Drought effects on tropical estuarine benthic assemblages in Eastern Brazil

Journal Pre-proof Drought effects on tropical estuarine benthic assemblages in Eastern Brazil

Luiz Eduardo de Oliveira Gomes, Angelo Fraga Bernardino PII:

S0048-9697(19)35484-1

DOI:

https://doi.org/10.1016/j.scitotenv.2019.135490

Reference:

STOTEN 135490

To appear in:

Science of the Total Environment

Received date:

20 August 2019

Revised date:

7 November 2019

Accepted date:

10 November 2019

Please cite this article as: L.E. de Oliveira Gomes and A.F. Bernardino, Drought effects on tropical estuarine benthic assemblages in Eastern Brazil, Science of the Total Environment (2019), https://doi.org/10.1016/j.scitotenv.2019.135490

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

© 2019 Published by Elsevier.

Journal Pre-proof

Drought effects on tropical estuarine benthic assemblages in Eastern Brazil Luiz Eduardo de Oliveira Gomes*, Angelo Fraga Bernardino

Grupo de Ecologia Bêntica, Departamento de Oceanografia and Ecologia, Universidade Federal do Espírito Santo, Av. Fernando Ferrari, 514, Goiabeiras, Vitória, ES, 29055-60

of

* Corresponding author: [email protected] (L.E.O. Gomes)

ro

Abstract

Climate change will increase the frequency and intensity of extreme weather events with

-p

potential effects in coastal and estuarine ecosystems. During drought periods, higher salinity and temperature can directly impact estuarine benthic assemblages through physiological stress and

re

alteration of sedimentary habitats, but these effects are poorly evaluated to date. Here we report a 14-month monitoring of benthic assemblages in a tropical estuary in the Eastern Brazil Marine

lP

Ecoregion during the severe drought period of 2015/2016. The drought in Eastern Brazil resulted in a decrease of estuarine mean sediment particle size and concurrent changes in

na

macrofaunal benthic assemblages during the driest months. We also observed a 3-fold reduction on macrofaunal abundance with dominance of surface-dwelling Magelonid, Sternaspid, Capitellid and Oligochaeta annelids. The changes in macrofaunal structure during the severe

Jo ur

drought also decreased the community bioturbation potential (BPc) by 5-fold, if compared to pre-drought periods. We argue that the projected increases in the frequency and severity of climatic events, such as observed during severe droughts worldwide, will greatly change the benthic fauna and their ecological functions in tropical estuarine ecosystems. Keywords: Climate change, Drought, Estuaries, Macrofauna, Bioturbation

1. Introduction Estuaries are transition ecosystems between continents and the sea varying in shape, size, hydrography, salinity, tidal characteristics and sedimentation (Kennish, 2002; McLusky and Elliott, 2004). Estuaries provide key ecological services and social benefits such as sediment burial, organic degradation, and provide habitat and food for a range of marine and estuarine species. Despite the importance of the estuarine services, 1

Journal Pre-proof these ecosystems are largely influenced by human activities, such as coastal development, pollution and alteration of hydrological regimes (Kennish, 2002; Worm et al., 2006; MacKay et al., 2010). In recent years, climate change has become an increasing threat to estuarine conservation with potential losses to the estuaries’ ecological and socioeconomic services (Worm et al., 2006; Elliott and Whitfield, 2011). Climate change is increasing the average global temperature and changing precipitation patterns (IPCC, 2001; Doney et al., 2012; Cook et al., 2014). Flood and drought events will likely increase in frequency and magnitude in the next few centuries and can change estuarine salinity gradients and sediment habitats (IPCC, 2001; Day et

of

al., 2008; García-Rodriguez et al., 2013). During El Nino events drought periods (lower precipitation) are more intense and increase the duration of heatwaves and associated

ro

impacts such as lower surface primary production and impacts on biodiversity (Pollack

-p

et al., 2011; Rodrigues et al., 2019). Furthermore, the increase in El Niño frequency (dryer periods) and La Niña (humid periods) in the South Atlantic influence the

re

freshwater supply, with episodic hypersaline or flood conditions, leading to changes in benthic assemblages (Drexler and Ewel, 2001; Hastie and Smith, 2006; Pillay and

lP

Perissinotto, 2008; MacKay et al., 2010; Pollack et al., 2011; Rodrigues et al., 2019). Changes in estuarine salinity and warming temperatures can impact benthic

na

assemblages through physiological stress, changing their composition and behavior (García-Rodriguez et al., 2013; Dittmann et al., 2015). Lower freshwater input to

Jo ur

estuaries can also alter sedimentary habitats (e.g. particle size and porosity) with effects on benthic macrofaunal structure (Gray and Elliott, 2009; Pratt et al., 2014). Drought effects have been associated with a decrease in benthic macrofaunal abundance, species richness and biomass in estuaries, with additional changes in species composition towards tolerant and opportunist taxa (Dolbeth et al., 2011; Pillay and Perissinotto, 2008; MacKay et al., 2010; Pollack et al., 2011). These effects may impact macrofaunal ecological functions including sediment bioturbation and biogeochemical cycling at the water-sediment interface (Mermillod-Blondin, 2011; Laverock et al., 2011; Braeckman et al., 2014; Kristensen et al., 2014). Community bioturbation potential (BPc) estimates the average distance travelled by particles through a benthic assemblage from bioturbation (Queirós et al., 2015). BPc can be assessed by following changes in benthic assemblage structure and their predicted ecological behavior, including their mobility capacity (ranging from fixed in tubes to free movement), and the sediment reworking potential (from bioturbation at the sediment-water interface to transferring 2

