# Importance of the microphytobenthos in the foodweb of tropical mudflats

Alexandre Carpentier, Anne Lizé, Hien Nguyen Thanh, Pierrick Bocher, Christel Lefrançois, Antoine Gardel, Pierre-Yves Pascal, Christine Dupuy

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## To cite this version:

Alexandre Carpentier, Anne Lizé, Hien Nguyen Thanh, Pierrick Bocher, Christel Lefrançois, et al. Importance of the microphytobenthos in the foodweb of tropical mudflats. Estuarine, Coastal and Shelf Science, 2025, 319, pp.109257. 10.1016/j.ecss.2025.109257. hal-05056908

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Submitted on 29 Jul 2025

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# Importance of the microphytobenthos in the foodweb of tropical mudflats

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Alexandre Carpentier<sup>a,1,*</sup>, Anne Lizé<sup>b,c,d,1</sup>, Hien Nguyen Thanh<sup>e,f</sup>, Pierrick Bocher<sup>f,g</sup>, Christel Lefrançois<sup>f</sup>, Antoine Gardel<sup>g</sup>, Pierre-Yves Pascal<sup>h</sup>, Christine Dupuy<sup>f</sup>

## ARTICLE INFO

### Keywords:

Meiofauna

Fish

Shorebirds

Benthic food web

Isotopes

Mixing model

Niche overlap

French Guiana

## ABSTRACT

Mudflats are peculiar dynamic ecosystems, at the interface of terrestrial and aquatic ecosystems, known for their large carbon storage ability. Mudflats also provide food source and constitute important habitats for photosynthetic organisms and consumer communities. Tropical mudflats are highly unstable and only temporarily accessible to either aquatic or aerial consumers because of tides, which raises the question of the trophic functioning of these habitats. Their importance in terms of trophic resources for species that temporarily feed there as well as the carbon origin of mudflat foodweb deserve to be explored. This was assessed, over a year in a tropical mudflat (French Guiana) at two sites (Sinnamary and Awala-Yalimapo), from primary producers to predators, using stable isotope ratios (δ¹³C and δ¹⁵N) as a proxy of their diet. The results showed that trophic interactions were similar in each site and only a few influences of the seasons were detected for the meiofauna (*Halomonhystera* sp.), and fish (*Gobionellus oceanicus* only in Sinnamary). The microphytobenthos constituted the dominant primary source incorporated by the meiofauna, which in turn was an important one for the fish. The three shorebird species depended mainly on the microphytobenthos, green algae and Tanaidacea and secondarily on the meiofauna. The two resident fishes relied on the same sources as the birds but incorporating higher proportions of the meiofauna taxa (Copepoda, Nematoda, and Ostracoda). The analyses of species niche overlaps between the three shorebirds and the two resident fish demonstrated that they might compete for resources. The results are discussed in relation to the central place of the MPB as a direct or indirect source of carbon for the vast majority of organisms present on these tropical mudflats, whether transient or resident species.

## 1. Introduction

Among coastal ecosystems, intertidal flats are key systems, known as one of the most productive on earth (Walker and Mossa, 1982), and providing many ecological functions such as nursery for fish and feeding area for birds (e.g. Morrisson et al., 2002; Granadeiro et al., 2007). However, ecological functioning of intertidal mudflats remains partially documented in tropical areas, and especially in French Guiana. The coast located between the Amazon and Orinoco Rivers (1500 km long) is considered the muddiest in the world because of the large flow of suspended sediments discharged from the Amazon along the coast (754 M

t/year ± 9%; Martinez et al., 2009). These tropical mudflats, which differ from temperate ones, and considered unique in the world, are characterised by their high instability (Anthony et al., 2010). Tropical mudflat sediments are more fluid than in temperate systems, forming series of huge mudflats through the action of waves, tides, wind and coastal currents. These "migrating mudflats" move over more than a kilometre per year and stretch over an area of at least 10–60 km long and 20–30 km wide (126,000 km²) on the 330 km of the French Guiana coast (Anthony et al., 2010). These mudflats can extend down to 9 m depth, with 5 % of its surface located in the intertidal area, imposing geomorphological dynamics leading to rapid shoreline changes and fast

<footnote><sup>a</sup> Université de Rennes, Laboratoire de Biologie des Organismes et des Écosystèmes Aquatiques (BOREA), MNHN, SU, CNRS, IRD, UA. 35000 Rennes, France</footnote>

<footnote><sup>b</sup> Laboratoire de Biologie des Organismes et des Écosystèmes Aquatiques, Muséum National d'Histoire Naturelle (MNHN), SU, CNRS, IRD, UA. F-75005 Paris, France</footnote>

<footnote><sup>c</sup> Station Marine de Dinard du Muséum National d'Histoire Naturelle, 35800, Dinard, France</footnote>

<footnote><sup>d</sup> School of Biosciences, University of Liverpool, L697ZB Liverpool, United Kingdom</footnote>

<footnote><sup>e</sup> University of Science and Technology of Hanoi, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Str., Hanoi, 100000, Vietnam</footnote>

<footnote><sup>f</sup> Littoral Environnement et Sociétés (LIENSs), CNRS-La Rochelle Université, 17000, La Rochelle, France</footnote>

<footnote><sup>g</sup> Centre National de la Recherche Scientifique-CNRS, UG, IFREMER (LEEISA URS 3456), Centre de Recherche de Montabo, 97334, Cayenne Guyane française, France</footnote>

<footnote><sup>h</sup> Institut de Systématique, Évolution, Biodiversité (ISYEB), Université des Antilles, MNHN, SU, CNRS, EPHE, F-97157, Pointe-à-Pitre, Guadeloupe</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: alexandre.carpentier@univ-rennes.fr (A. Carpentier).</footnote>

<footnote n="1">¹ These two authors contributed equally.</footnote>
alternations of facies types (Anthony et al., 2010).

