Temporal changes of a food web structure driven by different primary producers in a subtropical eutrophic lagoon

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Highlights

  • δ13C and δ15N values in food sources and consumers were studied in a hypertrophic lagoon.

  • Temporal changes in primary energy sources and isotopic signals of primary consumers were found.

  • Ulva (March) and phytoplankton (September) blooms were utilized by the entire food web.

  • Omnivores acted as a conduit for different food sources up to the highest trophic levels.

  • Omnivores play a central role in the lagoon's functioning under persistent eutrophic conditions.

Abstract

Coastal lagoons are often characterized by eutrophic conditions which are known to impair the structure and functioning of both pelagic and benthic compartments. However, the manner in which eutrophication triggers a series of cascade effects in the whole food web in coastal lagoons has received little attention. Using stable isotope (SI) analyses, we investigated the food web structure in the hypertrophic lagoon of Yundang (Xiamen, China) in two periods of the year characterized by the recurrent alternation of Ulva lactuca and phytoplankton blooms in the cool (March) and warm (September) seasons, respectively. Large temporal fluctuations in the dominance of primary producers (i.e. macroalgae vs. phytoplankton) and, thus, in the available food items, were reflected in major changes in the diet and SI signals of several primary consumers, such as the amphipod Grandidierella japonica, the polychaetes Neanthes japonica and Capitella capitata, and omnivorous fishes (i.e. Mugil cephalus, Oreochromis niloticus, and Sardinella zunasi), while these changes were limited in top carnivorous fishes, such as Lateolabrax japonicus. Furthermore, reduced macrozoobenthic abundance available for omnivores in September was found to force omnivores to switch their feeding habits to those of herbivores. The present study provides evidence that the periodical alternation of macroalgal and phytoplankton blooms throughout the year strongly affect the relations among different trophic levels leading to a cascading effect across the whole food web and to major changes in the lagoon's food web structure. Importantly, our study shows that the lagoon's food web structure under persistent eutrophic conditions can still cope with seasonal changes in primary energy source type from macroalgae to microalgae due to the ability of omnivorous fishes to conduit different food sources up to the highest trophic levels. Thus, this study suggests that in such a highly variable eutrophic system, omnivores play a central role in the lagoon's functioning, and help to sustain the biological resources and the ecosystem services provided by the lagoon.

Introduction

Eutrophication in coastal marine and transitional (e.g. estuaries and lagoons) waters is a major environmental problem worldwide (Rabalais et al., 2009; McIver et al., 2019; Padedda et al., 2019). Anthropogenic nitrogen and phosphorous that are massively discharged into these aquatic environments cause recurrent blooms of ephemeral macroalgae and phytoplankton, and the loss of important habitats, such as seagrass beds (Hauxwell et al., 2003; Zheng et al., 2015; Magni et al., 2017; Campbell et al., 2018). These events can lead to anoxic crises caused by frequent biomass decomposition and the accumulation of decaying organic matter in sediments (Magni et al., 2008; Baeta et al., 2011), which creates critical conditions for autochthonous organisms with reduced lifecycles, young individuals, and a prevalence of epifaunal species over infauna (Sfriso et al., 2001; Gravina et al., 2020).

Significant changes in species composition and the abundance of primary consumers, especially macrozoobenthos (Bachelet et al., 2000; Hummel et al., 2017), translate into changes in the food web structure resulting from shifts in the fish diet (Fox et al., 2009; Como et al., 2012, 2018a; Schmidt et al., 2017; Sporta Caputi et al., 2020). It has been proven that the generation and persistence of anoxic zones can significantly reduce the system's biological richness and diversity (Norkko and Bonsdorff, 1996; Worm and Lotze, 2006; Fox et al., 2009; Ehrnsten et al., 2020), which necessitates that omnivores shift to a more herbaceous diet (Fox et al., 2009; Gao et al., 2017) and carnivorous fishes feed on low-trophic-level organisms (Dörner et al., 2009; Sabo et al., 2010; Sporta Caputi et al., 2020).

