Function in ecology can be understood as the role that each component plays in the surrounding environment (i.e., control the fluxes of energy, nutrients, and organic matter) (Calow, 1987; Jax, 2005; Bellwood et al., 2019). But, in the ecological literature, the term is used in different ways depending on the scale (local or regional) and/or the object (individual, population, or ecosystem) (Nunes-Neto et al., 2013; Mlambo, 2014; Queirós et al., 2015; Clare et al., 2016; Luiza-Andrade et al., 2017; Drylie et al., 2020). At the individual level, function is the role that an organism plays in the environment, and at the ecosystem level it refers to the combined effects of all natural processes that sustain an ecosystem and can result in global processes and ecosystem services (Paterson et al., 2012; Snelgrove et al., 2014; Degen et al., 2018).

Determining the roles that organisms play is important to identify key species and understand ecosystem functioning (Bremner, 2008). One way to access the ecological functions performed by species is to classify them into functional groups according to a set of characteristics, i.e., traits, that respond to certain environmental conditions (Díaz and Cabido, 2001). These functional traits, for instance, may describe the way of life, feeding mode and reproduction strategies, which are associated with intrinsic biological characteristics as well as with activities that organisms perform in the ecosystem (Violle et al., 2007; de Bello et al., 2010).

The distribution of functional traits in a community can be a better indicator of ecosystem functioning than assemblage structure, including species abundance, richness and other metrics (e.g., Bolam et al., 2002). For instance, different species can have similar traits, thus performing similar functions. Therefore, functional redundancy may occur when in the absence of one taxon, another (with a similar set of traits) performs the same function (Walker, 1995; Magalhães and Barros, 2011). On the other hand, species with different traits will perform different functions resulting in complementarity and in an increase of functional diversity (Loreau et al., 2001; Hillebrand and Matthiessen, 2009).

It is well known that benthic macroinvertebrates are very important for estuarine and marine habitats and that polychaetes are frequently an abundant and diverse group (Hutchings, 1998; Magalhães and Barros, 2011; Barros et al., 2012). Due to their large morphological variability, they have an array of traits, including different feeding modes, movement capabilities and reproduction types. Through different trait combinations, polychaetes can perform several functions such as sediment stabilization, sediment oxygenation and transport of dissolved material from water to sediment (Braeckman et al., 2010; Wong and Dowd, 2015; Wrede et al., 2018; Bhowmik and Mandal, 2021). For example, the ability to burrow the sediment and construct tubes facilitates the penetration of water and oxygen, therefore increasing oxygenation (i.e., aeration function) of the sediment (Aller, 1988; Shull et al., 2009; Laverock et al., 2011; Kristensen et al., 2012; Queirós et al., 2015; Murphy and Reidenbach, 2016; Wrede et al., 2017). However, how these functions are distributed in space and time depends in part on how species, and thus, their functional traits, respond to environmental variations.

It is well known that estuaries are strong environmental gradients that are subject to great variability in their environmental conditions (e.g., salinity, grain size, and organic matter content) due to the mixing of freshwater and seawater (McLusky and Elliott, 2004). Different taxa interact with the physical and chemical characteristics of the environment, thus environmental variables can act as filters (e.g., Egres et al., 2019), selecting taxa with sets of traits that will occupy different estuarine regions. From this perspective, the environment is a selective force and filter, excluding species that are unable to tolerate certain conditions at a particular location (Kraft et al., 2015). Therefore, environmental variability plays an important role structuring estuarine benthic macroinvertebrate communities (Alves et al., 2020) and selecting traits (e.g., Morais et al., 2019).

The spatial patterns of benthic assemblages in estuaries has been described by several studies. For instance, lower estuarine regions have a greater number of taxa (Ysebaert et al., 2003; Fujii, 2007; Barros et al., 2012, 2014; Alves et al., 2020) in part due to the fact that most species found in estuaries have a marine origin. Thus, sites closer to the marine waters are richer than sites closer to freshwater, as fewer estuarine species can arrive and/or survive in lower salinity (Attrill and Rundle, 2002). It has been suggested that changes of species along the salinity gradient can result in modifications in ecosystem functioning (Oug et al., 2012; van der Linden et al., 2016). However, most functional studies are focused on the effects of environmental impacts on traits (Bremner et al., 2003, 2006a,b; Paganelli et al., 2012) and do not explore how these changes explicitly translate into different functions, or function intensities. Thus, the knowledge on how functions of the benthic community are distributed along estuaries and how it varies in time (e.g., weeks, months, seasons, or years) is still limited (Darr et al., 2014; van der Linden et al., 2016, 2017).