In temperate coastal areas, the intertidal mudflat productivity has been shown to play a central role. Indeed, mudflats enrich the adjacent terrestrial and marine zones through physical and biological mechanisms, such as waves, estuarine currents and tides (Allison et al., 2000), and the exports by mobile consumers such as birds and fish (Bocher et al., 2014; Carpentier et al., 2014). In subtropical and tropical estuarine areas, research and conservation efforts have mainly focused on mangroves (Faunce and Serafy, 2006; Nagelkerken et al., 2008; Marley et al., 2020), as their structural complexity is expected to shelter more biodiversity and convey greater ecological functions, compared to unvegetated open flats (Tse et al., 2008; Marley et al., 2020). Despite the interest devoted to mangroves, the role of adjacent habitats such as intertidal mudflats has been ignored until recently (Campos et al., 2015; Zulkifli et al., 2016; Beninger et al., 2018; Lee et al., 2019), even if they often represent larger areas and constitute the necessary substrate for mangrove growth after sediment consolidation. Moreover, intertidal mudflats are used as shelters for aquatic organisms living in mangroves, which have to leave these temporary habitats at low tides (Igulu et al., 2014). Compared to temperate areas, only few data on biodiversity, benthic community structure, and food web functioning of tropical mudflats are available, and understanding the dynamics of biological communities associated with these highly unstable environments is still in its infancy. The food web in temperate intertidal mudflats and by extension the trophic role of this habitat for transient species (notably fish and birds) is particularly well studied in Europe (Leguierrier et al., 2003; Pascal et al., 2009; Ubertini et al., 2012). According to these studies, 35-70 % of benthic meio-macrofaunal diet is composed by microphytobenthos (hereafter called MPB), whereas grazing on bacteria would be limited (van Oevelen et al., 2006; Pascal et al., 2009). By comparison, the few studies on French Guiana intertidal mudflats highlighted a thicker biofilm (of 200 µm), coupled with a high abundance and biomass of benthic meiofauna and macrofauna, particularly deposit-feeders (Dupuy et al., 2015; Nguyen et al., 2017). Additionally, the meiofauna of French Guiana intertidal mudflats has been shown to be an important prey for predators such as a crab (Portunidae), a shrimp (Penaeidae) and a fish (Gobiidae), during their early life or in the absence of other large food items (Pascal et al., 2019). In these habitats, a very high abundance of migrating and wintering shorebirds, as well as local waterbirds such as egrets, and fish, including commercially exploited ones, were also found (Guéguen, 2000). As in temperate mudflat systems, MPB is expected to represent a large proportion of the diet of the meio- and macrofauna in tropical mudflats.

MPB is mainly limited by light and temperature under temperate climate (Denis et al., 2012) and suffers damages in extreme light conditions. In response, algal cells can either migrate or physiologically regulate their photosynthesis to avoid photoinhibition damages (Cartaxana et al., 2011). It is likely that temperature and light conditions are much more constraining in tropical climates and strongly influence the composition and responses of MPB biofilm components. MPB-associated meiofauna (40 µm–1 mm length) constitutes an inconspicuous component of the benthic fauna and may provide generally the most abundant and diverse taxa in marine sediments (Purwoko and Wolff, 2008). Meiofauna consumes MPB (Montagna et al., 1995) and can be important prey for macrofauna such as fish and infauna (Gee, 1989; Pascal et al., 2019). However, relatively little is known about the role of meiofauna in food web of tropical systems (Alongi, 1989). Macrofauna (length >1 mm) is usually a major part of the total biomass of temperate mudflats and has a central role in the functioning of these ecosystems (Gray and Elliott, 2009; Nguyen et al., 2017). Conversely, the macrofauna compartment is poorly represented in the Atlantic Amazonian coast (Purwoko and Wolff, 2008; Nguyen et al., 2017) and its importance in food web needs to be explored. Polychaetes appear to be the most diverse group with densities rarely exceeding $1 ind.m^{-2}$ whereas mudshrimps present densities reaching $24,000 ind.m^{-2}$ (Purwoko and Wolff, 2008; Nguyen et al., 2017).

Temperate intertidal mudflats are also important for the lifecycle of numerous fish species (e.g. Laffaille et al., 1998; Morrison et al., 2002; Almeida, 2003; Carpentier et al., 2014). For instance, intertidal mudflats provide nurseries for juveniles, and feeding areas for adults, preying on macrofauna or more rarely, grazing on biofilm. In French Guiana, preliminary investigations on common fish species living in or on mudflats, like the four-eyed fish (*Anableps microlepis*) and the highfin goby (*Gobionellus oceanicus*), showed that their stomach were often filled with mud, suggesting their grazing capacities. Finally, previous research demonstrated that numerous shorebird species depend on intertidal mudflat habitats during the non-breeding period (van de Kam et al., 2004; Laguna et al., 2012; Hall et al., 2021). They commonly feed on macrofaunal benthic preys (Colwell, 2010), while the small-size shorebirds may also ingest biofilm (Kuwa et al., 2012). Despite the recent decline of some species, as observed for the semipalmated sandpiper (*Calidris pusilla*) (Morrison et al., 2012), migrating and wintering birds remain very abundant along the French Guiana coast (Laguna et al., 2012).