Journal Pre-proof sediment at depth to the surface). Therefore, BPc allows assessments of the relative assemblage bioturbation intensity and may provide an ecological index for benthic ecosystem function that is increasingly being used in marine ecosystems in spatial and temporal analyses (Solan et al., 2004; Queirós et al., 2013, 2015). Here we report results from 14 months of ecological monitoring in a tropical estuary in the Eastern Brazilian Marine Ecoregion during a severe drought period that was likely associated with the 2015-2016 El Niño. We monitored estuarine water properties and tidal flat benthic assemblages in two estuarine sites to identify temporal changes in estuarine sediments and benthic assemblages in response to the drought

of

period. We hypothesized that benthic assemblages and their bioturbation potential would be impacted by the drought as a result of changes in sediment particle size,

-p

2.1. Study area and sampling design

re

2. Materials and Methods

ro

higher salinity and higher temperatures.

lP

This study was conducted in the Piraquê Açú-Mirím estuary (PAM, 17º58’S; 40º00’W), within the Eastern Brazil Marine Ecoregion (Figure 1). The PAM estuary has

na

a semi-diurnal microtidal regime (<2m) and a Y-shape morphology; it comprises approximately 12 Km2 of preserved mangroves, dominated by Rhizophora mangle,

Jo ur

followed by Avicennia schaueriana and Laguncularia racemose (Servino et al., 2018). Coastal development led to mangrove removal in some areas along the estuarine margin for agriculture and construction of houses and piers for fishermen to access the river (Bernardino et al., 2018a). The PAM is a riverine estuary with depths of 4 to 16m and located on a wave dominated coast in Eastern Brazil (Lana and Bernardino, 2018). It is one of the most pristine estuaries on the Eastern coast with limited land use and pollution, and is included in a municipal protection area (Bernardino et al., 2018b; Hadlich et al., 2018; Varzim et al., 2019). The PAM estuary is also strongly stratified and dependent on continental freshwater influx (Bissoli and Bernardino, 2018), making it reasonable model ecosystems on the study of climate change scenarios. The Eastern Brazil has two well-defined seasons, the dry season (April to September) with precipitation volumes of 53.0 to 97.0 mm.mo-1 and the wet season (October to March) with precipitation of 101.1 to 211.5 mm.mo-1 and annual temperatures from 24 to 26 °C (Bernardino et al., 2015). 3

Journal Pre-proof Over 14 months, we tested spatial and temporal changes in benthic assemblages and measured sediment variables (total mud content, total organic content, carbonate, chlorophyll-a and phaeopigments) within two sectors (A=lower estuary and B=upper estuary), both located within a polyhaline salinity gradient. Two spatial scales were tested, sectors (A vs B, 1000’s of meters) and sites (S1 and S2, two per sector, 100’s of meters; Figure 1). Each site (S1 and S2) was subdivided into two sampling plots along the intertidal mudflat, 10 m apart and at least 1 m from the nearby mangrove forests. Monthly sampling occurred from May of 2015 to June of 2016 during low spring tides. Monthly samples were grouped for analysis into three periods: Dry 2015 (May to

of

September of 2015; N=5 months), Wet 2015 (October of 2015 to March of 2016; N=6 months) and Dry 2016 (April to June of 2016; N=3 months).

ro

In each plot (n=2 per site), three replicate faunal samples and one sediment

-p

sample (0.008 m²) were collected for analysis of grain size, total organic content and carbonate. Surface sediment (15 g, 0-3 cm) was sampled for analysis of chlorophyll-a

re

and phaeopigments. Water pH, total dissolved solids (TDS, ppt) and dissolved oxygen (mg.L, DO) were measured in situ with a HANNA multiparameter at each site at the

lP

time of sampling. Semi-continuous monitoring of water conductivity and temperature were performed using a HOBO data-logger (U24-002-C, collection frequency of 2

na

minutes), deployed for periods of 5 to 24 days at 1 meter above the estuarine bottom (~3 meters deep, low tide). For sectors A and B, 33 days and 40 days were monitored,

Jo ur

respectively. The data-logger allowed monitoring of salinity oscillations across spring/neap tides during the Dry 2015 (spring tides), Wet 2015 and Dry 2016 (spring and neap).

