Positive effects of high salinity can buffer the negative effects of experimental warming on functional traits of the seagrass Halophila ovalis
Introduction
Global change is threatening ecosystems worldwide (Bellard et al., 2012; IPCC, 2014) and is considered a major driver of the erosion of marine biodiversity (Poloczanska et al., 2013). Coastal ecosystems are particularly vulnerable to global change because they are exposed to a range of cumulative impacts, including, eutrophication, physical alterations, pollution and overfishing, all strongly linked to human population pressures on the coast in addition to climate change impacts (Halpern et al., 2015; Orth et al., 2006). Increased temperatures due to global warming and heatwaves (Smale et al., 2019) can impact coastal ecosystems, often in additive or synergistic ways with other stressors (e.g. Humanes et al., 2016; Ontoria et al., 2019a). This is of particular concern for ecosystem engineers, such as habitat forming corals, mangroves or seagrasses, due to the major cascading effects on biodiversity and ecosystem functions (Smale et al., 2019) including primary production, fisheries provision, carbon sinks and buffering acidification (Beaumont et al., 2007).
Estuaries are subject to environmental fluctuations, both gradual and abrupt. These pose significant physical forcing and influence ecological relationships (Day et al., 2012) making estuaries particularly vulnerable to climate change (Hallett et al., 2018). Organisms inhabiting estuaries generally tolerate salinity changes using a range of ecophysiological mechanisms via different metabolic pathways (Gupta and Huang, 2014). With progressive warming and heat waves, evaporation rates from estuaries are likely to increase, resulting in increases in salinity, especially where flushing with fresh or marine water is limited. These two physical factors, temperature and salinity, are likely to impact estuarine ecosystems beyond the range of variation already experienced (Hallett et al., 2018).
Seagrasses, one of the most productive ecosystems on Earth (Hemminga and Duarte, 2000) and highly valued economically and ecologically (Orth et al., 2006), are a dominant habitat in estuaries. Temperature clearly effects seagrass plant performance across a range of scales, from the molecular to population level (Campbell et al., 2006; Marín-Guirao et al., 2017; Ruiz et al., 2018; Ruocco et al., 2019). They are sensitive and vulnerable to warming (e.g. Strydom et al., 2020) with negative effects on plant performance (e.g. Collier et al., 2011; Ontoria et al., 2019a) and survival (Díaz-Almela et al., 2009) documented. Changes in salinity also alter seagrass physiological functioning and, consequently, influence plant growth and survival (Sandoval-Gil et al., 2012a; Salo and Pedersen, 2014; Salo et al., 2014; Touchette and Burkholder, 2000). Seagrass die-off has been observed with hypersalinity events (Wilson and Dunton, 2018). However, despite the recent increasing interest in interactions between thermal and salinity tolerance thresholds and acclimation mechanisms, this is still poorly understood for seagrasses, particularly with hypersalinity. Temperature increases could affect plant performance not only directly but also through its interaction with plant tolerance mechanisms to changes in salinity (Piro et al., 2015). The higher respiratory demand under hypersaline conditions (Johnson et al., 2018) could lead to synergistic impacts with temperature.
Estuaries in Mediterranean climate regions, such as southwestern Australia, experience high temperatures and elevated salinities in summer and these are predicted to increase with climate change (Hallett et al., 2018). Halophila ovalis is one of the most common seagrass species found in estuaries of southwestern Australia. It is a fast growing, colonizing species (sensu Kilminster et al., 2015) with a clear ability to recover quickly from disturbances. H. ovalis has a wide tolerance range, occurring in waters between 10 °C and 40 °C (Ralph, 1998) and from 5 to 45 psu (Hillman, 1995; Tyerman, 1982), which coincides with its broad distribution and abundance in estuarine environments. Previous short-term experiments (five days, Ralph, 1998) with laboratory-cultured plants revealed that while H. ovalis has its optimum photosynthetic range between 25 and 30 °C, its tolerance to salinity can range from 9 to 52 psu. However, there is a lack of knowledge about the responses to periods longer than five days to each one of these factors, as well as about their potential interaction.
The present study aims to explore the response of an estuarine seagrass, H. ovalis, to warming and salinity changes linked to climate change and, specifically, to assess whether temperature increases affect plant tolerance to salinity fluctuations. To do this, two indoor mesocosm experiments were performed to evaluate plant responses to changing salinity under thermal increase, at the physiological, individual and population levels. We hypothesize that the simultaneous occurrence of warming and high salinities will lead to deleterious effects on plant performance.
Section snippets
Material and methods
The response of H. ovalis to increases in temperature under different salinity conditions was assessed through two independent mesocosms experiments, thus evaluating the responses not only to short-term (1 day) but also to medium-term (13 days) temperature and salinity exposure. The two experiments were required to enable measurements across a range of plant scales: physiological, individual and population levels and also with a range of treatments that were not possible in a single experiment
Experiment A: Photosynthesis-irradiance curves
Typical Michaelis-Menten-like curves with no photoinhibition were observed in each experimental condition for the H. ovalis plants (Fig. 1). All of the photosynthetic parameters extracted from the photosynthesis-irradiance (PI) curves were significantly affected by the experimental factors, either temperature only, salinity only, both and/or an interaction between the two (Fig. 2, Table 1). Maximum gross photosynthesis values ranged from 2.6 to 6.6 mg O2 g DW−1 h−1, and were significantly
Discussion
In this work, the response of H. ovalis to temperature and salinity, both individually and in combination, was assessed in two indoor mesocosm experiments. Overall, our exploratory results show negative effects of the high temperatures but, interestingly, high salinities seem to buffer, to some extent, the impacts of short-term warming.