The question of the origin of carbon in transitional habitats between sea and land is crucial to better understand their ecological functioning. In French Guiana, the importance of the mangroves and the high estuarine flows are expected to enrich the adjacent mudflat foodweb, through terrestrial and coastal inputs. However, several studies on tropical mudflats showed some independence of carbon sources between these different compartments (e.g. Burford et al., 2008; Claudino et al., 2015), and their respective foodwebs (see the review of Lee, 1995; Lee et al., 2019; Zulkifli et al., 2016), despite a homogeneous distribution of fish for example (Pessanha et al., 2021). In this context, we hypothesized that the origin of carbon in French Guiana mudflat foodweb mostly derives from the MPB, with a lesser influence of terrestrial (mangrove leaves) and coastal (green algae) inputs. In this study, we assessed the carbon origin in a tropical mudflat foodweb by focusing on two mudflats (estuarine and coastal) of French Guiana over a year (dry and wet seasons), using stable isotopes as a proxy of species diet. We further assessed the dependence of primary consumers and predators to potential primary sources of mudflats (MPB, mangrove leaves and green algae). Finally, we discussed the role of these mudflats and their potential ecological functions through niche partitioning for fish and shorebirds.

## 2. Material and methods

### 2.1. *Sampling sites*

The study was carried out on two out of six moving mudflats along the coast of French Guiana at the time of the study: Awala-Yalimapo (05°44′N, 53°55′W) and Sinnamary (05°27′N, 53°00′W) (Fig. 1). Both mudflats constitute a meso-tidal system with semidiurnal tidal range between 0.8 m (neap tide) and 2.9 m (spring tide). These two mudflats were selected because of their reliable location and their proximity to the main rivers, Sinnamary and Maroni. According to Plaziat and Augustinus (2004), the evolution of the mudflat in Awala-Yalimapo (hereafter names Awala) has been characterized by a gradual overall west-ward extension of the mud cape along the coast, without intensive erosion or accretion. In contrast, the mudflat in Sinnamary has undergone several consecutive accretion and erosion phases (Fromard et al., 2004). During the sampling period, the Sinnamary mudflat was migrating westward with most of its intertidal part having crossed the Sinnamary River sector (Gensac et al., 2015). Therefore, the Sinnamary mudflat is more exposed to the river flow (estuarine mudflat), compared to the Awala one, qualified as a seafront mudflat. The climate is tropical and humid, with two main periods: a wet season from January to July, and a dry season from August to December. A total of four different contexts (2 seasons x 2 sites) were therefore considered for the analysis of the food webs: the wet and dry seasons in Awala and Sinnamary.
<figure><img src="image_5.png" /><figcaption>**Fig. 1.** Locations in French Guyana of sites (1: Awala, 2: Sinnamary) sampled over the wet and dry seasons in 2014.</figcaption></figure>

## 2.2. Sampling design

Except for shorebirds sampled in Awala in 2011, all samples were collected in 2014 in the mudflats intertidal area during the wet season (May–June) and late in the dry season (November–December) in both Awala and Sinnamary (Fig. 1). Sampling was focused on the most abundant taxa of the mudflat with a potentially greater role in the food web (see supplementary material). Biofilm of MPB was collected at the low tide in all sites and seasons, except in Sinnamary during the wet season. The upper-layer (approx. 500 µm) of the sediment was collected at the low tide, and immediately brought back to the laboratory. After sieving through a 500 µm mesh to remove macrofauna, the sediment was homogenized and placed in a layer of 2 cm in trays maintained under natural light conditions. On the surface of the sediment layer, 2 nylon nets (200 µm and 60 µm) were placed to allow the migration of the majority of MPB and its separation from the sediment. The 60 µm mesh was scraped to recover the MPB, and then preserved in 70 % ethanol. In AWS, filamentous green algae (hereafter named green algae) were collected by hand at the surface of the sediment. To explore the influence of the terrestrial sources and by extension the freshwater ones, mangrove tree leaves from three species (*Avicennia germinans*, *Laguncularia racemosa*, and *Rhizophora mangle*) were collected during the wet season in the mangrove along the Sinnamary River estuary.

The meiofauna was sampled with a core (Ø: 15 cm) to a depth of 2 cm. At the laboratory, the sediment was sieved through a 50 µm mesh and the samples were preserved in 70 % ethanol. Three phyla of meiofauna were selected: Nematoda, Ostracoda and Copepoda. For Nematoda, specimens were randomly handpicked for observation and identification (Seinhorst, 1959), and pooled per taxa (n ≥ 100) to obtain enough material for the isotopic analysis. The same procedure was followed for Copepoda (n ≥ 100) and Ostracoda (n ≥ 100). All samples were then washed three time with clear tap water. The macrofauna was sampled with a core (Ø: 15 cm) to a depth of 20 cm. At the laboratory, the sediment was sieved through a 500 µm mesh and the samples were preserved in 70 % ethanol. Individuals from the Tanaidacea family and Polychaeta class were washed three times with clear tap water and handpicked for species identification. Two species of fish were considered as resident for this study, the highfin goby (*Gobionellus oceanicus*) and the four-eyed fish (*Anableps microlepis*), although the latter reaches shallow water at completely low tide. Individuals of *G. oceanicus*, were collected by hand in their burrow at the low tide while individuals of *A. microlepis* were caught with a hand net or a beach-seine at rising tide. Juveniles from other fish species were also randomly caught with a hand net and a pushnet during high tide, before being identified and preserved in 70 % ethanol before dissection for muscle collection. Large fish

individuals were caught with gill nets of various mesh sizes, a beach-seine or a fishing rod, before a biopsy was carried out for further analysis on muscle. Shorebirds were caught with mist-nets on high tide roosts bordering the rice fields of Mana close to Awala, during non-moonlit nights from October to December 2011 (dry season). Less than 300 µL of whole blood was sampled from the wing vein and kept in 70 % ethanol from randomly selected individuals among the three most abundant small-size shorebirds (the least sandpiper (*Calidris minutilla*), the semipalmated plover (*Charadrius semipalmatus*), and the semi-palmated sandpiper (*Calidris pusilla*)), after which the birds were immediately released.