2.2. Standardized Precipitation Index (SPI; Climatic drought index) Drought conditions were assessed by the Standardized Precipitation Index (SPI) using precipitation data from 1948-2019. The SPI quantifies the precipitation deficit, useful to identify and monitor climatic droughts by categories (ranging from extreme wetness ≥2 SPI to extreme dryness ≤-2 SPI (Supplemental table S1, S2; McKee et al., 1993). The SPI was assessed through the precipitation patterns using data from meteorological stations located in the nearest areas of the PAM estuary from the Brazil National Weather Agency (total daily precipitation; ANA, 2017, stations 1940002, 1940021 and 2549007; Servino et al., 2018). 4

Journal Pre-proof

2.3. Laboratory analysis Sediment grain size was determined by wet sieving and reported as mud sediment fraction (silt and clay; i.e., grain sizes >2 mm, 2-1 mm, 1-0.5 mm, 0.5-0.25 mm, 0.25-0.125 mm, 0.125-0.063 mm and <0.063 mm). The total organic content was determined by drying the samples at 60 °C for 48 h, with subsequent ignition for 4 h at 450 °C. Sediment carbonate content was determined by the addition of hydrochloric acid (10 %, 2 mL) until effervescence ceased, dried at 60 °C for 48 h and weighed.

of

Chlorophyll-a and phaeopigments were analyzed according to Lorenzen (1967) and measured with spectrophotometry (absorbance read at 430 and 665 nm) after extraction

-p

acidification with 0.1 NHCl (Lorenzen, 1967).

ro

with 100 % acetone (Quintana et al., 2015). Phaeopigments were determined after Macrofaunal samples were sieved in the field (500 μm) and preserved in 70 %

re

ethanol until sorting. In the laboratory, all organisms were sorted and identified to family or lower taxonomic levels. After sorting, the total biomass of the macrofauna

lP

(wet weight) was determined using a balance with 0.001 g precision. The macrofauna functional groups (deposit feeders, OCO - omnivores, carnivores and others -, filter

na

feeders, suspension feeders and detritivore feeders) were defined according to Magalhães and Barros (2011) and Jumars et al., (2015). The bioturbation potential of

Jo ur

each taxa (BPi), here calculated from the relative abundance of the dominant taxa, included Magelonidae, Sternaspidae, Capitellidae, Goniadidae, Paraonidae and Oligochaeta (Bpi; ~90 % relative abundance; Solan et al., 2004). The BPc was calculated from the sum of the bioturbation potential of the dominant taxa; just the dominant taxa were used because the weight of the remaining taxa was not sufficient to perform the calculations, wet weight <0.001 g. Mobility information (Mi) and reworking (Ri) of the fauna were based on Queirós et al. (2013). In general, the closest taxonomic level was applied if there were no species-specific data available. 2.4. Statistical analyzes Water temperature and salinity were examined for relationships to season (Dry 2015, Wet 2015 and Dry 2016) and for spatial variations (sectors A and B) using a twoway permutational multivariate analysis of variance (PERMANOVA) with 9999 5

Journal Pre-proof permutations of residuals under a reduced model (Clarke and Gorley, 2006; Anderson et al., 2008). The data was normalized before applying a Euclidean distance dissimilarity resemblance matrix. However, water pH, total dissolved solids (TDS, ppt) and dissolved oxygen (mg.L, DO) were used to characterize the water column, being not statistically tested due the small dataset. Changes in sediment parameters (total mud content, total organic content, carbonate, chlorophyll-a and phaeopigments) and biological variables (macrofaunal composition, total macrofaunal density, dominant taxa density - Magelonid, Sternaspid, Capitellid, Paraonid, Goniadid and Oligoqueta -, total biomass, species richness,

of

Shannon H', Pielou J’, functional groups and bioturbation potential) were nested in a three-way PERMANOVA across seasons, sectors and sites (with the latter nested within

ro

sectors, four levels). Once the environmental variables of water were not tested for site

-p

scale (temperature and salinity using a two-way PERMANOVA within season and sector) as done for sediment (total mud content, total organic content, carbonate,

re

chlorophyll-a and phaeopigments using a three-way PERMANOVA across season, sectors and sites), two sets of abiotic factors were tested. Sediment variables and

lP

macrofaunal H’, J’, and BPc were square-root transformed before applying a Euclidean distance dissimilarity resemblance matrix, while macrofaunal composition, total

na

macrofaunal density, dominant taxa density (Magelonid, Sternaspid, Capitellid, Paraonid, Goniadid and Oligoqueta), biomass and functional groups density (deposit

Jo ur

feeders, OCO feeders, filter feeders, suspension feeders and detritivore feeders) were square-root transformed using abundance data with the Bray-Curtis resemblance matrix under a reduced residuals model to give more weight to less abundant taxa in the analyses. Since our macrofaunal composition data set had samples with no individuals, we added a dummy variable to the matrix (weight 1, Clarke and Gorley, 2006). If significant, a post-hoc pairwise test was performed on biotic and abiotic to assess significant differences in the global PERMANOVA (Anderson, 2008). A multidimensional scaling analysis (MDS) was applied using the squar-root abundance of all taxa from the Bray-Curtis similarity matrix. Macrofaunal assemblages were compared by MDS clustering significance using similarity percentage analysis (SIMPER; Clarke and Gorley, 2006). Distance-based Linear Model (DistLM) routines were performed to look for sediment variables (total mud content, total organic content, carbonate, chlorophyll-a and phaeopigments) influence to benthic assemblage across a drought period using a 6

Journal Pre-proof step-wise procedure (selection criterion = adjusted AICc on the biological macrofaunal abundance and sediment; McArdle and Anderson, 2001; Clarke and Gorley, 2006; Anderson et al., 2008). Macrofaunal composition data was square-root transformed and analyzed using the Bray-Curtis similarity matrix, while the total mud content, total organic content, carbonate, chlorophyll-a and phaeopigments in the sediment were analyzed using Euclidean distance. The BIO-ENV procedure was applied to relate the multivariate patterns of the macrobenthic assemblages with the sediment (total mud content, total organic content, carbonate, chlorophyll-a and phaeopigments; Spearman's classification, p between the two matrices of similarity). All analyses were performed

of

using PRIMER v 6.0 software with the PERMANOVA + add-on package (Clarke and

ro

Gorley, 2006; Anderson et al., 2008).

