Elsevier

Marine Pollution Bulletin

Volume 158, September 2020, 111404
Marine Pollution Bulletin

Positive effects of high salinity can buffer the negative effects of experimental warming on functional traits of the seagrass Halophila ovalis

https://doi.org/10.1016/j.marpolbul.2020.111404Get rights and content

Highlights

  • High temperature adversely affects H. ovalis at biochemical and physiological level.

  • Increased salinity has no negative effects on Halophila ovalis plant performance.

  • The simultaneous occurrence of warming and high salinity shows interactive effects.

  • High salinities seem to buffer the impacts of transient warming.

Abstract

Coastal ecosystems, and especially estuaries, are subject to environmental fluctuations that can be amplified by anthropogenic changes. Under a future scenario of global warming, temperature and salinity are likely to be altered and the persistence of macrophyte-dominated ecosystems can be compromised, particularly native or local seagrass communities. This study examined the response of the local seagrass Halophila ovalis to the joint effect of a short-term salinity increase and a transient temperature stress, through two mesocosm experiments. Warming caused a decline in Fv/Fm, TNC content in leaves and plant growth, and increased dark respiration, revealing clear detrimental symptoms of heat stress on plant metabolism and performance. Salinity increase in isolation favoured ramet survival. However, in combination with warming, salinity had a positive effect on Gross Pmax. This suggests that increased salinities might dampen the negative effects of high temperatures, buffering, to some extent, the impact of global warming in temperate estuaries.

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 (Psingle bondI) 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

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