## 2.3. Isotope analysis

All samples were preserved in 70 % ethanol due to logistic difficulties to export them from French Guiana to metropolitan France for laboratory isotopic analyses. Muscle tissues were extracted when possible (i.e. for large individuals, >1 cm), whereas entire animals were used when they were too small. The isotopic analysis of muscle and entire animals provides a trophic proxy over a mid to long-term period of the diet (about one month). For shorebirds, the entire blood sample was used (plasma + cells) as it integrates the diet over at least 20 days (Ogden et al., 2004).

Back at the laboratory, vegetal and animal samples were freeze-dried (i.e. Fischer Scientific® – Alpha 1–2 LD plus) during 24h and grounded with a ball mill (i.e. Retsch® MM 200) into a fine and homogeneous powder. The nitrogen (N) and carbon (C) isotopic ratios of samples (δ¹³C and δ¹⁵N respectively), expressed in ‰, were determined using EA-IRMS (Isoprime, Micromass, UK), with δX = [(RReference/RSample) − 1] × 1000, where X = δ¹³C or δ¹⁵N and R is the ratio ¹³C:¹²C or ¹⁵N:¹⁴N in the sample and in the reference material (Vienna Pee Dee Belemnite).

## 2.4. Data analysis

δ¹³C and δ¹⁵N values were used to estimate the contributions of several sources to the isotopic composition of consumers including meiofauna, macrofauna and vertebrates components using Bayesian stable-isotope mixing models with the package 'MixSIAR' 3.1.12 (Stock and Semmens, 2016) in R 4.2.1 (R Core Team, 2022). These models allow the inclusion of isotopic signatures from food web components, elemental concentrations and trophic enrichment factors (TEF) together with the uncertainty of these values within the model. Since TEF were not known for all predator-prey relationships, we used theoretical values from literature. TEF were set to 1 ± 0.1 ‰ and 2.4 ± 0.1 ‰ for carbon and nitrogen respectively (Zanden and Rasmussen, 2001) between
primary producers and first consumers and to 1 ± 0.1 ‰, and 3.4 ± 0.1 ‰ between first consumers and their potential predators (trophic level >1) (De Niro and Epstein, 1978). The tolerance of 0.1 ‰ was chosen according to (Phillips and Gregg, 2003) recommendations. Models were set up with the following characteristics: three chains with 300,000 iterations and a burn-in of 200,000 with a thin of 100 to allow for adequate model convergence, which was checked using Gelman-Rubin and Geweke diagnostics.

The mangrove tree leaves were only sampled in the Sinnamary River estuary during the wet season and were used as primary sources in all

models. In Sinnamary, MPB isotopic composition was not available during the wet season (see supplementary material), so data from MPB during the dry season were used in the mixing model. In the mixing models run for meiofauna in the four contexts, green algae, mangrove leaves and MPB were included as food sources for Copepoda, Ostracoda, *Halomonhystera* sp., and *Metachromadora* sp. The mixing model for birds (the least sandpiper, semipalmated plover and semipalmated sandpiper) was run solely on the Awala dry season context, while the one for resident fish (*A. microlepis* and *G. oceanicus*) was run on all four contexts. These two mixing models were set with green algae, MPB, Copepoda,

<figure><img src="image_6.png" /><figcaption>**Fig. 2.** Biplot of the means and standard deviations of δ¹³C (x-axis) and δ¹⁵N values (y-axis) of sources and consumers (meiofauna, macrofauna, birds, and fish) sampled in Awala and Sinnamary during the dry and wet seasons. Within the fish, *Colomesus psittacus*, *Engraulidae*, *Harengula jaguana*, *Mugilidae*, *Pterengraulis atherinoides* were juveniles, while all others were adult individuals.</figcaption></figure>
Nematoda, Ostracoda and Tanaidacea as sources. In these models, mangrove leaves and the nematod *Sphaerolaimus* sp. were not considered as sources because of their high trophic position in the food web, leaves having particularly high δ¹⁵N values and *Sphaerolaimus* sp. is a carnivorous (Yeates et al., 1993).

Isotopic niche widths (δ¹³C and δ¹⁵N) of each shorebird and resident fish species and overlaps were analysed using the R package, SIBER 2.1.7 (Jackson et al., 2011; Rossman et al., 2016). Posterior ellipsoids were calculated after 2 × 10⁴ iterations, a burn-in of 1 × 10³, over two chains. Bayesian standard ellipse areas (SEA_B) were calculated, and the 95 % predicted Bayesian confidence interval (SEA_B CI95) were used to estimate the proportion of overlapping between species. Details of all the R script, raw data and model results of this study are available as Supplementary Material.

# 3. Results

## 3.1. Mudflat food web general pattern

A total of 38 taxa was sampled during the two seasons at both sites (see supplementary material), including three different primary sources (MPB, green algae and mangrove tree leaves (A. germinans, L. racemosa, and R. mangle)). Although all these sources were not sampled for all seasons and sites, their isotopic signatures were considered stable over seasons and sites (like MPB sampled in three contexts over four).

The benthic meiofauna was composed of undetermined Copepoda, undetermined Ostracoda and four genera of Nematoda: *Halomonhystera* sp., *Pseudochromadora* sp., *Metachromadora* sp., *Sphaerolaimus* sp. The benthic macrofauna comprised one species belonging to the Tanaidacea and three genera of Polychaeta: *Nephys* sp., *Alitta* sp. and *Sigambra* sp. For fish, two resident species were sampled, the four-eyed fish (A. microlepis) and the highfin goby (G. oceanicus) and seventeen transient ones of which two families could not be determined to the species level (*Apionichthys dumerili*, *Catharops spixii*, *Centropomus ensiferus*, *Centropomus parallelus*, *Centropomus undecimalis*, *Colomesus psittacus* as juveniles, *Cynoscion acoupa*, Engraulidae as juveniles, *Harengula jaguana* as juveniles, *Megalops atlanticus*, Mugilidae as juveniles, *Pterengraulis atherinoides* as juveniles, *Sciades couma*, *Sciades proops*, *Sphoeroides testudineus*, *Stellifer rastrifer*, *Symphurus plagusia*). Samples of three species of foraging small-size shorebirds, the least sandpiper (C. minutilla), the semipalmated sandpiper (C. pusilla), and the semipalmated plover (C. semipalmatus) were considered.

