Elsevier

Science of The Total Environment

Volume 635, 1 September 2018, Pages 1132-1143
Science of The Total Environment

Evaluation of four seagrass species as early warning indicators for nitrogen overloading: Implications for eutrophic evaluation and ecosystem management

https://doi.org/10.1016/j.scitotenv.2018.04.227Get rights and content

Highlights

  • The first benchmark for seagrass as early warning indicator for nitrogen loads

  • Leaf C/N of eelgrass is used as eutrophic assessment at global and local scale.

  • Seagrasses respond differently to nitrogen loading in phenotype.

Abstract

Seagrasses are major coastal primary producers and are widely distributed on coasts worldwide. Seagrasses show sensitivity to environmental stress due to their high phenotypic plasticity, and therefore, we evaluated the use of constituent elements in four dominant seagrass species as early warning indicators for nitrogen eutrophication of coastal regions. A meta-analysis was conducted with published data to develop a global benchmark for the selected indicator, which was used to evaluate nitrogen loading at a global scale. A case study at three bays was subsequently conducted to test for local-scale differences in leaf C/N ratios in four seagrasses. Additionally, morphological and physiological metrics of seagrasses were measured from the three locations under varied nitrogen levels to develop further assessment indexes. The benchmark and local study showed that leaf C/N ratios of Zostera marina were sensitive to nitrogen discharge, which could be a highly valuable early warning indicator on a global scale. Moreover, the threshold value of seagrass leaf C/N was determined according to the benchmark to differentiate eutrophic and low nitrogen levels at a local scale. Of the eight phenotypic metrics measured, leaf width, total chlorophyll (a + b), chlorophyll ratio (a/b), and starch in the rhizome were the most effective at discriminating between the three locations and could also be promising indicators for monitoring eutrophication.

Introduction

Seagrass beds are recognized as important and productive types of coastal ecosystems, with providing valuable ecological and socioeconomic services such as nursery function, sediment stabilization, and carbon sequestration (Christianen et al., 2013; Short et al., 1993). However, as occurs in other marine ecosystems such as mangroves and coral reefs, seagrass beds are subjected to habitat fragmentation with degeneration in large areas due to climate change and anthropogenic disturbance (Cardoso et al., 2008). Globally, the areas of seagrass beds were estimated to be declined at an annual rate of 7% since 1990 (Waycott et al., 2009). Eutrophication is thought to be the primary stressor to influence distributions and functions of benthic primary producers (e.g., seagrass and seaweed) by stimulating explosive growth of phytoplankton, macroalgae, and epiphytic algae, which limit the light available to submerged macrophytes (Cardoso et al., 2004; Govers et al., 2014b). As the response of marine ecosystems to excessive nutrient release from anthropogenic activities, eutrophication is causing considerable concern worldwide (Gray et al., 2002; Elser et al., 2007). The nitrogen level has increased by >10-fold during the past century and a half primarily as a result of the increasing demand for reactive nitrogen in agriculture and in energy production (Galloway et al., 2008).

To understand the impact of eutrophication on the aquatic ecosystem, nutrient loading in different media (e.g., sediment, water, and organism) has been studied in estuarine and coastal regions worldwide (Duarte, 1990; Mohammed and Johnstone, 2002; Li et al., 2010; Bucholc et al., 2014). In situ monitoring of dissolved inorganic nutrient concentrations in seawater directly is ineffective, because nutrients are rapidly absorbed by phytoplankton and submerged macrophytes, in addition to the diluting and dissipative effects of hydrodynamic action in water (Lee et al., 2004). Sediments and pore water, which are sensitive to environmental changes and anthropogenic pressures, are generally considered the primary reservoirs for nutrients and organic contaminants and sensitive indicators for contamination of coastal environments (Engelsen et al., 2008; Yang et al., 2015). However, the adsorption capacity of sediments for pollutants is limited due to sediment-specific characteristics (e.g. grain size and organic matter content). Additionally, collection and conservation of pore water samples are difficult, particularly in estuaries and coastal zones (Martin et al., 2003). Bio-indicators, particularly sensitive species, can be efficient monitoring tools for estuarine and coastal pollution (Warwick and Pearson, 1987). Fast growth of macroalgae, drifting algal mats and nuisance algal blooms are widely acknowledged as indicators for the decline of water quality and are linked to excessive nutrient loading and mortality of perennial macrophytes (Norkko and Bonsdorff, 1996; O'Neill et al., 2015; Paerl et al., 2016). However, by the time these bio-indicators are visible, the functioning of the marine ecosystem may have been severely damaged (Kemp et al., 1983). Early detection of the effect increases the chance of preventing or reversing eutrophication. Candidate early warning indicators should be sensitive to small changes in a stressor and respond in a rapid and predictable manner. Timely detection by early warning indicators is essential to control and mitigate hazardous effects of seawater eutrophication (Gerbersdorf et al., 2015).

