Introduction
Saltmarshes are plant formations that inhabit the intermediate zone between marine and terrestrial habitats (Regteren et al., Reference Regteren, Amptmeijer, De Groot, Baptist and Elschot2020) and are widely recognized as one of the most productive coastal ecosystems globally (Banerjee et al., Reference Banerjee, Sappal, Ramachandran and Ramesh2017) for their carbon storage capacities (Brown et al., Reference Brown, Conrad, Akkerman, Fairfax, Fredericks, Hanrio, Sanders, Scott, Skillington, Tucker, Van Santen and Sanders2016). Overall, this ecosystem dominates large areas of intertidal zones in temperate regions (West, Reference West and Chapman1977), while in the tropics, saltmarshes are frequently found as patches (Braga et al., Reference Braga, Beasley and Isaac2009, Reference Braga, Silva, Rosa-Filho and Beasley2013) since the mangroves forests limit their distribution to pioneer formations at the seaward edge (Netto and Lana, Reference Netto and Lana1997; Pennings and Bertness, Reference Pennings, Bertness, Bertness, Gaines and Hay2001). Also, these plants have an important role as ecosystem engineers in several intertidal areas (sensu Jones et al., Reference Jones, Lawton and Shachak1994, Reference Jones, Lawton and Shachak1997), since their roots and rhizomes increases habitat complexity both above and below the sediment column (Rader, Reference Rader1984; Lana and Guiss, Reference Lana and Guiss1992; Bonnet et al., Reference Bonnet, Lana and Guiss1994; Netto and Lana, Reference Netto and Lana1996, Reference Netto and Lana1997; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020).
These plants are known as an important nursery ground for several aquatic animals (Minello et al., Reference Minello, Able, Weinstein and Hays2003; Valiñas et al., Reference Valiñas, Molina, Addino, Montemayor, Acha and Iribarne2012). Moreover, saltmarshes provide food, habitat, and refuge from predators for a wide variety of animals (Adam, Reference Adam1990), including the benthic fauna, which occupy a variety of niches (Lillebo et al., Reference Lillebo, Flindt, Pardal and Marques1999). The benthic invertebrates are a dominant and valuable component of saltmarsh and, in general, the diversity and abundance of these organisms are higher in saltmarshes in comparison with bare sediment environments (Netto and Lana, Reference Netto and Lana1996, Reference Netto and Lana1997; Reis et al., Reference Reis, Krull, Carvalho and Barros2019).
Saltmarshes are subject to wide variation in environmental factors, that trigger a series of physico-chemical and biological changes in the benthic system (Levin and Talley, Reference Levin, Talley, Weinstein and Kreeger2000;Neira et al., Reference Neira, Grosholz, Levin and Blake2006; Temmerman et al., Reference Temmerman, Bouma, Van de Koppel, Van der Wal, De Vries and Herman2007). In soft bottom habitats, the benthic fauna is distributed in three-dimensional space (Gray and Elliott, Reference Gray and Elliott2009) and the species composition and distribution (vertical and horizontal) are strongly influenced by changes in the vegetation characteristics (Bonnet et al., Reference Bonnet, Lana and Guiss1994; Lana and Guiss, Reference Lana and Guiss1991, Reference Lana and Guiss1992; Netto and Lana, Reference Netto and Lana1996, Reference Netto and Lana1997; Rader, Reference Rader1984). Thus, invertebrates inhabiting saltmarsh sediments are generally species that tolerate strong daily and seasonal fluctuations in environmental conditions (Kneib, Reference Kneib1984).
In marine intertidal vegetated areas, such as saltmarshes (e.g. Lana and Guiss, Reference Lana and Guiss1992), the presence of plant cover is one of the major sources of spatial heterogeneity in tropical (Braga et al., Reference Braga, Santos, Filho and Beasley2024; Reis et al., Reference Reis, Krull, Carvalho and Barros2019; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020) and subtropical (Costa and Davis, Reference Costa, Davis and Seeliger1992; Lana et al., Reference Lana, Couto and Almeida1997) areas. The vegetation affects the complexity of the area both on the surface and below the sediment surface. On the surface, the stems and leaves increase substrate availability (Netto and Lana, Reference Netto and Lana1997) and lead to the formation of microhabitats (Nybakken and Bertness, Reference Nybakken, Bertness, Nybakken and Bertness2005; Whitcraft and Levin, Reference Whitcraft and Levin2007), whereas below ground, the roots and rhizomes provide refuge, and physical support to tube builders and affect the vertical physico-chemical characteristics of the sediment (Adam, Reference Adam1990; Long and Mason, Reference Long and Mason1983). Therefore, the patterns of the variations in the spatial distribution (vertical and horizontal) are essential for understanding the ecological patterns of benthic fauna in the environment (Chapman et al., Reference Chapman, Tolhurst, Murphy and Underwood2010; Vieira and Fonseca, Reference Vieira and Fonseca2013).