Within primary resources, MPB had the highest δ¹³C values, while the lowest δ¹³C values were observed for mangrove leaves, fitting with a terrestrial-freshwater influence (Fig. 2). As the isotopic ratios were very similar between mangrove leave species, they were grouped as “mangroves leaves” in the mixing models. Finally, green algae had similar δ¹³C values to MPB but lower δ¹⁵N values (Fig. 2).

The isotopic composition of most studied taxa relies on MPB (totally or partially, Fig. 2) and secondarily on green algae and according to contexts, on mangrove leaves (Fig. 2). δ¹⁵N values were higher in green algae (4.49 ± 0.50 ‰) than in MPB (3.24 ‰ (only one replicate)) (Fig. 2 - Awala wet season). Finally, a few taxa seem totally excluded from MPB influence (low δ¹³C values) such as some fish like snooks (3 species of *Centropomus* sp.), longtail sole (*Apionichthys dumerili*) and the wingfin anchovy (*Pterengraulis atherinoides*) (Fig. 2 - Awala wet season), and two species of puffers (*Colomesus psittacus* and *Sphoeroides testudineus*) (Fig. 2 - Sinnamary dry season).

The position in the food web of the five taxa of meiofauna (Copepoda, *Halomonhystera* sp., *Metachromadora* sp., Ostracoda, and *Pseudochromadora* sp., excluding *Sphaerolaimus* known as carnivorous) showed that their potential primary sources of carbon could be green algae, MPB, and mangrove leaves (Fig. 2). These sources were thus used in the mixing models run for each of the five meiofauna taxa as consumers in each of the four contexts. The position in the food web of the three bird species (the least sandpiper, the semipalmated plover and the

semipalmated sandpiper) showed that their potential sources of food could be green algae, MPB, Copepoda, Ostracoda, the three genera of Nematoda (excluding *Sphaerolaimus* sp.) and Tanaidacea (Fig. 2 - Awala dry season). These sources were thus used in the mixing models run for each bird species as consumers in Awala during the dry season, as birds were only sampled in this context. The position in the food web of the two resident fish species (A. microlepis and G. oceanicus) showed that their potential sources of food could be green algae, MPB, Copepoda, Ostracoda, the three genera of Nematoda (excluding *Sphaerolaimus* sp.), and Tanaidacea (Fig. 2). These sources were thus used in the mixing models run for each fish as consumers in each of the four contexts.

## 3.2. Primary sources used by the first consumers, the meiofauna

According to the mixing models, the MPB was the main contributor to the isotopic composition of most first consumers of the meiofauna (Copepoda, Ostracoda, *Metachromadora* sp. and *Pseudochromadora* sp.), whatever the site and season (Fig. 3). For *Halomonhystera* sp., the MPB dominated only in Sinnamary during the dry (80.0 %) and wet seasons (78.7 %) and was replaced by green algae in Awala during the dry (60.2 %) and wet seasons (61.8 %). The MPB contribution to the isotopic composition of the meiofauna taxa in Awala varied from 79.1 % for Copepoda during the wet season to 32.3 % for *Halomonhystera* sp. during the dry season. In Sinnamary, the MPB contribution to the isotopic composition of the meiofauna taxa was even more important, with contributions varying from 93.3 % for Copepoda (wet season) to 61.6 % for Ostracoda (dry season).

In Awala during the dry and wet seasons respectively, the main second source contributing to the isotopic composition of the meiofauna was green algae for Copepoda (20.2 % and 13.4 %), Ostracoda (41.0 % and 12.5 %), and *Metachromadora* sp. but only during the wet season (31.5 %), while during the dry season it was mangrove leaves (18.9 %).

Contrastingly in Sinnamary, only two meiofauna taxa had a second source contributing to their diet: green algae for Ostracoda (26.1 %) during the dry season, and mangrove leaves for *Halomonhystera* sp. during the wet season (17.3 %) (Fig. 3).

## 3.3. Food sources used by resident fish species

The results of the mixing models showed that the isotopic composition of the two fish species depended on different proportions of primary producers, meiofauna, and macrofauna (Fig. 4). There is no effect of seasons on the isotopic composition of the resident four-eyed fish, A. microlepis. In Awala, this species depended mainly on MPB and Copepoda during the dry (32.4 % and 20 % respectively) and wet seasons (17.2 % and 20.2 % respectively). In Sinnamary, A. microlepis isotopic composition depended principally on Nematoda and MPB during the dry (20.7 % and 17.2 % respectively) and wet seasons (23.4 % and 16.8 % respectively). Other food items contributing to isotopic composition of A. microlepis were similar in Awala during the dry and wet seasons and included green algae (7.2 % and 11.9 %), Nematoda (11.4 % and 9.7 %), Ostracoda (8.4 % and 16.9 %) and Tanaidacea (9.4 % and 12.9 %). This composition was similar in Sinnamary with green algae (7.2 % and 11.9 %), Nematoda (11.4 % and 9.7 %), Ostracoda (8.4 % and 16.9 %), and Copepoda (absent and 12.9 %) during the dry and wet seasons.

In Awala, the isotopic composition of the resident fish, G. oceanicus, is somewhat similar throughout the year with contribution of Tanaidacea (23.7 %) and MPB (17.1 %) during the dry season and MPB (33.3 %) and Copepoda (18.3 %) during the wet season. However, the isotopic composition of this species varied seasonally in Sinnamary, with the principal contribution of Nematoda (35.6 %) and Ostracoda (22.5 %) during the dry season, and Copepoda (19.8 %), MPB (18.5 %), and green algae (16.7 %) during the wet season.

