Importance of estuary morphology for ecological connectivity with their adjacent coast: A case study in Brazilian tropical estuaries

Highlights

• The origin of the organic matter underlying food webs was investigated in three estuaries with distinct morphologies.

• Coastal organic matter contributed more to fish diet when landscape properties enabled a better sea-connection.

• Estuary morphology regulates interactions between estuaries and their adjacent coast.

Abstract

Coastal habitats are interlinked by ecological connectivity, defined as the exchange of organic matter or organisms between habitats. The degree of this connectivity will depend in particular on the geometric properties of the landscape. The increasing anthropogenic alterations in estuaries therefore raises the need to understand how their morphological characteristics influence fluxes between habitats. We used stable isotopes to investigate the variability of ecological connectivity between three estuaries and their adjacent coastal areas by tracking the origin of the organic matter (estuarine vs coastal) underlying the diet of the migrant species Eucinostomus argenteus. The chosen estuaries were geomorphologically distinct, exhibiting, in particular, differences in their degree of connection to the sea, corresponding to the morphological features (shape, mouth width) controlling key physico-chemical variables in this habitat (e.g. salinity). The sampling of the basal food sources contributing to the food web was performed in the three estuaries and in their adjacent coasts. The variability in stable isotope ratios between estuaries was examined for both fish and sources of organic matter. In the three estuaries, Bayesian models were applied for each season (dry and rainy) to quantify the relative contribution of sources from estuarine and coastal environments supporting the diet of the silver mojarra. The share of coastal organic matter increased with the degree of sea connection, indicating that the properties of the seascape can regulate the intensity of interactions between ecosystems. Variations in ecological connectivity are likely to affect the functioning of ecosystems as they influence trophic pathways and energy flows between adjacent habitats. Morphological modifications could thus significantly disturb ecosystems by altering the structure of food web, thereby affecting certain ecosystem services such as the availability of living marine resources.

Introduction

The emergence of seascape ecology brought the need to consider coastal habitats as a single continuum rather than as separate biomes (Green et al., 2012; Berkström et al., 2013). This conceptual change aimed at a more integrated management of the coastal zone (Beger et al., 2010). In particular, addressing the connectivity between habitats is essential for fisheries management because coastal habitats provide complementary ecological functions that are critical for marine living resources (Sheaves, 2009). Coastal habitats should therefore not be considered as isolated patches in which different sub-populations occur, since a comprehensive view reflects population dynamics more accurately (Burgess et al., 2014).

Ecosystem interactions can be primarily subdivided into biological, chemical and physical interactions (Ogden, 1997). The connectivity degree between coastal habitats will depend in particular on the geometric properties of the landscape (Olds et al., 2017). More specifically, landscape characteristics affect ecological connectivity which consists of the interactions between ecosystems through the movement of organisms and the exchange of nutrients and organic matter that are involved in ecological processes within these systems (Nagelkerken, 2009). Previous work demonstrated that variability in the geometric characteristics of the seascape, such as the distance between habitats, can affect the intensity of flows between habitats (Mumby et al., 2004; Berkström et al., 2013).

Estuaries include a wide range of different transitional water bodies with distinct landscape characteristics (Flemming, 2011). Thereby, the classification of estuaries requires the consideration of physico-chemical variables such as hydrodynamics and bathymetry, as they determine not only the dynamics and structure of the sediments, but also the nature of the primary producers (Elliott and McLusky, 2002; Whitfield and Elliott, 2011). Consequently, the morphology of estuaries and, in particular, the set of geometrical variables controlling the degree of sea water dilution in the estuary (like depth and mouth width), could have an influence on ecological connectivity. This morphological variability, which can be viewed as their degree of connection to the sea, is likely to enhance or prevent flows with adjacent coastal habitats. In addition, estuarine morphologies suffer from increasing anthropic alterations, such as the construction of polders, harbours or dykes which can drastically change the sedimentary dynamics and the composition of estuarine biological communities (Wetzel et al., 2012; Du et al., 2016; Lechêne et al., 2018). It is thus relevant to investigate how estuarine morphological characteristics influence interactions between habitats. The implications of this variability in terms of ecosystem functioning need to be taken into account before deciding to modify seascape features or implement restoration measures through eco-engineering (Elliott et al., 2016).