-p

3. Results

re

3.1. Seasonal climatic and estuarine changes

The SPI index indicated that this study occurs during the most intense drought

lP

period in Eastern Brazil (between 2014 to 2016), with moderate to extreme drought conditions persisting until 2017 (Figure 2). The driest periods were observed during Wet

na

2015 (SPI=-1.65) and Dry 2016 (SPI=-1.71). After the Wet 2017 period, SPI values increased in 2017 to 2019, reaching conditions considered near normal to moderate

Jo ur

wetness (Figure 2; Supplemental table S1, S2). Matching SPI changes, water temperature increased continuously from the Dry 2015 period (25.4±0.9 ºC) to the Dry 2016 period (29.9±0.9 ºC), following intensification of the drought indicated by the SPI index (PERMANOVA, df=2, PseudoF=6.6073, p=0.026; Table 1). By this, water salinity was higher in estuarine sector A if compared to sector B for all sampled seasons (PERMANOVA, df=1, Pseudo-F=17.302, p=0.003; Figure 3; Supplemental figure S1). Estuarine sectors A and B exhibited basic pH, from 7.6±0.0 to 8.9±0.2, while TDS ranged from 17.8±0.2 ppt to 30.5±0.0 ppt. The dissolved oxygen (DO) concentrations were lowest during the Dry 2016 period (<0.01 mg.L-1), if compared to previous seasons (Dry 2015=66.7±6.0 mg.L-1; Wet 2015=41.3±24.0 mg.L-1; Supplemental table S3). 3.2. Sediment parameters

7

Journal Pre-proof We observed significant seasonal and spatial changes in total mud content and total organic content in the estuary following the drought period (PERMANOVA, df=2, p<0.015; Table 1, 2; Supplemental table S4). Sediment total mud content increased from Dry 2015 to Dry 2016 (PERMANOVA, df=2, Pseudo-F=483.3, p=0.001; Supplemental table S5). However, sediment TOC and chlorophyll-a decreased during the same period (PERMANOVA, df=2, p=0.002). Sediment carbonate and phaeopigments also decreased from the Dry 2015 (Carbonate=16.5±10.8 %; Phaeopigments=4.0±1.3 µg.g-1) to Wet

2015 period (Carbonate=8.6±6.7

%;

Phaeopigments=3.1±1.9

µg.g-1;

PERMANOVA, df=2, p<0.047). We also observed spatial changes on sediment total

of

mud content, with higher values in the sector A (79.0±2.1 %) compared to sector B

ro

(76.2±2.7 %; PERMANOVA df=1, Pseudo-F=63.1, p=0.019).

-p

3.3. Macrofaunal assemblages

re

Macrofaunal density decreased following the intensification of the drought period from the Dry 2015 to the Dry 2016 (PERMANOVA, df=3, Pseudo-F=26.57,

lP

p=0.007; Figure 4; Table 1; Supplemental table S5, S6). Macrofaunal richness also decreased from the Dry 2015 to Wet 2015 period (PERMANOVA, df=2, Pseudo-

na

F=15.19, p=0.018). The estuary was dominated by deposit feeders (88.9 % rel. ab.), followed by OCO (omnivores, carnivores and others, 8.4 % rel. ab.). Filter feeders,

Jo ur

suspension feeders and detritivore feeders represented 2.7 % of the overall macrofauna. The density of deposit feeders decreased across the Dry 2015 and Dry 2016 seasons following an overall decrease in macrofaunal abundances (PERMANOVA, df=2, Pseudo-F=29.86, p=0.004; Figure 5; Table 1; Supplemental table S5, S6). In general, the decrease in macrofaunal species richness, Shannon H’, Pielou J’, OCO feeders and detritivore feeders were less intense in sector A than at sites from sector B across seasons. However, the abundance of macrofaunal filter feeders increased in both sectors over time (PERMANOVA df=4, p<0.031). Overall, changes in the community bioturbation potential (BPc) were influenced by the observed changes in benthic assemblages through the drought period. The BPc decreased over the drought period from Dry 2015 to Dry 2016 (PERMANOVA, df=2, Pseudo-F=14.794, p=0.011; Figure 4; Table 1; Supplemental table S5, S6). There were also taxa specific differences, with the BPi of Sternaspid and Paraonid annelids decreasing from Dry 2015 to Dry 2016 (PERMANOVA df=2, p<0.007). Differences in 8

Journal Pre-proof bioturbation potential among estuarine sectors were also observed with a stronger decrease in BPc in the sector A if compared to sector B. These followed community changes between those sectors, with Sternaspid becoming dominant in sector A, while Goniadid and Paraonid annelids dominated bioturbation in sector B. The BPc was higher in sector A (225.5±25.3 BPc) compared to sector B (131.6±12.3 BPc; PERMANOVA, df=1, Pseudo-F=123.09, p=0.013). 3.4. Multivariate analyses

of

Annelida was the most abundant taxa with Magelonid (685±720 ind.m-2, 49.3 %) and Sternaspid (314±524 ind.m-2, 22.6 %) representing over 71 % of the total

ro

macrofauna during the study. Benthic macrofaunal assemblage changed across all seasons suggesting continuous effects of drought intensification from 2015 to 2016