The cordgrass Spartina alterniflora (Loiseleur, 1807) is the dominant and pioneer species in all saltmarshes along the Brazilian southeastern coast (Lana and Guiss, Reference Lana and Guiss1992), whereas most saltmarsh beds along the Brazilian northern coast are dominated by two species: S. brasiliensis and S. alterniflora. These species usually colonize tidal flats or creeks as narrow discontinuous bands in front of mangroves (Braga et al., Reference Braga, Beasley and Isaac2009, Reference Braga, Monteiro, Rosa Filho and Beasley2011, Reference Braga, Silva, Rosa-Filho and Beasley2013, Reference Braga, Santos, Filho and Beasley2024). However, on the Brazilian Amazon coast, Spartina marshes can be found on both marine and freshwater sites (Menezes et al., Reference Menezes, Berger and Mehlig2008) in several environments such as beaches (exposed and protected), muddy flats, tidal creeks, estuaries, mangroves, and islands of recent sedimentation (Braga et al., Reference Braga, Beasley and Isaac2009, Reference Braga, Monteiro, Rosa Filho and Beasley2011, Reference Braga, Silva, Rosa-Filho and Beasley2013, Reference Braga, Santos, Filho and Beasley2024; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020, Reference Santos, Venekey and Petracco2023).
The Brazilian Amazonian coast has several unique features (e.g. high volumes of river discharge, intense rainfall regime, macro/megatides) compared with other coastal areas in the world (Pereira et al., Reference Pereira, Vila-Concejo, Short, Short and Klein2016; Sousa-Felix et al., Reference Sousa-Felix, Pessoa, Coasta, Jimenez, Pereira, Malvárez and Navas2020; Souza-Filho et al., Reference Souza-Filho, Lessa, Cohen, Costa and Lara2009). These unique features contribute to marked fluctuations in the water salinity and hydrodynamics in coastal environments throughout the year (Pereira et al., Reference Pereira, Vila-Concejo, Short, Short and Klein2016; Rosa Filho et al., Reference Rosa Filho, Pereira, Aviz, Braga, Monteiro, Costa, Asp, Beasley, Lana and Bernardino2018; Souza-Filho et al., Reference Souza-Filho, Lessa, Cohen, Costa and Lara2009). Also, in the tropics, rainfall patterns and associated runoff may differ greatly throughout the year and this provokes extreme temporal variations in the characteristics of Amazonian benthic communities (Braga et al., Reference Braga, Silva, Rosa-Filho and Beasley2013; Rosa Filho et al., Reference Rosa Filho, Almeida and Aviz2009, Reference Rosa Filho, Gomes, Almeida and Silva2011; Santos et al., Reference Santos, Almeida, Aviz and Rosa Filho2021a; Silva et al., Reference Silva, Souza, Souza-Filho and Rosa-Filho2011; Venekey et al., Reference Venekey, Melo and Rosa Filho2019).
The literature on the fauna of saltmarshes is impressive, especially regarding the northern hemisphere where they are widespread (Santos et al., Reference Santos, Rabelo, Beasley and Braga2020). In Brazil, most studies on benthic macrofauna in saltmarshes have been carried out in the southern and southeastern coasts (e.g. Lana and Guiss, Reference Lana and Guiss1991; Netto and Lana, Reference Netto and Lana1996, Reference Netto and Lana1997, Reference NETTO and LANA1999; Pagliosa and Lana, Reference Pagliosa and Lana2005), and despite its singular environmental characteristics and high economic, ecological importance, and their great distribution along the Amazon coast, until today, few studies have been carried out including its diversity and ecology (e.g. Braga et al., Reference Braga, Beasley and Isaac2009, Reference Braga, Monteiro, Rosa Filho and Beasley2011, Reference Braga, Silva, Rosa-Filho and Beasley2013, Reference Braga, Santos, Filho and Beasley2024; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020).
In addition, to our knowledge, there have been no studies that assess the seasonal changes in the vertical distribution of the macrobenthic fauna in Amazon saltmarshes so far. Thus, this study aimed to characterize the vertical distribution pattern of macrobenthic fauna in S. alterniflora marshes and their seasonal changes (rainy season and dry season). Therefore, the present study tested if the structure and vertical distribution of the macrobenthic assemblage in S. alterniflora marshes vary between climatic seasons on the Amazon coast. The results are shown here to provide important ecological data for Amazon saltmarshes and shall serve as a basis for other studies, thus contributing to the conservation of this environment.