There are a variety of ways to access the ecological function (Petchey and Gaston, 2002; Podani and Schmera, 2006; Villéger et al., 2008; Pla et al., 2012). However, they often consider ecological function as an emerging property of the community, and the information on which taxa or trait play an important role for a given function is frequently overlooked (Teal et al., 2009, 2010; Sturdivant et al., 2012; Queirós et al., 2013, 2015). Many studies use species traits that are not linked to any function (Mlambo, 2014) and this can lead to wrong conclusions about the functioning and the fate of a given estuarine area. For example, the selection of excessive redundant traits can overestimate functional diversity. On the other hand, if an essential trait for a given function is not considered, this can lead to an underestimation of this function.

The aim of the present study was to investigate the distribution pattern of ecological functions over space and time in estuarine environments, through the use of combinations of specific functional traits. For this, we first: (i) defined combinations of functional traits explicitly related to ecological functions in estuaries; (ii) established the intensity of the functions performed by polychaetes; and (iii) tested for potential differences in the intensity of ecological functions in different salinity zones (following the Venice System). Our expectation was that the functional structure would not significantly change along the estuarine gradient (i.e., salinity zones). This expectation assumes that some subsets of taxa are spread along the estuarine gradients (Alves et al., 2020) and will contribute to the function maintenance.

Bioturbation, organic matter fragmentation and nutrient cycling were the most frequent functions performed by polychaetes along the estuarine systems, remaining present throughout the gradient but with variable intensities. Although bioturbation is frequently perceived as a small-scale phenomenon, this function has important roles in estuarine systems. For example, it causes topographic variation, increases in aeration and oxygenation of deep layers of sediment, directly affecting community metabolism, changes in organic content, reworking of sediments, reduction of sediment compaction and influences the fate of pollutants (metals, organic pollutants) (e.g., Little, 2000; Gray and Elliott, 2009; Day et al., 2013). Bioturbation is even more relevant in areas with muddy sediments, with low permeability, low concentrations of oxygen and a greater accumulation of contaminants (i.e., reduced water exchanges between sediments and water column) (Hatje et al., 2006; Mermillod-Blondin, 2011). In the three estuaries investigated, the highest percentage of fine sediments was found mainly in high salinity zones (Barros et al., 2012). Virtually all taxa identified in the three estuaries were classified as bioturbators, with the exception of two less frequent and abundant taxa (Sphaerodoridae and Sigalionidae). Trichobranchidae showed the highest score for bioturbation, being a subsurface deposit feeder, mobile, with a large body and tubicolous. These polychaetes can burrow the sediment in search of food in the lower layers and promote mixing of the sediment and water inflow (Kristensen et al., 2012; Jumars et al., 2015).

Fragmentation of organic matter also plays relevant roles such as reducing the particle size of detritus due to ingestion and passage through the digestive tract, increasing the susceptibility to microbial attack, enhancing rates of decomposition of detritus favoring active bacteria and mobilizing nutrients (Day et al., 2013). Nereididae was one of the most frequent and abundant taxa and, since they are omnivorous and have jaws, these organisms can reduce the particle size of detritus (Jumars et al., 2015). This taxon contributed to the maintenance of fragmentation intensity along the estuarine gradient. Bioturbation and fragmentation were performed more intensively in euhaline zones, decreasing in mesohaline but increasing in oligohaline zones. In this zone many polychaetes do not tolerate the low salinity conditions, therefore Nereididae can be found and are functionally crucial for increase the bioturbation and fragmentation in the upper estuary.

The variation of intensity in nutrient cycling along estuaries was similar to fragmentation, but frequently decreased in the upper estuary (i.e., oligohaline zone). Nutrient cycling increases nutrient fluxes, mobilization and transferring of nutrients between different sediment compartments (Day et al., 1987). Many taxa showed traits that allowed them to perform this function, contributing to the maintenance of nutrient cycling along the estuary. For example, Cirratulidae and Orbiniidae, which were quite frequent and more abundant in the lower estuary (e.g., euhaline and polyhaline zone), contributed to an increase in nutrient cycling in these zones. Additionally, Capitellidae (also abundant in these zones) were also found in the upper estuary (e.g., Oligohaline zones). Therefore, cirattulids and capitellids, being depositivorous, mobile, burrowing and infaunal, are especially important for cycling the nutrients in estuaries.

