Temporal changes of a food web structure driven by different primary producers in a subtropical eutrophic lagoon
Graphical abstract
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.
References (98)
- et al.
δ15N and δ13C in the Mondego estuary food web: seasonal variation in producers and consumers
Mar. Environ. Res.
(2009) - et al.
Modelling the effects of eutrophication, mitigation measures and an extreme flood event on estuarine benthic food webs
Ecol. Model.
(2011) - et al.
Short term effects of hypoxia and bioturbation on solute fluxes, denitrification and buffering capacity in a shallow dystrophic pond
J. Exp. Mar. Biol. Ecol.
(2009) - et al.
Eutrophication in a semi-desert coastal ecosystem promotes increases in N and C isotopic signatures and changes in primary sources
Mar. Environ. Res.
(2019) - et al.
Dynamic changes in seagrass assemblages under eutrophication and implications for recovery
J. Exp. Mar. Biol. Ecol.
(2004) - et al.
Food web structure of two Mediterranean lagoons under varying degree of eutrophication
J. Sea Res.
(2008) - et al.
Quantifying the trophic base for benthic secondary production in the Nakdong River estuary of Korea using stable C and N isotopes
J. Exp. Mar. Biol. Ecol.
(2009) - et al.
Natural and anthropogenic disturbances shape benthic phototrophic and heterotrophic microbial communities in the Po River Delta system
Estuar. Coast. Shelf Sci.
(2019) - et al.
Spatial variations in δ13C and δ15N values of primary consumers in a coastal lagoon
Estuar. Coast. Shelf Sci.
(2012) - et al.
Stable isotopes as tracers can reveal resource allocation in juvenile golden gray mullets (Liza aurata, Risso, 1810)
J. Exp. Mar. Biol. Ecol.
(2018)
Studies on the biology of young grey mullet, Mugil cephalus L. II. Food and feeding
Aquaculture
Spatial shifts in food sources for macrozoobenthos in an estuarine ecosystem: carbon and nitrogen stable isotope analyses
Estuar. Coast. Shelf Sci.
Herbivory of omnivorous fish shapes the food web structure of a Chinese tropical eutrophic lake: evidence from stable isotope and fish gut content analyses
Water
Disentangling heterogeneity and commonalities in nanotidal Mediterranean lagoons through environmental features and macrozoobenthic assemblages
Estuar. Coast. Shelf Sci.
Spatial changes in a macrozoobenthic community along environmental gradients in a shallow brackish lagoon facing Sendai Bay, Japan
Estuar. Coast. Shelf Sci.
Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta
Aquat. Bot.
Growth and feed intake regulation responses to anorexia, adaptation and fasting in Japanese seabass, Lateolabrax japonicas when fishmeal is totally replaced by plant protein
Aquaculture
Analyses of stomach contents and stable isotopes reveal food sources of estuarine detritivorous fish in tropical/subtropical Taiwan
Estuar. Coast. Shelf Sci.
Sediment features, macrozoobenthic assemblages and trophic relationships (δ13C and δ15N analysis) following a dystrophic event with anoxia and sulphide development in the Santa Giusta lagoon (western Sardinia, Italy)
Mar. Poll. Bull.
Effects of Zostera marina on the patterns of spatial distribution of sediments and macrozoobenthos in the boreal lagoon of Furen (Hokkaido, Japan)
Mar. Environ. Res.
The influence of anthropogenic organic matter and nutrient inputs on the food web structure in a coastal lagoon receiving agriculture and shrimp farming effluents
Sc. Tot. Environ.
Linking eutrophication indicators in eelgrass habitats to nitrogen loading and mitigating site characteristics in eastern New Brunswick, Canada
Mar. Environ. Res.
A preliminary investigation of the fish food web in the Gironde estuary, France, using dietary and stable isotope analyses
Estuar. Coast. Shelf Sci.
Macroalgae blooms and δ15N in subtropical coastal lagoons from the Southeastern Gulf of California: discrimination among agricultural, shrimp farm and sewage effluents
Mar. Poll. Bull.
Benthic macrofauna changes in areas of Venice lagoon populated by seagrasses or seaweeds
Mar. Environ. Res.
Sources and transfer of organic matter in food webs of a Mediterranean coastal environment: evidence for spatial variability
Estuar. Coast. Shelf Sci.
Temporal and spatial variations of macrofouling organisms on ecological floating beds in Yundang Lagoon, China
Mar. Poll. Bull.
Food sources of benthic animals on intertidal and subtidal bottoms in inner Ariake Sound, southern Japan, determined by stable isotopes
Estuar. Coast. Shelf Sci.
Roles of epiphytes associated with macroalgae in benthic food web of a eutrophic coastal lagoon
Cont. Shelf Res.
Grazing pressure by amphipods on microalgae in Gamo Lagoon, Japan
Mar. Ecol. Prog. Ser.
Seasonal changes in macrophyte and macrozoobenthos assemblages in three coastal lagoons under varying degrees of eutrophication
ICES J. Mar. Sci.