Material and methods
Study area
The Algodoal-Maiandeua island is an Environmental Protected Area (EPA) located on the Northern Brazilian Amazon coast (0°34′45″–0°37′30″ S, 47°32′05″–47°34′12″ W) and is surrounded by rivers and estuarine channels on three sides and by the Atlantic Ocean on the western face (Figure 1). The tidal range peaks at 7 m in the equinoctial spring tides (Klein and Short, Reference Klein, Short, Short and Klein2016). The local climate is humid tropical with a mean annual temperature of 27.7 ± 1.1°C. Rainfall varies considerably throughout the year, with a well-defined rainy season from January to July (monthly rainfall over 1,657 mm), and a dry season from August to December (total rainfall of about 490 mm) (Moraes et al., Reference Moraes, Costa, Costa and Costa2005). The trade winds blow from the northeast in the summer and southeast in the winter, generating low to moderate waves which are attenuated across wide intertidal sand and mud flats, with zero wave energy at low tide and only low waves reaching the beaches at high tide (Klein and Short, Reference Klein, Short, Short and Klein2016; Pereira et al., Reference Pereira, Vila-Concejo, Short, Short and Klein2016). Spartina alterniflora marshes are common in the intertidal zone of the island (Braga et al., Reference Braga, Monteiro, Rosa Filho and Beasley2011).
Map showing the location of Algodoal-Maiandeua island with the location of the study Spartina alterniflora saltmarsh during the study seasons (rainy: April; dry: November).
Sampling procedures
Sampling was carried out during low spring tide in April 2008 (Rainy season) and November 2008 (Dry season). Three saltmarshes were randomly selected for sampling and had their areas (m2) individually measured. To avoid border effects, sampling was carried out at least 1 m away from the saltmarsh edge (Santos et al., Reference Santos, Rabelo, Beasley and Braga2020). For the assessment of macrofauna, four samples vertical stratified samples (Upper layer: 0–10 cm and Lower layer: 10–20 cm) were collected haphazardly in each saltmarsh using a cylindrical core with 10 cm diameter and 20 cm length. These samples were washed in a 0.3-mm mesh screen, and the macrofauna was fixed in 4% formalin saline. This mesh ensures more effective retention of juveniles of the benthic macrofauna than the traditional 0.5-mm mesh screen (Bemvenuti, Reference Bemvenuti1994). Simultaneously to the biological sampling, one sediment sample was collected from each sediment layer, and removed from each saltmarsh for granulometric (mean grain size, sorting) analyses and organic matter (OM) content using the same corer sampler using the same corer.
Using a similar sampling design, a single plot (0.25 m2) was randomly selected from each saltmarsh for the sampling of vegetation characteristics. Mean vegetation height (cm) was obtained by measuring all stems, and vegetation density was obtained by counting the number of saltmarsh stems inside each plot (Braga et al., Reference Braga, Monteiro, Rosa Filho and Beasley2011). The area in each plot was dug to a depth of 20 cm and all plant material (above and below ground) was removed to estimate vegetation H2O content and OM. These samples were kept cool in the field and later frozen in the laboratory to prevent decomposition and loss of biomass until final processing in the laboratory.
Laboratory procedures
The biological samples were examined using a stereoscopic microscope, and the organisms observed were counted and identified to the lowest possible taxonomic level. A granulometric analysis was carried out by sieving coarse sediments and pipetting fine sediments, as proposed by Suguio (Reference Suguio1973). Textural parameters (mean grain size, sorting, sand, and gravel) were calculated using the equations by Folk and Ward (Reference Folk and Ward1957). Grain sizes were determined by sieving the sediment through an automatic shaker and classifying it according to the Wentworth scale (Buchanan, Reference Buchanan, Holme and McIntyre1984). Sediment H2O content was initially estimated as water loss after drying the sediment at 60°C for 24 h. Dried samples were combusted at 550°C for 4 h to determine sediment OM content (Dean, Reference Dean1974).
For vegetation, the aerial parts (stem, leaves, flowers, shoots) and underground parts (roots) were separated to determine the OM and H2O contents. Saltmarsh H2O content was estimated as water loss after drying the sediment at 90°C until constant weight. The saltmarsh OM content was estimated by burning 2 g of dry vegetation at 500°C for 4 h (Braga et al., Reference Braga, Monteiro, Rosa Filho and Beasley2011).
Statistical analysis
We calculated the richness (total taxa) and density (ind/m2) of each biological sample. To test the assumption of homogeneity of variances, Kolmogorov–Smirnov and the Levene tests were applied, respectively. Where necessary, data were (fourth root) transformed. Differences in the biological descriptors and sediment (mean grain size, sorting, % sand and % fines, soil temperature, OM, and H2O content) and vegetation data (area, OM, and H2O content, density, and height) between seasons (rainy and dry) and sediment layers (upper: 0–10 cm and lower: 10–20 cm), were analyzed using an analysis of variance (two-way ANOVA). When ANOVA detected a significant difference, Tukey’s a posteriori test was applied to identify significant pairwise differences.