Stabilization of sediment, although less observed, was more frequent in the polyhaline zone and sometimes in the euhaline zone (i.e., Paraguaçu and Subaé estuaries). It was performed by traits found in Sabellidae, Serpullidae, and Terebellidae. These taxa occurred in the lower Subaé and Paraguaçu estuaries at one occasion and in the middle of Jaguaripe and Paraguaçu estuaries. Sabellidae and Serpulidae share several traits, such as tentacular crown and the capacity for building mucous and sediment tubes. These taxa are sessile and suspension feeders like Terebellidae and largely dependent upon bottom currents to bring particles within range of their collecting systems (Jumars et al., 2015). In many large Sabellidae and Terebellidae, the tube is occupied permanently while serpulids can secrete calcareous tubes. Stabilization promotes resistance to erosion by water flow and may facilitate recruitment of some taxa (Little, 2000). We did not observe this function in the oligohaline zones, which are usually composed of coarser sediments (Barros et al., 2012) a result of strong currents which may not allow the construction of semi-permanent tubes.

Benthic secondary production in general is high in the estuarine system when compared with other aquatic ecosystems (Day et al., 2013). It controls the energy flow through the food web, supporting a high diversity of organisms in the sediments and water column (e.g., larger invertebrates, demersal nekton and wading and diving birds) (Day et al., 2013). This function may be affected by stresses of the estuarine environment, such as salinity variation (Day et al., 2013). Polychaete secondary production was remarkably smaller than bioturbation and fragmentation but increased in oligohaline zones, reaching similar proportions to those other functions in this region. Information about the reproductive traits of polychaetes is not always accessible and, since we did not use biomass but body size as a proxy, proper formal testes are needed for evaluating if secondary production in estuarine sediments is really more intense in the upper estuary.

There are a few studies on ecological function along estuarine gradients (Oug et al., 2012; Otegui et al., 2016; van der Linden et al., 2016) but they are mostly based in the variability of all biological traits (Bremner et al., 2006a,b; Paganelli et al., 2012; van der Linden et al., 2012, 2017; Veríssimo et al., 2012; Darr et al., 2014; Egres et al., 2019). It has been suggested that the use of any functional traits can result in a redundant trait or in traits not necessarily related to the functions (Mlambo, 2014; Beauchard et al., 2017; Luiza-Andrade et al., 2017). Therefore, functions are often not explicitly addressed, neither are traits precisely associated with specific functions. Some studies use indexes that gather all traits information and calculate functional diversity in the environment (Lefcheck et al., 2015; van der Linden et al., 2016), but the interpretation of which function is varying might be complex.

The understanding of ecosystem functioning improves when we define how combinations of functional traits are related to specific functions and the mechanism by which these traits perform their roles (de Bello et al., 2010; Beauchard et al., 2017). In the present study, traits were clearly associated with function allowing the evaluation of function intensity along an ecological gradient.

Synthesizing information from the literature on which traits are associated with specific ecological functions is the first step for experiments to be performed and to actually test the effect of specific functional traits on sedimentary processes and ecosystem properties (de Bello et al., 2010; Mlambo, 2014). Much experimental work is needed to evaluate who (i.e., trait) does what (i.e., function) and at which intensity. For instance, experiments measuring how the movement of an organism, when building galleries and feeding on deposits, will affect the fragmentation of organic matter, are necessary.

This study showed that the distribution of ecological functions is dynamic, and varies in time and space. Variability was observed in the patterns of functions at different times, especially in the estuaries of Paraguaçu and Subaé. where the intensity of some polychaetes functions increased in time. In the Paraguaçu estuary, the change in sediment stabilization in the different sampling dates along the salinity zones was marked. This may be caused by differences in hydrodynamical regimes which shows the demand for research investigating the drivers of variation in function intensity under different situations (e.g., low to extreme river flows).

Biological assemblages and their distribution of functional traits determine the roles that will be performed at each environment and make possible to predict how the environment might recover from different disturbances (e.g., dredging event, dam construction) (de Bello et al., 2010; Bolam, 2014). For instance, functional redundancy allows the function to continue to be performed (Walker et al., 2004; Olsgard et al., 2008; Magalhães and Barros, 2011). That is, even in the absence of a taxon, due to some disturbance, there may be other species with similar traits capable of keeping the function (i.e., functional compensation; Walker, 1995; Naeem, 1998). Thus, ecological functions are indicative of ecosystem health and resilience and are intrinsically related to various ecosystem services that benefit society (Millennium Ecosystem Assessment, 2005; Strong et al., 2015).

It is important to investigate how each set of environmental characteristics (e.g., salinity, particle size, and organic matter) and how human impacts can affect the distribution of ecological functions. Using traits associated with specific ecological functions, rather than all available traits, allows one to observe patterns of function variation in space and time. Future studies may investigate how each function responds to different variables and also empirically test how traits alter environmental characteristics (sediment oxygenation, nutrient content) and ecosystem properties (resilience).

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.

AM: conceptualization, formal analysis, data curation, methodology, and writing – original draft. FB: supervision, conceptualization, formal analysis, data curation, methodology, and writing – review and editing. Both authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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