-p

(PERMANOVA, df=2, Pseudo-F=5.6602, p=0.001; Supplemental table S5, S6). In

re

addition, Magelonid, Sternaspid, Capitellid and Paraonid annelids drastically decreased in abundance across the same period, while Oligochaeta started to become abundant in

lP

the dry season of 2016 (PERMANOVA, df=2, p>0.005; Table 1; Supplemental S7, S8). The density of Paraonid annelids was higher in sector A (65±123 ind.m -2) compared to

na

sector B (28±74 ind.m-2; PERMANOVA, p<0.001). Changes in density of Magelonid, Sternaspid, Capitelid, Goniadid and Paraonid annelids were mostly responsible for

Jo ur

seasonal assemblage dissimilarity (70 to 72 %; SIMPER analysis), with spatial differences also being important (sector=71 %; Site=70 to 73 %; SIMPER analysis). The multivariate changes in the macrofaunal assemblages during the drought period were explained by the climate-related increase in total mud content (10.7 %), with lesser contribution from other sediment variables (all sediment variables explained 14.1 % of macrofaunal total variation). Additionally, the higher total sediment mud content in sector A influenced macrofaunal assemblages across estuarine sectors (BEST R=0.105, p=0.009; Table 3, 4; Figure 6; Supplemental figure S2). 4. Discussion Our study revealed ecological changes in estuarine benthic assemblages during the onset of a prolonged 14-month drought period on the Eastern Brazil Marine Ecoregion. The estuary had lower precipitation, increased water temperatures and 9

Journal Pre-proof salinity, and lower dissolved oxygen concentrations during the intense drought months. Benthic assemblages are greatly influenced by lower dissolved oxygen levels (DO<2 mg.L-1; Vaquer-Sunyer and Duarte, 2008), which may have followed decreased estuarine mixing and higher temperatures during the drought period. The lower freshwater influx into the estuary that likely occurred during the drought period may have also contributed to seasonal increases in water salinity and temperature. These observed changes in the estuary could be responsible for subsequent sedimentary changes through increased sedimentation and sinking of aggregates, resulting in the increasing mud content (Eisma, 1986; MacKay et al., 2010; Mari et al., 2012). In

of

addition, the mean grain size reduction may have resulted in decreased sediment permeability, increased TOC content, and lower oxygen penetration depth (Pratt et al.,

ro

2014; Thrush et al., 2003; Anderson, 2008), further contributing to overall changes in

-p

benthic macrofaunal composition.

The drought period likely reduced freshwater input to the estuary, which

re

associated throughout increases in salinity and temperature enhanced mud sediment aggregation and sedimentation processes over the estuary. The increased particle

lP

aggregation of fine sediments may have resulted from increased salinity and tidal flow from the nearby mangrove forests (Eisma, 1986; Mari et al., 2012; Servino et al., 2018;

na

Sippo et al., 2018). Furthermore, the spatial changes in total sedimentary mud content may have followed changes in water flow velocities in the seaward sector, resulting in

Jo ur

higher sediment aggregation and sedimentation processes compared to upper estuarine sectors (Dai et al., 2006; Mari et al., 2012). However, sediment organic matter decreased over time along with concurrent increases in water temperatures, which may have intensified sedimentary aerobic respiration, organic matter degradation and dissolved oxygen consumption (Dai et al., 2006). Changes in estuarine pelagic productivity during drought months also likely contributed to lower sediment organic matter content. Decreases in freshwater input and increases in water salinity and temperature may influence microphytobenthic assemblages through structure loss and nutrient deprivation, which would contribute to reduced cellular chlorophyll-a and phaeopigments (Carrasco et al., 2007; Gordon et al., 2016). The drought period significantly changed the estuarine benthic macrofauna structure, confirming our hypothesis. The total macrofaunal density decreased up to 3fold, while a continuous shift of dominant macrofaunal taxa was observed towards the prevalence of surface-dwelling macrofauna including oligochaete worms. However, 10

Journal Pre-proof some taxa including Magelonid, Sternaspid, Capitellid and Goniadid annelids continued to occur during drought periods, revealing a marked adaptation to the abiotic changes that occurred in the estuary (Montagna et al., 2002). Although several macrofaunal taxa persisted during drought months, their density decreased. As a result, changes in benthic assemblage structure were observed that resulted in a decrease in predominance of deposit feeders, omnivores and carnivores in the estuary. Our study supports previous assertions of drought impacts on marine and estuarine ecosystems through loss of less tolerant benthic taxa and impact on ecosystem functions. Drought periods may occur frequently in some regions, but El Niño periods

of

can intensify their impacts through an increase in their magnitude and duration. Intense drought events result in stronger biological impacts in the estuary if compared to natural

ro

seasonal oscillations in precipitation (Drexler and Ewel, 2001; Mermillod-Blondin,