To evaluate the effects of saltmarshes on macrofauna and validate our a priori clustering (rainy and dry seasons; upper and lower sedimentary layers), a Principal Coordinate Analysis (PCO) was run on a Bray–Curtis similarity matrix of the fourth root transformed species abundance data. To identify the species that characterized each area and layer, species that were correlated (Spearman’s coefficient) with one of the first two axes by more than 60% were plotted in each PCO. At the same time, the same density matrices used for the PCO were analyzed using a two-way Permutational ANOVA (PERMANOVA) designed with the same layout as the ANOVA. The P-values were corrected through Monte Carlo random draws from the asymptotic permutation distribution, due to the number of the possible permutations not being large (Anderson and Robinson, Reference Anderson and Robinson2003).
The contribution of each taxon to the dissimilarity found between groups was evaluated using the SIMPER (similarity percentage) routine. For linking the macrobenthic descriptors with the sediment and saltmarsh characteristics a distance-based linear model (DistLM; Anderson, Reference Anderson2001) was performed. This technique analyzes and models the relationship between a multivariate data cloud, as described by a resemblance matrix and predictor variables. Resemblance matrices were calculated using Euclidean distance (log(x +1) transformed data). The best models in DistLM were chosen using a forward routine with 9999 permutations based on AIC selection criteria (Anderson et al., 2008). A 5% significance level was considered for all analyses.
Results
Environmental parameters
Overall, salinity varied between seasons, ranging from 9.16 ± 10.06 ‰ in the rainy season, to 13.16 ± 14.45 ‰ in the dry season. Higher precipitation was found in the rainy season (428.8 mm) while no rain was registered in the dry season (0 mm). The wind speed showed higher values in the dry period (0.72 ± 0.58 m/s) and lower values in the rainy period (0.32 ± 0.041 m/s). The wind direction varied during the study, where they were predominantly from the northeast in the rainy period and the east in the dry period (Supplementary material 1).
The mean grain size varied from silt to medium sand, and according to the sorting coefficient, samples ranged from very well-sorted to moderated sorted (Table 1). Significant differences were found in mean grain size between seasons and sediment layers, however, no significant differences were found in the interaction season x sediment layer (Table 2). Overall, the rainy season was characterized by silt to fine sand and very well-sorted sediments at all depths. On the other hand, the dry season was characterized by medium sand and moderate sorted sediments at all depths. Sediment OM and H2O content varied significantly between seasons and sediment layers (Table 2), with higher values found in the rainy season and in the lower sediment layer of both seasons (Table 1).
Environmental and sedimentary characteristics between seasons (rainy and dry) and sediment layers (upper: 0–10 cm and lower: 10–20 cm) in Spartina alterniflora saltmarshes of Algodoal-Maiandeua island
FS = fine sand; MS = medium sand; VWSort = very well-sorted; MSort = moderate sorted.
Summary of ANOVA results for comparisons of sediment environmental parameters of macrobenthic fauna in Spartina alterniflora saltmarshes of Algodoal-Maiandeua island
df = degrees of freedom.
** Significant differences (p < 0.05).
Spartina alterniflora marsh characteristics
The mean Spartina area varied from 740.53 ± 444.77 m2 in the rainy season to in the dry season to 1073.82 ± 468.84 m2 (Figure 2A); however, no significant differences were found among seasons (F (1.46) = 0.23, p = 0.63). Similarly, no significant differences (F (1.44) = 92.03, p = 0.51) were found in Spartina height among seasons (Figure 2C); however, higher values were found in the dry season compared to the rainy season (40.8 ± 16.19 ind/50 cm2 and 35.04 ± 16.67 cm2, respectively). Significant differences were found only in Spartina density (F (1.44) = 9275.03, p = 0.00), where higher values were found in the dry season (242.66 ± 37.22 ind/50 cm2) than in the rainy season (46.66 ± 5.03 ind/50 cm2) (Figure 2B).
Mean values (± SD) of the vegetation variables (A–D) between seasons (rainy and dry) and sedimentary layers (upper: 0–10 cm and lower: 10–20 cm) from Spartina alterniflora saltmarshes of Algodoal-Maiandeua island. Different letters indicate significant differences (Tukey’s test; p < 0.05); uppercase letters (A ≠ B) indicate differences among seasons and lowercase letters (A ≠ B) indicate differences between sedimentary layers.
The Spartina OM and H2O content varied significantly among seasons (F (1.44) = 15,004.16, p = 0.001; F (1.44) = 67.35, p = 0.001, respectively) with higher values found in rainy season (Figure 2D). However, concerning sedimentary layers, significant differences in OM and H2O content were found only in the dry season (F (1.44) = 0.16, p > 0.05; F (1.44) = 0.01, p > 0.05, respectively), with higher values found in the lower sedimentary layer (Figure 2D).