Symptoms of thermal stress were detected in most plant traits evaluated. The sensitivity of the photosynthetic apparatus to warming was reflected by the decline
Conclusions
The assessment of the effects of global change on ecosystems in fluctuating environments is a relatively unexplored field of research. Based on our findings, H. ovalis populations living in variable salinity environments, such as in the estuaries of southwestern Australia, may be negatively impacted by more frequent and extreme warming events. Extrapolating these exploratory results to real world, suggest that if warming, in turn, results in high salinity conditions through increased
CRediT authorship contribution statement
Y. Ontoria:Conceptualization, Methodology, Formal analysis, Investigation, Writing - original draft.C. Webster:Conceptualization, Methodology, Investigation, Writing - review & editing.N. Said:Methodology, Investigation, Writing - review & editing.J.M. Ruiz:Resources, Writing - review & editing.M. Pérez:Resources, Validation, Writing - original draft.J. Romero:Resources, Validation, Writing - original draft.K. McMahon:Conceptualization, Methodology, Formal analysis, Investigation, Resources,
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank Caitlyn O'Dea, Sian McNamara and Elena Álvarez for their help in the field and laboratory. Laboratory facilities were provided by School of Science and Centre for Marine Ecosystems Research at ECU. We thank Department of Water and Environmental Regulation staff Dr. Kieryn Kilminster, Marta Sánchez Alarcón and Katherine Bennett for logistical and in-kind support of this project. Carbohydrates analysis were performed at the Oceanographic Center of Murcia (Spanish Institute of
References (65)
- et al.
Identification, definition and quantification of goods and services provided by marine biodiversity: implications for the ecosystem approach
Mar. Pollut. Bull.
(2007) - et al.
Measuring rates of photosynthesis of two tropical seagrasses by pulse amplitude modulated (PAM) fluorometry
Aquat. Bot.
(2000) - et al.
Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature
J. Exp. Mar. Biol. Ecol.
(2006) - et al.
Temperature extremes reduce seagrass growth and induce mortality
Mar. Pollut. Bull.
(2014) The distribution, biomass and primary production of the seagrass Halophila ovalis in the Swan/Canning Estuary, Western Australia
Aquat. Bot.
(1995)- et al.
Effects of nitrogen addition on nitrogen metabolism and carbon reserves in the temperate seagrass Posidonia oceanica
J. Exp. Mar. Biol. Ecol.
(2004) - et al.
Hypersalinity as a trigger of seagrass (Thalassia testudinum) die-off events in Florida Bay: evidence based on shoot meristem O2 and H2S dynamics
J. Exp. Mar. Biol. Ecol.
(2018) - et al.
Unravelling complexity in seagrass systems for management: Australia as a microcosm
Sci. Total Environ.
(2015) - et al.
Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review
J. Exp. Mar. Biol. Ecol.
(2007) - et al.
Photosynthesis, growth and survival of the Mediterranean seagrass Posidonia oceanica in response to simulated salinity increases in a laboratory mesocosm system
Estuar. Coast. Shelf Sci.
(2011)
Responses of the Mediterranean seagrass Posidonia oceanica to hypersaline stress duration and recovery
Mar. Environ. Res.
Carbon economy of Mediterranean seagrasses in response to thermal stress
Mar. Pollut. Bull.
Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance
Mar. Pollut. Bull.
Interactive effects of global warming and eutrophication on a fast-growing Mediterranean seagrass
Mar. Environ. Res.
The rise and fall of the “marine heat wave” off Western Australia during the summer of 2010/2011
J. Mar. Syst.
Experimental evidence of warming-induced flowering in the Mediterranean seagrass Posidonia oceanica
Mar. Pollut. Bull.
Synergistic effects of altered salinity and temperature on estuarine eelgrass (Zostera marina) seedlings and clonal shoots
J. Exp. Mar. Biol. Ecol.
Population specific salinity tolerance in eelgrass (Zostera marina)
J. Exp. Mar. Biol. Ecol.
The effect of salinity increase on the photosynthesis, growth and survival of the Mediterranean seagrass Cymodocea nodosa
Estuar. Coast. Shelf Sci.
Ecophysiological plasticity of shallow and deep populations of the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa in response to hypersaline stress
Mar. Environ. Res.
Effects of salinity on photosynthesis and respiration of the seagrass Zostera japonica: a comparison of two established populations in North America
Aquat. Bot.
Response of the seagrass Halophila ovalis to altered light quality in a simulated dredge plume
Mar. Pollut. Bull.
Seagrass-salinity interactions: physiological mechanisms used by submersed marine angiosperms for a life at sea
J. Exp. Mar. Biol. Ecol.
Overview of the physiological ecology of carbon metabolism in seagrasses
J. Exp. Mar. Biol. Ecol.
Investigating cellular stress response to heat stress in the seagrass Posidonia oceanica in a global change scenario
Mar. Environ. Res.
Antioxidant response to heat stress in seagrasses. A gene expression study
Mar. Environ. Res.
A new method for non parametric multivariate analysis of variance
Aust. Ecol.
PERMANOVAþ for PRIMER: Guide to Software and Statistical Methods
Impacts of climate change on the future of biodiversity
Ecol. Lett.
Simulating light-saturation curves for photosynthesis and calcification by reef-building corals
Mar. Biol.
Primer v6: User Manual/Tutorial. Primer-E, Plymouth
Thermal tolerance of two seagrass species at contrasting light levels: implications for future distribution in the Great Barrier Reef
Limnol. Oceanogr.
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