The second sources contributing to the isotopic composition of G. oceanicus varied according to context as did their primary ones. In
<figure><img src="image_7.png" /><figcaption>**Fig. 3.** Boxplots of the median contributions (with 50 % and 95 % Bayesian confidence intervals) of each source (green algae, mangrove leaves and MPB) to the five taxa of meiofauna (Copepoda, *Halomonystera* sp., *Metachromadora* sp., *Pseudochromadora* sp. and Ostracoda) during the dry (clear plots) and wet (dark plots) seasons in Awala and Sinnamary. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</figcaption></figure>

<figure><img src="image_8.png" /><figcaption>**Fig. 4.** Boxplots of the median contributions (with 50 % and 95 % Bayesian confidence intervals) of each source (green algae, MPB, Copepoda, Nematoda, Ostracoda, and Tanaidacea) to the two resident fish species: *Anableps microlepis* and *Gobionellus oceanicus*, during the dry (clear plots) and wet (dark plots) seasons in Awala and Sinnamary. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</figcaption></figure>

Awala, this species secondarily depended on green algae (13.3 % and 7.9 %), Nematoda (10.0 % and 8.2 %), and Ostracoda (12.4 % and 11.2 %) respectively for the dry and wet seasons. In Sinnamary, the role played by Copepoda (9.7 %) during the dry season is replaced by Tanaidacea (11.3 %) during the wet season (Fig. 4).

### 3.4. Food sources used by shorebirds

The results of the mixing models showed that the isotopic composition of the three species of birds depended on different proportions of primary producers, meiofauna, and macrofauna (Fig. 5). The isotopic composition of the least sandpiper was mainly based on green algae (28.6 %) and Tanaidacea (17.2 %), while the semipalmated plover and the semipalmated sandpiper depended mainly on MPB (24.9 % and 37.4 %).
<figure><img src="image_9.png" /><figcaption>Fig. 5. Boxplots of the median contributions (with 50 % and 95 % Bayesian confidence intervals) of each source (green algae, MPB, Copepoda, Nematoda, Ostracoda, and Tanaidacea) to the three bird species: the least sandpiper, the semipalmated plover and the semipalmated sandpiper, during the dry season in Awala. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</figcaption></figure>

% respectively), and to a lesser extent on green algae (17.8 %) for the semipalmated plover, and Tanaidacea (18.6 %) for the semipalmated sandpiper.

The second source contributing to the isotopic composition of the three species of birds showed that they depended globally on similar proportions of Copepoda, Nematoda and Ostracoda (9.8 %, 11.2 % and 10.8 % for the least sandpiper, 13.3 %, 12.8 % and 7.8 % for the semipalmated plover, and 16.5 %, 9.5 % and 8.9 % for the semipalmated sandpiper respectively) (Fig. 5).

## 3.5. Isotopic niches of shorebirds and resident fish at Awala during the dry season

The isotopic niche widths of shorebird and resident fish species of Awala during the dry season varied as the Mean SEA_B [CI95] was maximum for *G. oceanicus* (4.268 ‰² [2.512–8.513]), then decreased for the least sandpiper (2.826 ‰² [1.530–6.191]), *A. microlepis* (1.573 ‰² [1.122–2.224]), the semipalmated sandpiper (1.375 ‰² [1.098–1.748]) and the semipalmated plover (1.165 ‰² [0.575–2.725]) (Fig. 6). Correction for sample size applied to SEA_B did not significantly alter the niche widths of these species, but marginally for *G. microlepis* (SEA_B = 4.268 ‰², SEAc = 5.196 ‰²) and the least sandpiper (SEA_B = 2.826 ‰², SEAc = 3.601 ‰²) (Supplementary material).

Each shorebird and resident fish species overlapped with each other (Fig. 7). The isotopic niches of *G. oceanicus* and the least sandpiper, which were the widest niches observed (Fig. 6), were the most overlapping ones on other species (Fig. 7). By contrast, the isotopic niches of the semipalmated plover, the semipalmated sandpiper and *A. microlepis*, which were the smallest niches observed (Fig. 6), were the most overlapped ones (i.e. the species expected to be the most impacted ones in case of trophic competition) (Fig. 7).

## 4. Discussion

### 4.1. Carbon origin in the tropical mudflat foodweb of French Guiana

Our results demonstrated that the carbon origin in French Guiana mudflat foodweb, from the meio- to the macrofauna, mostly derived from the MPB, at both seasons (dry and wet) and sites (Awala and Sinamary). Indeed, the MPB contributed to more than 60 % of the isotopic composition of the meiofauna. In temperate mudflats, the benthic foodweb is supported by the primary production of the MPB (Leguerrier et al., 2003; Rzeznik-Orignac et al., 2003; van Oevelen et al., 2006), representing 35–70 % of the benthic consumer diet (the

<figure><img src="image_10.png" /><figcaption>Fig. 6. Resident fish and shorebird isotopic niche widths as Bayesian standard ellipse areas (SEA_B) for δ¹³C and δ¹⁵N. Box width and colour denote credible intervals (colours: 50 %, medium, first box: 75 %, narrow, second box: 95 %); black dots: median, red crosses: predicted standard ellipse area of 95 % (2.5 %–97.5 %) corrected by sample size (SEAc). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</figcaption></figure>
<figure><img src="image_11.png" /><figcaption>**Fig. 7.** Bipartite graph of the overlapping niches of resident fish and shorebird species (left group) on the isotopic niche width of overlapped species (right group). Niche width is retrieved as Bayesian standard ellipse areas (SEA_B) for δ¹³C and δ¹⁵N of each species. The width of the bars between the left and right groups represents the expected proportion (see numbers) of potential impact from the left species on the right ones in case of trophic competition between these species, calculated as the overlap between the two species divided by the niche width of the right one.</figcaption></figure>

meio-macrofauna) (Pascal et al., 2009; Ubertini et al., 2012). In temperate mudflats, the meiofauna has a small biomass but is described as a very active compartment compared to the macrofauna (Leguerrier et al., 2003; van der Heijden et al., 2020), with a central role in the functioning of these ecosystems (Gray and Elliott, 2009; Ubertini et al., 2012). In French Guiana mudflats, the meiofauna is more abundant than the macrofauna (Dupuy et al., 2015; Nguyen et al., 2017; Jourde et al., 2017) and is thus expected to play a key role in these ecosystems.