Macrobenthic assemblage
A total of 38 macrobenthic taxa were recorded in this study, of which 9 taxa were exclusively found in the rainy season and 11 were exclusively found in the dry season (Supplementary material 2). Overall, Annelida (16 taxa) and Arthropoda (11 taxa) comprised the phylum with the highest number of taxa. In addition, Annelida was the phylum with the highest density in the rainy season, while Arthropoda was the phylum with the highest density in the dry season (Figure 3A). Concerning sediment layers, Annelida density increased from the upper to the lower sediment layer while Arthropoda density decreased towards the lower sediment layer in both seasons. Furthermore, higher mollusk density was recorded at the upper layer in both seasons (Figure 3A).
Relative abundance (%) of taxonomic groups (A), trophic groups (B), mean density (ind./m2 ± standard error) (C) and richness (number of taxa) (D) of the macrobenthic fauna between seasons (rainy and dry) and sediment layers (upper: 0–10 cm and lower: 10–20 cm) in Spartina alterniflora saltmarshes of Algodoal-Maiandeua island. Different letters indicate significant differences (Tukey’s test; p < 0.05), uppercase letters (A ≠ B) indicate differences among seasons and lowercase letters (A ≠ B) indicate differences between sedimentary layers.
The polychaetes Laeonereis culveri (527.4 ± 404.7 ind./m2), Neanthes succinea (232.06 ± 87.9 ind./m2), and Capitella capitata (147.6 ± 76.06 ind./m2) reached their highest densities at the upper layer of the rainy season. Conversely, C. capitata (94.93 ± 84.08 ind./m2), L. culveri (63.2 ± 42.6 ind./m2), and the oligochaete Tubificidade sp. (42.1 ± 28.4 ind./m2) reached their highest density at the lower layer. In the dry season, the tanaidacea Halmyrapseudes spaansi (28,681.43 ± 10,232.57 ind./m2) and the polychaete C. capitata (31,96.2 ± 1056.4 ind/m2) reached their highest densities at the upper layer, although they were also the most abundant at the lower layer (Supplementary material 2).
Regarding the feeding mode, deposit feeders were the dominant group in the rainy season, while predators were the dominant trophic group in the dry season (Figure 3B). In addition, a greater diversity of functional groups was recorded during the dry season. Concerning sediment layers, suspensive feeders decreased from the upper to the lower sediment layer. Conversely, deposit feeders and detritivores decreased towards the lower sediment layer in the rainy season. On another hand, a marked increase in deposit feeders and a decrease in suspension feeders towards the lower sediment layer were observed in the dry season (Figure 3B). ANOVA results showed significant differences in density and richness between seasons and sediment layers (Table 3). Overall, higher density and richness were found in the dry season. Concerning sediment layers, the highest mean values of both variables and in both seasons occurred at the upper layer (Figure 3C and D).
Summary of ANOVA results for comparisons of community descriptors of macrobenthic fauna in Spartina alterniflora saltmarshes of Algodoal-Maiandeua island
df = degrees of freedom.
** Significant differences (p < 0.05).
The PCO plot distinguished macrofauna samples between study seasons and sediment layers (Figure 4A). Axis 1 explained 34.1% of the variation in the data and was responsible for separating seasons and sediment layers (Figure 4A). In the rainy season (Figure 4B), axis 1 explained 33.3% of the variation in the data and was responsible for separating the sedimentary layers. The species most correlated with this axis were more abundant in the upper sedimentary layer, including the polychaetes C. capitata, N. simoni, N. succinea, and S. grubii and the bivalve C. fuminensis. Similarly, in the dry season, axis 1 explained 47.6% of the variation in the data and was responsible for separating the sedimentary layers with C. capitata, N. succinea, and S. grubii and the crustacean H. spansii were more abundant in the upper sedimentary layer (Figure 4C).
Results of the principal coordinates ordination (PCO) of macrobenthic fauna samples (A) collected in different seasons (B: rainy and C: dry) and at different sediment layers (upper: 0–10 cm; lower: 10–20 cm) in Spartina alterniflora saltmarshes of Algodoal-Maiandeua island. The vectors represent species that are correlated by more than 50% (based on the Spearman’s correlation coefficient) with one of the first two PCO axes.