Modelling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes
Nature
Effect of the invasive bivalve Mytilopsis sallei on the macrofaunal fouling community and the environment of Yundang Lagoon, Xiamen, China
Hydrobiologia
Herbivore community determines the magnitude and mechanism of nutrient effects on subtropical and tropical seagrasses
J. Ecol.
Mechanisms regulating amphipod population density within macroalgal communities with low predator impact
Sci. Mar.
Temporal variation in the trophic levels of secondary consumers in a Mediterranean coastal lagoon (Cabras lagoon, Italy)
Estuar. Coasts
Comparison of the areal amount of chlorophyll a of planktonic and attached microalgae in a shallow coastal lagoon
Hydrobiologia
Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers
Ecology
Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation
Mar. Ecol. Prog. Ser.
The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: considerations based on multiple stable isotope analysis
Mar. Ecol. Prog. Ser.
Necton resources state of Yundang lake in xiamen
J. Fujian Fisher.
Microphytobenthic biomass, diversity and exopolymeric substances in a shallow dystrophic coastal lagoon
J. Mar. Microbiol.
Piscivory and trophic position of Anguilla anguilla in two lakes: importance of macrozoobenthos density
J. Fish Biol.
Distribution and production of Microdeutopus gryllotalpa (Amphipoda: aoridae) in a shallow coastal lagoon in the Bay of Cadiz, Spain
J. Crust. Biol.
The meagre future of benthic fauna in a coastal sea—benthic responses to recovery from eutrophication in a changing climate
Glob. Ch. Biol.
The guild approach to categorizing estuarine fish assemblages: a global review
Fish Fish
Restructuring of benthic communities in eutrophic estuaries: lower abundance of prey leads to trophic shifts from omnivory to grazing
Mar. Ecol. Prog. Ser.
13C/12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows
Mar. Biol.
A comparative study on the feeding habits of Oreochromis niloticus (Linnaeus) in Nyanza Gulf Lake Victoria and sewage fish ponds
Cited by (18)
Growth characteristics and population dynamics of Macrophthalmus japonicus with decreasing microphytobenthos biomass in muddy estuarine tidal flat
2024, Regional Studies in Marine ScienceDecade changes of the food web structure in tropical seagrass meadow: Implication of eutrophication effects
2021, Marine Pollution BulletinCitation Excerpt :These results seem to be reasonable because a large amount of nitrogen loading into Xincun Bay decreased the biomass of seagrass but led to the clear proliferation of macroalgae, epiphytes, and POM (see Section 4.1). These fast-growing algae are not only more likely to be consumed by consumers because of their higher palatability and nutritional value than seagrass (Burkholder et al., 2012; Zheng et al., 2020), but they might also alter the consumers' ability to find, acquire, and consume its food source through high biomass (Jankowska et al., 2019). Therefore, the high biomass of fast-growing algae for the diet of consumers might lead to their homogeneous or limited feeding strategies, which has been also proved by the consistently lower δ13C values and higher δ15N values for algae carbon sources and consumers.
Fecal pollution mediates the dominance of stochastic assembly of antibiotic resistome in an urban lagoon (Yundang lagoon), China
2021, Journal of Hazardous MaterialsCitation Excerpt :Widespread antibiotic use, organic fertilization with manure, and discharge of antibiotic residues from hospitals, livestock farms, pharmaceutical industries, and wastewater treatment plants (WWTPs) all contribute to the accumulation of ARGs in urban landscape water (Proia et al., 2018; Zhu et al., 2013). More importantly, due to horizontal gene transfer (HGT), ARGs could be exchanged and transferred among environmental microbes and pathogens through mobile genetic elements (MGEs) such as integrons, plasmids, and transposons (W.L. Zheng et al., 2020; X. Zheng et al., 2020). Therefore, recently the public calls for a comprehensive understanding of the pollution sources, and variation, of the antibiotic resistome in urban landscape water to manage and reduce the dissemination and accumulation of ARGs (Hou et al., 2020; Lorenzo et al., 2018).
Trophic importance of the seagrass Halophila ovalis in the food web of a Hepu seagrass bed and adjacent waters, Beihai, China
2021, Ecological IndicatorsCitation Excerpt :These benthic herbivores or detritus feeders fed directly on H. ovalis or its detritus, which resulted from the good palatability of seagrass Halophila due to high nutritional values compared to other slow-growing seagrasses, e.g., Amphibolis, Posidonia, and Cymodocea (Bendell, 2006; Burkholder et al., 2012). It has been widely accepted that macrozoobenthos in coastal waters shift their dietary items, depending largely on the shifts in the primary carbon sources (Doi et al., 2005; Kanaya et al., 2007; Burkholder et al., 2012; Zheng et al., 2020). In Singapore’s seagrass meadows, gastropod Euplica scripta shifted the diet from seagrass Halophila ovalis in Chek Jawa Wetlands to seagrass Euplica scripta in Tanjung Rimau, responding to a shift in dominant seagrass species (Burkholder et al., 2012).