-p

2011; Laverock et al., 2011; Kristensen et al., 2014; Rodrigues et al., 2019). Despite regional differences of benthic assemblage composition from the tropical PAM estuary

re

to other estuaries impacted by intense droughts, the resulting impacts were similar with loss of macrofaunal organisms and altered taxa composition (Ysebaert e Herman, 2002;

lP

Dolbeth et al., 2011; 2019; Supplemental table S9). Drought periods change ecosystems in a similar fashion, but the effects vary with the stress intensity across spatial and

na

temporal scales. The lower changes on macrofaunal assemblages in the seaward sector A could be associated with a higher tolerance of benthic assemblages to changes in

Jo ur

water and sediment properties, if compared to upper estuarine B regions. Although the estuary is largely polyhaline, macrofaunal assemblages of seaward regions should be historically more adapted to salinity increases (and related environmental changes in sediment) than macrofaunal assemblages from upper regions. Therefore, during intense droughts the salt-water intrusion intensively impair these upper regions. By another hand, during La Niña related wetness estuarine upper regions should present higher persistence to salinity decreases than seaward regions. However, with the increase in frequency and intensity of El Niño related droughts and La Niña related wetness, these changes should drastically impair estuarine macrofaunal assemblages persistence as a hole, being a urgent outreach in the understand of climate change impacts in wetlands ecosystem functions and services. The observed less pronounced assemblage impacts in sector A resulted in spatial differences in benthic bioturbation potential. These observed changes resulted in a 5fold decrease of the benthic bioturbation potential that may have further decreased 11

Journal Pre-proof overall sediment health (Folke et al., 2004; Braeckman et al., 2014). Because BPc highlights the capacity of benthic assemblages to transport particles across the sediment layer, and likely affects sediment re-working and ventilation, this index can be used as a proxy for ecosystem health as it partially reflects the degree of change in benthic assemblages. This is the first study to conduct a 14-month sampling experiment during a drought period that allowed an unprecedented view of continued loss of estuarine benthic diversity and function. The continued decrease in benthic ecosystems health demonstrated implications of potential future scenarios from increases in intensity and

of

frequency of extreme weather events in tropical estuaries, supporting their monitoring and use as models for coastal management (Dolbeth et al., 2011; Elliott and Whitfield,

ro

2011; Mcleod et al., 2011; Bernardino et al., 2016). Despite the unique relevance of

-p

estuarine ecosystems, only 19 estuaries globally are continuously monitored and have data to support observation of the long-term effects of drought (Supplemental table S9).

re

Some of these sites have decades of long-term monitoring thus allowing assessments of effects of drought, floods and recovery processes. With the predicted intensification of

lP

drought and other climatic events in the next century, it will be critical to identify changes in the state (or tipping points) of estuarine benthic assemblages if we are to

na

understand the resilience of these ecosystems to global climate change. Current international long-term monitoring networks (e.g. Long-Term Ecosystem Research

Jo ur

LTER-Europe and iLTER; Muelbert et al., 2019) will be key to align these efforts globally and across multiple ecosystems. 5. Conclusions

This is the first study that demonstrated drought impacts on a South American estuary, with changes in benthic habitats, water quality and benthic macrofaunal assemblages through altered dominance of functional groups and loss of bioturbation potential. The lower benthic bioturbation potential in the estuary is an ecological proxy for potential loss of ecosystem services caused by climate change. However, a continued spatial and temporal monitoring of this estuary will be key to understand inter-annual and decadal ecological shifts in a changing climate.

6. Acknowledgements 12

Journal Pre-proof

Thanks to R. Servino, L. Garcez and to many students for field support. Also, thanks to P. Tinelli for map support. This study was funded by a FAPES Biodiversidade 61847429/2013 and PELD (79054684/2017) grants to AFB. AFB was also supported by PELD

HCES

CNPq/CAPES

301412/2013-8,

470542/2013-6

and

PQ

grant

301161/2017-8. LEOG was supported by a FAPES graduate scholarship. This is a PELD-HCES contribution #007.

of

7. References Anderson, M.J. 2008. Animal-sediment relationships re-visited: characterising species’

splines.

J

Exp

Mar

Biol

Ecol,

366:16–27.

Doi:

-p

regression

ro

distributions along an environmental gradient using canonical analysis and quantile

10.1016/j.jembe.2008.07.006

re

Anderson, M.J., Gorley, R.N., Clarke, K.R. 2008. PERMANOVA. PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E Ltd., 214 p.

lP

Bernardino, AF., Netto, S.A., Pagliosa, P.R., Barros, F., Christofoletti, R.A., RosaFilho, J.S., Colling, J., Lana, P.C. 2015. Predicting ecological changes on benthic

Ecoregions.

na

estuarine assemblages through decadal climate trends along Brazilian Marine Estuarine,

Coastal

and

Shelf

Science,

74-82.

Doi:

Jo ur

10.1016/j.ecss.2015.05.021.

Bernardino, A.F., Pagliosa, P.R., Christofoletti, R.A., Barros, F., Netto, S.A., Muniz, P., Lana, P.C. 2016. Benthic estuarine communities in Brazil: moving forward to longterm studies to assess climate change impacts. Braz. j. oceanogr., 64, 2. Doi: 10.1590/S1679-875920160849064sp2 Bernardino, AF., Gomes, L.E.O., Hadlich, H.L., Andrades, R., Correa, L.B. 2018a. Mangrove clearing impacts on macrofaunal assemblages and benthic food webs in a

tropical

estuary.

