zostera noltii to co-occurring hydrodynamic and light stresses

    Mar. Ecol. Progr. Ser.

    (2010)
  • C.B. De los Santos et al.

    Leaf-fracture properties correlated with nutritional traits in nine Australian seagrass species:implications for susceptibility to hebivory

    Mar. Ecol. Prog. Ser.

    (2012)
  • C.B. De los Santos et al.

    A comprehensive analysis of mechanical and morphological traits in temperate and tropical seagrass species

    Mar. Ecol. Prog. Ser.

    (2016)
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