The PERMANOVA analysis showed significant differences between seasons and sediment layers (Table 4). SIMPER analysis indicated a mean dissimilarity of more than 85% between seasons and sedimentary layers. The crustacean Halmyrapseudes spaansi and the polychaete Capitella capitata were the species that contributed most for the dissimilarity between seasons and sedimentary layers, being were more frequent and abundant in the dry season and at the upper layer (Supplementary material 1). Regarding sediment layers within each season, most predominant species found in rainy season (e.g. Neanthes succinea, Laeonereis culveri, and C. capitata) were more frequent and abundant at the upper layer. In dry season, conversely, three species (H. spaansi, C. capitata, and N. succinea) were responsible for more than 50% of the dissimilarity between sediment layers, due to their increased frequency and density at the upper layer (Supplementary material 3).
PERMANOVA results for comparisons of community descriptors of macrobenthic fauna in Spartina alterniflora saltmarshes of Algodoal-Maiandeua island
df = degrees of freedom. MS = mean squares.
** Significant differences (p < 0.05).
The best DistLM explained 73.6% of richness and 61.2% of density variation of macrobenthic assemblage in the study. Salinity, sediment OM, saltmarsh OM, and saltmarsh density were the principal environmental variables correlated with both descriptors (Table 5). In the rainy season, sediment and saltmarsh OM and H2O content and variables related to sediment characteristics were principally related to density and richness. In the dry season, sediment and saltmarsh OM, saltmarsh density, and granulometric variables (grain size, % fines) were related to macrobenthic density. On the other hand, salinity was the main variable related to richness (Table 5).
Best distance-based linear models (DistLM) fitted for macrobenthic fauna descriptors against environmental variables in the Spartina alterniflora saltmarshes of Algodoal-Maiandeua island
Values in brackets: proportion of variability explained by each variable.
Discussion
The Brazilian Amazon coastal environments are extremely dynamic due to their natural characteristics (i.e. hydrodynamic conditions, semidiurnal macrotidal regimes, freshwater inputs, variations in salinity and rainfall, wave and wind regime), which subjects saltmarshes to a wide range of environmental factors (Braga et al., Reference Braga, Silva, Rosa-Filho and Beasley2013; Dittmar and Lara, Reference Dittmar and Lara2001; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020, Reference Santos, Almeida, Aviz and Rosa Filho2021a; Souza-Filho et al., Reference Souza-Filho, Lessa, Cohen, Costa and Lara2009). These include sediment composition, OM, flow regime, salinity, and O2 within porewaters (Evin and Talley, Reference Evin, Talley, Weinstein and Kreeger2002). A variety of abiotic and anthropogenic factors has a major influence on the composition and distribution of invertebrates in these environments (Braga et al., Reference Braga, Silva, Rosa-Filho and Beasley2013; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020, Reference Santos, Petracco and Venekey2021b).
Overall, in the present study, taller and denser vegetation was observed in the dry season, where salinity was higher. It is well-known that fluctuations in salinity, degree of inundation, nutrient availability, and temperature are responsible for variations in productivity and growth in saltmarshes (Levin and Talley, Reference Levin, Talley, Weinstein and Kreeger2000). In the Amazon coast, differences in salinity are associated with fluctuations in hydrodynamic conditions, and fluvial discharges that vary according to the periodicity of rainfall and catchment size (Jaeger and Nittrouer, Reference Jaeger and Nittrouer1995; Souza-Filho et al., Reference Souza-Filho, Lessa, Cohen, Costa and Lara2009). Saltmarshes are halophytes that tolerate fluctuations in salinity and greater plant height, density, and area have been associated with higher salinity (Pennings and Bertness, Reference Pennings, Bertness, Bertness, Gaines and Hay2001). In addition, previous studies along the Amazon coast showed that saltmarshes in this region appear to be no exception to this rule (Braga et al., Reference Braga, Beasley and Isaac2009, Reference Braga, Silva, Rosa-Filho and Beasley2013; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020).
Even with lower height and density, when compared to the dry season, we observed higher OM in the rainy season. This higher sediment OM might be related to the environmental conditions on the Amazonian coast. As explained above, the coastal areas are very dynamic and temporally variable (Souza-Filho et al., Reference Souza-Filho, Lessa, Cohen, Costa and Lara2009). In the rainy season, with higher riverine discharge, more allochthonous OM (dissolved and particulate) is transported to the coastal environments, increasing the availability of OM. In addition, on the Amazonian coast, more intense easterly trade winds are typically found during the drier months, generating higher and more frequent waves, which resuspend more bottom sediments (Pereira et al., Reference Pereira, Vila-Concejo and Short2013). The influence of strong and more frequent waves and turbulence may prevent the deposition of fine sediments and OM in the dry season (Santos et al., Reference Santos, Almeida, Aviz and Rosa Filho2021a). Conversely, during the rainy season, winds are weaker, the period and height of the waves decrease and sediment discharge increases, thus increasing the availability and deposition of fine sediments (Pereira et al., Reference Pereira, Vila-Concejo, Short, Short and Klein2016; Souza-Filho et al., Reference Souza-Filho, Lessa, Cohen, Costa and Lara2009). As the accumulation of OM (derived from the decomposition of roots and leaves, as well as substrate humification) occurs over time (Ferreira, Reference Ferreira2008), and in seasons with high hydrodynamics, the influence of currents, waves, and turbulence may prevent the deposition of marsh OM in the sediment for a long time.