As described by several studies (Lee, 1995; Burford et al., 2008; Zulkifli et al., 2016; Lee et al., 2019), and despite high potential flow of terrestrial and estuarine inputs, mangrove isotopic contribution to the meiofauna and other consumers of higher trophic level was always low in the mudflats investigated. Note that the isotopic signature retrieved for mangrove leaves (A. germinans, L. racemosa, and R. mangle) in Sinamary during the wet season, were consistent with other studies in Brazil, French Guiana or Malaysia (Dittmar and Lara, 2001; Gontharet et al., 2014; Larcher et al., 2016; Lee et al., 2019). In French Guiana mudflats, green algae, as well as the MPB, were retrieved as an important source of carbon in Awala for Ostracoda and *Halomonhystera* sp. In our results, green algae and MPB had similar δ¹³C values, so the integration of green algae as a primary food source in our models could have biased the real contribution of the MPB in the foodweb. Green algae were suggested to play a role in the foodweb of the Malaysian tropical mudflat (Zulkifli et al., 2016) but this study did not consider the MPB potential contribution. Interestingly in this study, the isotopic compositions of the mudflat green algae are comparable to ours (4 and -20 ‰ in δ¹⁵N and δ¹³C respectively in Malaysia, 3 and -17 ‰ in French Guiana) and green algae are described as the main primary source of the mudflat food web compared to mangrove leaves. Although the MPB is the main source of carbon in French Guiana mudflat foodweb, its availability to consumers (i.e. the MPB production) was not measured in

our study, nor elsewhere (Dupuy et al., 2015). Therefore, the potential competition between consumers that could be induced by constrains of the MPB access could not be assessed. Further studies would be valuable to decipher the functioning of these ecosystems in relation to the MPB production.

## 4.2. The mudflat foodweb complexity in French Guiana

Our study also provides a thoroughly description of the tropical mudflat foodweb from primary producers to predators in French Guiana. Among taxa sampled, the meiofauna was the most difficult to explore in terms of trophic relationships, because of species identification difficulties. Nevertheless, our results demonstrated that the meiofauna occupies almost all trophic levels. Indeed, most of the meiofauna species sampled were grazers, other had mixed diet including primary producers and primary consumers, while some were predators, sharing δ¹⁵N values of vertebrates like for instance shorebirds and resident fish. Our results showed that Copepoda were mainly dependent on the MPB, whatever the sites and seasons. Similarly, Ostracoda relied principally on the MPB during the wet season, while during the dry season a mix of MPB and green algae was observed. In Nematoda, our results are consistent with diets described in the literature in which *Pseudochromadora* sp. and *Metachromadora* sp. are classified as “epistrate feeder”, *Halomonhystera* sp. is a “non selective deposit feeder”, and *Sphaerolaimus* sp. is an “omnivore predator” (Wieser, 1953).

As for the meiofauna, the macrofauna and fish taxa, with high δ¹³C values, mainly depend on the MPB. This is consistent with literature on fish sampled in tropical mudflats (e.g. Lugendo et al., 2006; Kruitwagen et al., 2010; Shahraki et al., 2014; Lee et al., 2019). This dependence is either direct as for example in MPB consumers (e.g. Tanaidacae), or indirect for higher consumers which feed on them. Only four transient
fish with low $\delta^{13}$C values, one benthic (the longtail sole) and the three species of snooks, appeared to depend more on mangrove leave carbon than on MPB one. These species are described as estuarine and two of them are known to enter in rivers (the longtail sole and the fat snook, the lowest $\delta^{13}$C values species) (Aliaume et al., 1997; Barros et al., 2011). In addition to their differential habitat exploitation (riverine and estuarine), they are predators, consuming young fish and/or crustaceans. Therefore, they potentially rely more on terrestrial-freshwater preys (not sampled) than other fish taxa investigated. Some fish taxa sampled in mudflat were found only as juveniles (*C. psittacus*, Engraulidae, *H. jaguana*, Mugilidae, *P. atherinoides*) confirming the nursery role of the mudflat often evoked in literature (e.g. Tse et al., 2008; Marley et al., 2020; Pessanha et al., 2021). Adult fish sampled exhibited diversified trophic ecology including benthophagous species (e.g. the catfishes, and Pleuronectiforms) and pelagic predators (e.g. Clupeiforms, the tarpon (*M. atlanticus*), and the acoupa weakfish (*C. acoupa*)).