Marine

Pollution

Bulletin,

126,

228-235.

Doi:

10.1016/j.marpolbul.2017.11.008 Bernardino, A.F., Azevedo, A.R.B., Pereira Filho, A.C.D., Gomes, L.E.O., Bissoli, L.B., Barros, F.C.R., 2018b. Benthic estuarine assemblages of the eastern marine Brazilian Ecoregion. In: Lana, P.C., Bernardino, A.F. (Eds.), Brazilian Estuaries: a Benthic Perspective. Springer International Publishing. Pgs 95-116. 212pp.

13

Journal Pre-proof Bissoli, L.B., Bernardino, A.F., 2018. Benthic macrofaunal structure and secondary production in tropical estuaries on the Eastern Marine Ecoregion of Brazil. PeerJ 6, e4441. https://doi.org/10.7717/peerj.4441. Braeckman, U., Yazdani-Foshtomi, M., van Gansbeke, D., Meysman, F., Soetaert, K., Vincx, M., Vanaverbeke, J. 2014. Variable importance of macrofaunal functional biodiversity for biogeochemical cycling in temperate coastal sediments. Ecosystems, 17, 720–737. Doi: 10.1007/s10021-014-9755-7 Carrasco, N., Perissinotto, R., Miranda, N.A.F. 2007. Effects of silt loading on the feeding and mortality of the mysid Mesopodopsis africana in the St. Lucia Estuary,

of

South Africa. Journal of Experimental Marine Biology and Ecology, 352, 152-164. Doi: 10.1016/j.jembe.2007.07.006

ro

Clarke, K.R., Gorley, R.N. 2006. PRIMER v6: User Manual/Tutorial, 6 ed, Plymouth

-p

Cook, B., Smerdon, J.E., Seager, R., Coats, S., 2014. Global warming and 21st century drying. Climate Dynamics, 43, 2607–2627. Doi: 10.1007/s00382-014-2075-y

re

Dai, M., Guo, X., Zhai, W., Yuan, L., Wang, B., Wang, L., Cai, P., Tang, T., Cai, W.J. 2006. Oxygen depletion in the upper reach of the Pearl River estuary during a drought.

Marine

Chemistry,

lP

winter

102,

159-169.

Doi:

10.1016/j.marchem.2005.09.020

na

Day, J.W., Christian, R.R., Boesch, D.M., Yanez-Arancibia, A., Morris, J., Twilley, R.R., Naylor, L., Schaffner, L., Stevenson, C. 2008. Consequences of climate

Jo ur

change on the ecogeomorphology of coastal wetlands. Estuaries and Coasts 31, 477-491. Doi: 10.1007/s12237-008-9047-6 Dittmann, S., Baring, R., Baggalley, S., Cantin, A., Earl, J., Gannon, R., Keuning, J., Mayo, A., Navong, N., Nelson, M. and Noble, W. 2015. Drought and flood effects on macrobenthic communities in the estuary of Australia's largest river system. Estuarine,

Coastal

and

Shelf

605

Science,

165,

36-51.

Doi:

10.1016/j.ecss.2015.08.023 Dolbeth, M., Cardoso, P.G., Grilo, T.F., Bordalo, M.D., Raffaelli, D., Pardal, M.A. 2011. Long-term changes in the production by estuarine macrobenthos affected by multiple stressors. Estuarine, Coastal and Shelf Science 92: 10-18. Doi: 10.1016/j.ecss.2010.12.00 Dolbeth, M., Crespo, D., Leston, S., Solan, M. 2019. Realistic scenarios of environmental disturbance lead to functionally important changes in benthic

14

Journal Pre-proof species-environment interactions. Marine Environmental Research, 150, 104770. Doi: 10.1016/j.marenvres.2019.104770 Doney, S.C., Ruckelshaus, M., Duffy, J.E., Barry, J.P., Chan, F. Englidh, C.A., Galindo, H.M. Grebmeier, J.M., Hollowed, A.B., Knowlton, N., Polovina, J., Rabalais, N.N., Sydeman, W.J., Talley, L.D. 2012. Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4: 11–37. Doi: 10.1146/annurev-marine-041911-111611 Drexler, J.Z., Ewel, K.C. 2001. Effect of the 1997–1998 ENSO-related drought on hydrology and salinity in a micronesian wetland complex. Estuaries, 24, 347-356. Doi: 10.2307/1353237

of

Eisma, D. 1986. Flocculation and de-flocculation of suspended matter in estuaries. Neth. J. Sea Res., 20: 183–199. Doi: 10.1016/0077-7579(86)90041-4

ro

Elliott, M., Whitfield, A.K. 2011. Challenging paradigms in estuarine ecology and

-p

management. Estuar Coast Shelf, 94: 306-314.

Folke, C., Carpenter, S., Walker, B., Scheffer, M., Elmqvist, T., Gunderson, L., Holling, Annu.

Rev.

re

C.S. 2004. Regime shifts, resilience, and biodiversity in ecosystem management. Ecol.

Evol.

Syst.,

35,

557-81.