The macrobenthic assemblage in the present study was predominantly composed of polychaete worms and typically estuarine and marine taxa which are the same composition found in other studies in Amazon saltmarshes (e.g. Braga et al., Reference Braga, Beasley and Isaac2009, Reference Braga, Monteiro, Rosa Filho and Beasley2011, Reference Braga, Silva, Rosa-Filho and Beasley2013, Reference Braga, Santos, Filho and Beasley2024; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020) as well as in other intertidal habitats of the Amazon coast (Beasley et al., Reference Beasley, Fernandes, Figueira, Sampaio, Melo, Barros, Saint-Paul and Schneider2010; Cardoso et al., Reference Cardoso, Petracco, Santos, Venekey and Aviz2023; Rosa Filho et al., Reference Rosa Filho, Almeida and Aviz2009, Reference Rosa Filho, Gomes, Almeida and Silva2011; Santos et al., Reference Santos, Almeida, Aviz and Rosa Filho2021a; Santos and Aviz, Reference Santos and Aviz2018, Reference Santos and Aviz2020; Santos et al., Reference Santos, Petracco and Venekey2022, Reference Santos, Venekey and Petracco2023, Reference Santos, Aviz and Rosa Filho2024a) and muddy environments (Rosa-Filho et al., Reference Rosa-Filho, Busman, Viana, Gregório and Oliveira2006; Santos et al., Reference Santos, Aviz and Rosa Filho2024b) and on the consolidated substrate (Morais and Lee, Reference Morais and Lee2013). Overall, annelids, mollusks, and crustaceans tend to dominate macrofaunal assemblages in Brazilian saltmarshes (Checon et al., Reference Checon, Corte, Cunha, Esmaeili, Fonseca, Amaral, Schaeffer-Novelli, Abuchahla and Cintron-Molero2023). Similar dominant taxa occurred in the present study; in general, saltmarsh fauna have low diversity (Adam, Reference Adam1990) but are very similar among different geographic locations due to ecological equivalence (Nybakken and Bertness, Reference Nybakken, Bertness, Nybakken and Bertness2005).
Overall, Annelida was the most dominant phylum in both seasons and at all sediment depths. The dominance of Annelida might be related to the shape of these organisms, which facilitates burrowing activities, provides high tolerance to environmental stress (Bouwman, Reference Bouwman1983; Rosa Filho et al., Reference Rosa Filho, Almeida and Aviz2009, Reference Rosa Filho, Gomes, Almeida and Silva2011), and a wider range of infaunal niches provided by Spartina roots and rhizomes (Santos et al., Reference Santos, Rabelo, Beasley and Braga2020). These niches in vegetated habitats provide refuges, detritus, and several types of infaunal prey (Attolini et al., Reference Attolini, Flynn and Tararam1997; Flynn et al., Reference Flynn, Wakabara and Tararam1998; Lana et al., Reference Lana, Guiss and Disaró1991). In addition, the high diversity of feeding habits, allows the annelids to use all available food resources (Jumars et al., Reference Jumars, Dorgan and Lindsay2015) in the saltmarshes.
In the present study, differences in the trophic groups were observed between seasons and sedimentary layers, with a higher diversity of trophic groups found in the dry season and upper sedimentary layer. This distribution of trophic groups in the study area can be explained by the sediment texture, and OM disponibility. In the rainy season, deposit feeders were more abundant in both sedimentary layers. On the other hand, in the dry season, predators, suspension feeders, and deposit feeders were more abundant. Overall, fine-organically rich muds tend to contain more burrowing deposit feeders, whereas more sandy sediments and dynamic environmental conditions typically harbour more mobile animals, predators, omnivores, and suspension feeders (Pearson and Rosenberg, Reference Pearson and Rosenberg1978).