In our study, the two resident fish species of mudflats, the highfin goby (*G. oceanicus*) and the four-eyed fish (*A. microlepis*), were expected to consume the MPB. The highfin goby is the only species able to stay at low tide in burrows, while the four-eyed fish, more mobile, reaches shallow waters of the mudflat at low tide (Kervath et al., 2001). As expected, both species, as well as Mugilidae, were the most MPB-dependant fish. Additionally, they presented a low intermediate trophic position (between the first and secondary consumers), probably reflecting a mixed diet based on the MPB and its associated meiofauna. The highfin goby is described as a detritivore and primary consumer (Vasconcelos Filho et al., 2003). The isotopic ratios retrieved in our study allowed to fine tune the feeding ecology of this species in mudflat. Indeed in Awala, the highfin goby diet mainly relied on Tanaidacea and MPB as first and second sources respectively during the dry season, while during the wet season, the MPB became the first source followed by Copepoda. In Sinnamary, Nematoda was the first source followed by Ostracoda during the dry season, while the highfin goby fed indifferently on Copepoda, the MPB and green algae during the wet season. The four-eyed fish exhibited a less diversified diet than the highfin goby in our study. In Awala, the four-eyed fish consumed mainly MPB as first source followed by Copepoda during the dry season, and inversely during the wet season. In Sinnamary, Nematoda was the first source followed by the MPB during the dry and wet seasons. Although this fish is more mobile than the highfin goby, its isotopic niche width was smaller, demonstrating that the four-eyed fish diet is more specific than the highfin goby one. This was confirmed by Kervath et al. (2001), who described in the four-eyed fish, a more specialised feeding behaviour in muddy substrate, mostly composed of smaller food particles (<2 mm in length of algae, "worms" and crustaceans) than in sandy ones (crustaceans, bivalves and macrobenthos). Another insight from our results was that it confirmed that the four-eyed fish sampled in Awala and Sinnamary in French Guiana was seemingly highly specific to mudflats and probably did not visit sandy beaches.

Among the 28 species of shorebirds overwintering or residing in French Guiana, the semipalmated sandpiper (*Calidris pusilla*) is by far the most abundant species representing half of the birds caught in this area (Laguna et al., 2012; Morrison et al., 2012). The least sandpiper (*Calidris minutilla*) is also an abundant species, as well as the semipalmated plover (*Charadrius semipalmatus*) (Laguna et al., 2012). These three species exceed 350,000 individuals during fall migration and between 50,000 and 100,000 during winter on the coast of French Guiana (Laguna et al., 2012). Inherently to the bird flying/movement capacity, and as birds sampled in this study were caught on roost bordering the rice fields of Mana, it was not possible to define the exact feeding area of each species. The least sandpiper is the most common species foraging in growing mangroves (Bocher, pers. obs.), explaining probably its distinct isotopic composition from the other two species. In French Guiana, while the least sandpiper relied mainly on green algae as primary food sources, the diet of the semipalmated sandpiper and the semipalmated plover were mainly based on the MPB. Indeed, the semipalmated sandpiper is known

to feed on the MPB and the crustacean, *Corophium volutator*, during its migratory stopover in the Bay of Fundy in Canada (Hamilton et al., 2006; Cheverie et al., 2014). In French Guiana, the three species fed on Tanaidacea, as well as Copepoda for the semipalmated plover and the semipalmated sandpiper, and also on Nematoda for the later. The diet dissimilarity observed in the semipalmated sandpiper and the semipalmated plover could be explained by a different beak structure (Elner et al., 2005). The isotopic most overlapping niche was observed in the least sandpiper, demonstrating that this species dominated the community. By contrast, the niches of the semipalmated sandpiper and the semipalmated plover were the most overlapped ones by the least sandpiper and the two resident fish species studied. Finally, some overlapping between the niches of the shorebirds and the resident fish studied were also observed. In this sense, the trophic competition between shorebirds and fish could be limited, as the formers exploit the mudflat food sources at low tide (Fonseca et al., 2017), while fish at high tide. Although the fish *G. oceanicus* remains buried on the mudflats at low tide, its feeding activity may be reduced, as they likely become exposed to predation by fish-eating birds (authors pers. obs.). Nevertheless, trophic competition could be triggered if food resources become limited.

## 5. Conclusion

This study provides evidence that the tropical mudflat foodweb in French Guiana deeply relies on a mudflat origin of carbon. Most organisms, even the most mobile ones like shorebirds or fish species, were highly dependent on the MPB, and considerably less on terrestrial (mangrove leaves) and coastal inputs (green algae). The variety of trophic levels observed in this tropical foodweb traduces a particularly complex network, where for instance the trophic level of some meiofauna species is equivalent to some fish or bird one. This is confirmed by the observed overlapping niches of some mudflat associated species. Further studies are needed to characterize these species trophic competitive interactions and the carrying capacity of tropical mudflats.

### CRediT authorship contribution statement

**Alexandre Carpentier:** Writing – review & editing, Writing – original draft, Visualization, Validation, Supervision, Methodology, Investigation, Formal analysis, Data curation, Conceptualization, Resources.
**Anne Lizé:** Writing – review & editing, Writing – original draft, Validation, Methodology, Formal analysis, Data curation. **Hien Nguyen Thanh:** Writing – review & editing, Data curation, Resources. **Pierrick Bocher:** Writing – review & editing, Validation, Supervision, Resources, Project administration, Methodology, Investigation, Funding acquisition, Data curation, Conceptualization. **Christel Lefrançois:** Writing – review & editing, Visualization, Validation, Methodology, Data curation, Conceptualization, Project administration, Resources. **Antoine Gardel:** Data curation, Funding acquisition, Resources, Writing – review & editing. **Pierre-Yves Pascal:** Writing – review & editing, Validation, Methodology, Conceptualization, Data curation, Resources. **Christine Dupuy:** Writing – review & editing, Validation, Supervision, Resources, Project administration, Methodology, Funding acquisition, Formal analysis, Data curation, Conceptualization.

### Disclosure statement

No potential conflict of interest was reported by the author(s).

### Funding details

This work was supported by the Ministry of Education and Training of Vietnam, the University of Science and Technology of Hanoi (USTH, Vietnam), the LIENSs laboratory of the University of La Rochelle and the European Regional Development Fund (ECOCOT).
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 the Awala reserve for providing the access to the coast in French Guiana and the laboratory in Awala. We are also thankful to Julien Guillaudeau for his fieldwork support, Gaël Guillou for stable isotope analysis at the platform IRMS of the University of La Rochelle and Sophie Dubois from Anastats for the statistical help.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.ecss.2025.109257.

Data availability

The raw data, model results and R script are provided as supplementary materials

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