Seagrasses are sensitive to contaminants and show phenotypic plasticity in response to various environmental conditions (Orth et al., 2006; Lafabrie et al., 2007; Romero et al., 2007), and therefore are considered excellent bio-indicators for marine pollution (Macinnis-Ng and Ralph, 2004; Maxwell et al., 2014). Physiological, chemical and morphological responses of seagrasses show a close correlation with available nutrient resources (Lee et al., 2004; Zhang et al., 2014; Ben Brahim et al., 2015). An additional advantage of seagrasses as bio-indicators for eutrophication is their wide distribution and abundance along the coasts, and in estuaries, which provide good monitoring tools at both local and global scales. Previous studies primarily concentrate on the response of individual seagrass species to eutrophication pressure (Roca et al., 2015; Han et al., 2017; Hitchcock et al., 2017). Indicators from multiple species of seagrass should provide more objective indicators for evaluating the relationship between responses and pressures. Additionally, some argue against the efficiency of seagrasses because of differences in physiological structures and assimilative capacities among different species, which might overestimate or underestimate pollution levels (Bing et al., 2016). Thus, screening suitable bio-indicators to assess anthropogenic effects on marine environments is imperative and indispensable. Although numerous reports on the responses of seagrasses to different levels of nutrients has been conducted, Chinese case studies are limited, and few studies provide a comprehensive evaluation of eutrophication using seagrasses on a global scale. Thus, a comprehensive overview of potential bio-indicators for eutrophication should be performed to identify an efficient, early warning monitoring tool.

Rongcheng offshore, located in the easternmost of the Jiaodong Peninsula of China, is characterized by significant temporal and spatial variations of nutrients due to intensive mariculture that includes fish cages and longline culture of seaweed and shellfish (Feng et al., 2004; Mahmood et al., 2016). The role of dissolved nutrient cycling in mariculture is particularly crucial, because fish cages release large quantities of excessive feed and fecal material, resulting in additional releases of nutrients to the sea (Bouwman et al., 2013). Moreover, river runoff and municipal and farming wastes of Rongcheng City are additional sources of nutrients into Rongcheng offshore (Mahmood et al., 2016). We aim to identify good, early warning biological indicators for nitrogen concentrations in the Rongcheng coastal area, which have increased significantly during 2006–2014 (Li et al., 2017). The sites selected in the present study were potentially subjected to different levels of nitrogen loading, as suggested by nitrogen contents in pore water and sediments, coastal residential and industrial buildup and mariculture activities, in addition to some large rivers flowing into the bay. Four seagrass species, Zostera marina, Zostera japonica, Zostera caespitosa, and Phyllospadix iwatensis, were observed along Rongcheng offshore in different habitats with different levels of nutrient loading (unpublished data).

In the present study, we compared the physiological responses of four seagrass species under different eutrophic conditions to test two primary hypotheses: (1) nitrogen contents of seagrass tissues are related to environmental eutrophic levels, and (2) physiological responses to different eutrophic levels are different among different seagrass species. The primary objectives of this study were to determine the most efficient seagrass variables as bio-indicators for nitrogen loading and to compile a global benchmark based on our research results and previous studies to establish a metric for reference of eutrophication assessment in marine ecosystems. The results of this study will help establish seagrass-based eutrophic evaluation criteria in coastal ecosystems on a global scale.

Section snippets

Study areas

Samples were collected in three areas on the easternmost coast of Jiaodong Peninsula, Shangdong Province, China: Swan Lake (37°20′-37°22′ N, 122°33′-122°35′ E), Sanggou Bay (37°00′-37°08′ N, 122°26′-122°36′ E), and Rongcheng Bay (37°08′-37°20′ N, 122°32′-122°37′ E). These three areas have different geomorphological features and environmental conditions (Fig. 1, Table 1). Swan Lake (SL) is the largest overwintering habitat for the whooper swan Cygnus cygnus in Asia with an area of 4.8 km2 and is

Spatio-temporal variations of nitrogen in different environmental media

Nitrogen contents in overlying water, pore water, and sediments among different locations showed large variations during sampling periods (Fig. 2). The concentration of DIN in SL ranged from 1.26 to 5.33 μM in the overlying water and from 6.73 to 21.14 μM in the pore water, with mean values of 2.73 and 12.33 μM, respectively. The nitrogen content in the sediments of SL ranged from 0.12 to 0.37% with a mean of 0.26%. In RC, the concentration of DIN ranged from 1.77 to 18.95 μM (mean 7.80 μM) in

Seasonal and spatial variation of nitrogen levels

Highest concentrations of nitrogen occurred in the northwestern sites of SG close to the mouth of the Guhe River and near a densely inhabited district. The mariculture production of Rongcheng increased from 1.01 × 106 t yr−1 in 1997 to 1.67 × 106 t yr−1 in 2016 (http://www.stats-wh.gov.cn/col/col12005/index.html), which could be one of the primary sources of nitrogen increase, in addition to river discharge with municipal sewage and aquacultural waste without proper treatment. The significant

Conclusions

This study determined that the leaf C/N ratio of Z. marina might be a useful bio-indicator based on comparisons of bio-monitoring performance of four widely distributed seagrass species and could be applied in future studies to evaluate nitrogen loads. We also compiled a global benchmark based on the selected indicator to form a baseline for marine eutrophic assessment. Additionally, measures of phenotypic diversity of Z. marina, including leaf width, total chlorophyll (a + b), chlorophyll

Acknowledgments

The authors express our gratitude to all the volunteers who participated in the field and laboratory work. This research is funded by the National Program on Key Basic Research Project (973 Program) (2015CB453302) and the National Natural Science Foundation of China (41676153).

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