Seasonally, higher density and richness were found in the dry season, a characteristic that has been widely reported in Amazonian coastal areas (e.g. Aviz et al., Reference Aviz, Silva and Rosa Filho2019; Beasley et al., Reference Beasley, Fernandes, Figueira, Sampaio, Melo, Barros, Saint-Paul and Schneider2010; Braga et al., Reference Braga, Silva, Rosa-Filho and Beasley2013; Rosa Filho et al., Reference Rosa Filho, Almeida and Aviz2009; Santos et al., Reference Santos, Almeida, Aviz and Rosa Filho2021a; Santos and Aviz, Reference Santos and Aviz2018; Silva et al., Reference Silva, Souza, Souza-Filho and Rosa-Filho2011). In contrast to saltmarshes from temperate regions, where changes in the structure of benthic communities are predominantly caused by modifications in temperature and photoperiod (Levin and Talley, Reference Levin, Talley, Weinstein and Kreeger2000), salinity is primarily responsible for temporal variations in density and richness in the Amazon coastal zone (Rosa Filho et al., Reference Rosa Filho, Almeida and Aviz2009; Santos et al., Reference Santos, Almeida, Aviz and Rosa Filho2021a). Changes in salinity in tropical coastal environments alter the structure of macrobenthic communities (Kinne, Reference Kinne and Kinne1971), as the dynamics of these ecosystems are controlled by variations in rainfall, hydrology, morphology, and the physicochemical conditions of the marine and freshwater environments (Day Junior et al., Reference Day Junior, Crump, Kemp and Yáñes-Arancibia2013). Also, high pluviosity and freshwater input by river discharge sharply reduce salinity, leading to the restriction or exclusion of species that are exclusively marine or poorly adapted to low salinity (Kinne, Reference Kinne and Kinne1971).
Overall, we found the macrobenthic fauna distributed in both sediment depths; however, higher density and richness occurred in the first 10 cm (upper layer) in both seasons. The vertical distribution in saltmarshes appears to be facilitated by the rhizosphere since the root structure increases oxygenation at deeper layers (Holmer et al., Reference Holmer, Gribsholt and Kristensen2002) leading to an even distribution of physical and biological parameters from the surface to lower layers (Pennings and Bertness, Reference Pennings, Bertness, Bertness, Gaines and Hay2001). Also, the high density and richness found in the upper layer of our study, result agree with most studies of saltmarshes, which show that organisms tend to concentrate in the top 10 cm (e.g. Netto and Lana, Reference Netto and Lana1997; Santos et al., Reference Santos, Rabelo, Beasley and Braga2020). The stems and leaves increase substrate availability (Netto and Lana, Reference Netto and Lana1997) and lead to greater food availability near the sediment surface.
In addition, although the rhizosphere may facilitate the vertical distribution of macrobenthic fauna in saltmarshes, inhibition of fauna by S. alterniflora roots may also occur since roots can occupy a significant fraction of the space in marsh sediments (Levin and Talley, Reference Levin, Talley, Weinstein and Kreeger2000). Therefore, denser S. alterniflora roots may hinder the infaunal burrowing and feeding activities of several invertebrates (Bertness, Reference Bertness1985; Brenchley, Reference Brenchley1982; Ringold, Reference Ringold1979), resulting in species migration from deeper sediment layers to more surface layers, in search of space and food. We can see this pattern during the dry season, where we observed higher density of Spartina and the organisms were concentrated almost exclusively in the upper layer, with few organisms in the lower layer. In a previous study, Santos et al. (Reference Santos, Rabelo, Beasley and Braga2020) found the fauna was restricted to the first 10 cm, and no organisms were found in lower depths in dense saltmarshes in the Amazon coast. Therefore, we suggest that the vertical distribution of the macrobenthic fauna may depend on the vegetation density in Amazon saltmarshes. In general, older marshes have well developed vegetation in terms of height and density (Osgood et al., Reference Osgood, Santos and Zieman1995), and a more complex root system (Levin and Talley, Reference Levin, Talley, Weinstein and Kreeger2000). These characteristics might prevent the macrobenthic fauna, especially the small infauna, from penetrate into deeper sediment layers.
Conclusion
This study provides novel insights into the distribution patterns of macrobenthic fauna in tropical macrotidal saltmarshes. Our results show that seasonal changes in the environmental characteristics of the regions induced marked differences in the density and richness of the macrobenthic community. In general, our results showed that higher densities and richness were found at near-surface layers (0–10 cm) in both seasons. Our results showed that salinity, sediment OM, vegetation density, and grain size were the most important environmental factors in structuring the macrobenthic community abundance and richness. Therefore, the tested hypothesis that the structure and vertical distribution of the macrobenthic community vary between climatic seasons was confirmed.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315425100088.
Acknowledgements
Special thanks to the students for their help in both the field and in the laboratory.
Authors’ contributions
T.M.T. Santos: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Data curation, Writing – original draft & editing. M.V.B. Silva: Conceptualization, Methodology, Resources, Validation, Formal analysis, Investigation, Data curation. C.F. Braga: Conceptualization, Methodology, Resources, Supervision, Funding acquisition.
Funding
This study was financed by the Brazilian National Research Council (CNPq) (Edital MCT/CNPq 15/2007-Universal Process No. 472234/2007-2) and the Instituto de Educação do Brasil (IEB).
Competing interests
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.