Understanding ecological connectivity involves studying energy pathways in food webs and their intrinsic trophic relationships in order to assess community structure and functional role of species living in the ecosystems (Pasquaud et al., 2010; França et al., 2011). Hence, estuarine food webs can be described by characterizing trophic relationships, sources of organic matter and energy flows between system components (Pasquaud et al., 2008). In these complex and dynamic ecosystems, food webs can be supported by the production of various local primary producers, as well as the transport of organic matter from adjacent coastal and riverine areas (Choy et al., 2009; Selleslagh et al., 2015). However, identifying the origin of the organic matter at the base of estuarine food webs can be difficult, in particular because conventional methods like gut content analysis provide only a snapshot of the diet at a given time (Pasquaud et al., 2008, 2010; França et al., 2011). Moreover, gut analyses do not enable a comprehensive food web analysis to reliably track the source of the organic matter underlying the diet of high trophic level consumers that do not feed directly on primary producers.

Stable isotope methods produce estimates of trophic position that can both capture complex trophic interactions and track energy flows between habitats (Carvalho et al., 2017; Whitney et al., 2018; Gonzalez et al., 2019). Since a consumer's stable isotope ratios reflect the values of its food sources, trophic position assessment is possible if the differences in isotopic composition between an animal and its prey, i.e. trophic level enrichment, are known (Caut et al., 2009). Indeed stable isotopes of nitrogen (δ¹⁵N) and carbon (δ¹³C) have been successfully used to study ecosystem functions and food webs (Le et al., 2018). δ¹⁵N can constitute a proxy for the trophic position of an organism since it increases considerably with the trophic level (Post, 2002; Caut et al., 2009). On the other hand, δ¹³C differs substantially between primary producers (Post, 2002; Herzka, 2005), providing an overview of the origin of organic matter (Fry, 2006).

In estuaries, the origin of organic matter has already been studied with stable isotopes and a high contribution of marine basal sources has been highlighted in some studies (Pasquaud et al., 2008; Selleslagh et al., 2015). Nevertheless, other studies conducted in estuaries have shown that in situ primary production can outweigh other food sources and contribute significantly to fish growth (Lobry et al., 2008). Therefore, knowledge on the extent of ecological connectivity between estuaries and their adjacent coastal areas is essential for designing the scale of conservation measures, particularly in the case of migratory species using multiple habitats (Vasconcelos et al., 2010; Reis-Santos et al., 2018).

Migratory species constitute a good proxy to study ecological connectivity between two habitats since their movements represent linkages across the seascape (Selleslagh et al., 2015). In this study, we chose Eucinostomus argenteus Baird and Girard (1855) to investigate the intensity of the flows between habitats. The silver mojarra is a member of the Gerreidae family comprising species with complex life strategies that are important for artisanal fisheries in north-eastern Brazil (Pinto et al., 2013). E. argenteus is one of the main Gerreidae in the region and can be classified as an estuarine-dependent species, as its juveniles are found in great abundance in estuaries (Ramos et al., 2016) where they reside since their reduced size at this ontogenetic stage (less than 13.5 cm) (Bouchon-Navaro et al., 2006) does not allow them to make large migrations (Franco et al., 2012). In those habitats, they were classified as second-order consumers, feeding opportunistically as well on microcrustaceans (amphipods, copepods, tanaidaceous, ostracods) as on detritus with variations in the proportion and frequency of different items according to their ontogeny and food availability (Chi-Espínola et al., 2018). Although adults of these species are more abundant in adjacent coastal areas (Ramos et al., 2016), they use estuaries as a feeding ground, predating mostly on Bivalvia siphons and polychaetes (Vasconcellos et al., 2018) or as a reproductive ground (Chaves and Bouchereau, 2000). The degree of ecological connectivity between estuaries and adjacent coast would be reflected by the dominant origin of the carbon sources (coastal vs estuarine origin) on which the species diet is based.

The objective of this study is to understand the variability in ecological connectivity between estuarine and coastal habitats. We are thus investigating the flows between three morphologically distinct estuaries and their adjacent coastal areas by tracking the origin of the organic matter (coastal or estuarine) underlying the diet of E. argenteus. Our hypothesis is that geomorphological disparities between estuaries influence the origin of the organic matter that supports the E. argenteus regime, based on the assumption that flows are enhanced in the estuaries most connected to the sea.