Limited research in coastal lagoons indicates that eutrophication influences the stable isotope (SI) composition of primary producers and consumers (Cardoso et al., 2004; Vizzini and Mazzola, 2003; Becherucci et al., 2019), and may result in a simplification of the food web structure (Carlier et al., 2008; Fox et al., 2009; Vizzini et al., 2016). Yet, the mechanisms under which eutrophication per se causes changes in the food web are not completely understood in coastal and transitional systems (Carlier et al., 2008; Fox et al., 2009; Vizzini et al., 2016). Some studies focused on the spatial shift in the community structure and the dietary shift of macrozoobenthos to indirectly clarify the food web dynamics under eutrophication (Kanaya et al., 2007, 2008). Other studies compared the food web structures of different systems undergoing varying degrees of eutrophication (Fox et al., 2009; Schein et al., 2013; Magni et al., 2013; Vizzini et al., 2016; Sporta Caputi et al., 2020). However, the influence of eutrophication on the food web dynamics also depends on external factors, such as precipitation and the inflow of 15N-rich nutrients accumulated in the catchment (Kanaya et al., 2020) or site-specific environmental features which may vary largely among systems. For example, in Stagnone di Marsala lagoon, Vizzini and Mazzola (2006) found that the hydrodynamic regime can control the origin and distribution of organic matter, as well as its transfer in the benthic food web. Yet, there is still little evidence of how seasonal changes in phytoplankton and macroalgal biomass in shallow eutrophic coastal lagoons, known to cause large fluctuations of macrozoobenthos (Bachelet et al., 2000; Cardoso et al., 2004; Kanaya and Kikuchi, 2008), would be reflected in temporal changes in the food web structure and trigger a series of cascade effects (Pascal et al., 2013; Vizzini et al., 2016).

In the present study, we investigated the temporal variation in the food web structure in the Yundang Lagoon a small, hypertrophic lagoon located on Xiamen Island (southeast China), characterized by recurrent macroalgal and phytoplankton blooms in the cool and warm season, respectively (Zheng et al., 2008, 2014; Liu, 2011). We compared the temporal differences in the carbon (C) and nitrogen (N) isotopic signatures of organic matter sources, primary producers, and consumers, analyzed the organic carbon sources and their transfer through the food web, as well as the trophic interaction among organisms and its temporal fluctuation, and reconstructed the food web in the lagoon. We hypothesized that the profound biological changes related to the periodical alternation of macroalgal and phytoplankton blooms throughout the year will affect the trophic relations among different trophic levels in the lagoon and will eventually cause a cascade effect to the food web structure.

Section snippets

Study area and sampling design

The present study was conducted in the Yundang Lagoon, a small subtropical lagoon located in densely populated Xiamen City, China. The lagoon has a total area of 1.5 km2 with an average depth of approximately 2.5 m. An artificially regulated sluice separates the lagoon from the western sea of the Xiamen Island, allowing a daily water exchange (Fig. 1). The water residence time in the lagoon is approximately 3 days (Zheng et al., 2019). Salinity remains relatively stable throughout the year at

δ13C and δ15N signatures

Items that were sufficiently abundant for the analyses on both sampling dates (March and September) included three organic matter sources (POM, BM, and SOM), four benthic macroinvertebrate species (Grandidierella japonica, Neanthes japonica, Capitella capitata and M. sallei), zooplankton, the shrimp Metapenaeus joyneri and seven fish species (Mugil cephalus, Oreochromis niloticus, Sardinella zunasi, Leiognathus sp., Acanthopagrus latus, Acentrogobius caninus, and Lateolabrax japonicus) (Table 2

Composition and temporal changes of diet in macrozoobenthos and zooplankton

The results showed that the amphipod G. japonica and the polychaetes N. japonica and C. capitata followed a significant temporal shift in their diet between March and September, which corresponded to the temporal change in the availability of different food items (He, 2002; Liu, 2011; Zheng et al., 2013a). It has been suggested that food items obtained by the macrozoobenthos in coastal waters and lagoons depend largely on shifts in primary carbon sources (Doi et al., 2005; Kanaya et al., 2007,

Funding

This work was funded by the National Key R&D Program of China (Grant No. 2018YFC1406302, 2018YFC1406301, 2016YFC0502904) and supported by the National Natural Science Foundation of China (Grant No. 41506123).

CRediT authorship contribution statement

Xinqing Zheng: Conceptualization, Methodology, Investigation, Data curation, Formal analysis, Writing - original draft, Writing - review & editing. Serena Como: Formal analysis, Writing - original draft, Writing - review & editing. Lingfeng Huang: Conceptualization, Funding acquisition, Writing - review & editing, Supervision. Paolo Magni: Conceptualization, Writing - original draft, Writing - review & editing, Supervision.

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 acknowledge the Short Term Mobility Programme (STM Italy-China 2015–2016) of the National Research Council of Italy granted to LH and PM. We thank three anonymous Reviewers for their constructive criticisms that contributed to improve the original manuscript.

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