Doi:

lP

10.1146/annurev.ecolsys.35.021103.105711

García-Rodriguez, F., Brugnoli, E., Muniz, P., Venturini, N., Burone, L., Hutton, M.,

na

Rodriguez, M., Pita, A., Kandratavicius, N., Paerez, L., Verocai, J. 2013. Warm phase ENSO events modulate the continental freshwater input and the trophic state

Jo ur

of sediments in a large South American estuary. Marine and Freshwater Research in press. Doi: 10.1071/MF13077 Gordon, N., Perissinotto, R., Miranda, N.A.F. 2016. Microalgal dynamics in a shallow estuarine lake: Transition from drought to wet conditions. Limnologica, 60, 20–30. Doi: 10.1016/j.limno.2016.05.010 Gray, J.S., Elliott, M., 2009. Diversity. In: Gray, J.S., Elliott, M. (Eds.), Ecology of Marine Sediments, second ed. Oxford, New York, pp. 52–57. Hadlich, H.L., Venturini, N., Martins, C.C., Hatje, V., Tinelli, P., Gomes, L.E.O., Bernardino, A.F. 2018. Multiple biogeochemical indicators of environmental quality in tropical estuaries reveal contrasting conservation opportunities. Ecological Indicators, 95, 21-31. Doi: 10.1016/j.ecolind.2018.07.027 Hastie, B.F., Smith, S.D.A. 2006. Benthic macrofaunal communities in intermittent estuaries during a drought: comparison with permanently open estuaries. J. Exp. Mar. Biol. Ecol. 330, 356-367. Doi: 10.1016/j.jembe.2005.12.039 15

Journal Pre-proof IPCC. 2001. Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change [Houghton, J.T., Y. Ding, D.J. Griggs, M. Noguer, P.J. van der Linden, X. Dai, K. Maskell, and C.A. Johnson (eds.)]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 881pp Jumars, P.A., Dorgan, K.M., Lindsay, S.M. 2015. Diet of worms emended: an update of polychaete feeding guilds. Annu. Rev. Mar. Sci. 7 14-39. Doi: 10.1146/annurevmarine-010814-020007 Kennish, M.J. 2002. Environmental threats and environmental futures of estuaries.

of

Environmental Conservation 29 (1), 78–107. Doi: 10.1017/S0376892902000061 Kristensen, E., Delefosse, M., Quintana, C.O., Flindt, M.R., Valdemarsen, T. 2014.

ro

Influence of benthic macrofauna community shifts on ecosystem functioning in

-p

shallow estuaries Front. Mar. Sci., 1, 1-14. Doi: 10.3389/fmars.2014.00041 Lana, P.C., Bernardino, A.F., 2018. Brazilian Estuaries: a benthic perspective. In: Turra,

re

A. (Ed.), Brazilian Marine Biodiversity Series. Springer International Publishing, ISBN 978-3-319-77779-5. https://doi.org/10.1007/978-3-319-77779-5. ISSN 2520-

lP

1085.

Laverock, B., Gilbert, J.A., Tait, K., Osborn, A.M., Widdicombe, S. 2011. Bioturbation:

na

impact on the marine nitrogen cycle. Biochemical Society Transactions, 39, 315– 320. Doi: 10.1042/BST0390315

Jo ur

Lorenzen, C.J. 1967. Determination of Chlorophyll and phaeopigments: spectrometric equations. Limnol. Oceanogr., 12: 343–346. MacKay, F. Cyrus, D., Russell, K. L. 2010. Macrobenthic invertebrate responses to prolonged drought in South Africa's largest estuarine lake complex. Estuarine, Coastal and Shelf Science, 86, 553–567. Doi: 10.1016/j.ecss.2009.11.011 Magalhães, W.F., Barros, F. 2011. Structural and functional approaches to describe polychaete assemblages: ecological implications for estuarine ecosystems. Marine and Freshwater Research, 62, 918–926. Doi: 10.1071/MF10277 Mari, X., Torréton, J.P., Trinh, C.B.T., Bouvier, T., Thuoc, C.V., Lefebvre, J.P., Ouillon, S. 2012. Aggregation dynamics along a salinity gradient in the Bach Dang estuary, North Vietnam. Estuarine Coast Shelf Sci, 96, 151-158. Doi: 10.1016/j.ecss.2011.10.028

16

Journal Pre-proof McArdle, B.H., Anderson, M.J. 2001. Fitting multivariate models to community data: a comment on distance‐ based redundancy analysis.

Ecology, 82(1). Doi:

10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2 McKee, T.B., Doesken, N.J., Kleist, J. 1993. The relationship of drought frequency and duration to time scales. Proceedings of the IX Conference on Applied Climatology. American Meteorological Society. Boston, MA, 179 - 184 p. Mcleod, E., Chmura, G.L., Bouillon, S., Salm, R., Bjork, M., Duarte, C.M., Lovelock, C.E., Schlesinger, W.H. & Silliman, B.R. 2011. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering

of

CO2. Frontiers in Ecology and The Environment, 9, 552 –560. Doi: 10.1890/110004

Oxford

University

Press,

New

York,

214pp.

Doi:

-p

management.

ro

McLusky, D.S., Elliott, M. 2004. The Estuarine Ecosystem: Ecology, Threats, and

10.1016/j.marpolbul.2014.03.049

re

Mermillod-Blondin, F. 2011. The functional significance of bioturbation and biodeposition on biogeochemical processes at the water-sediment interface in

10.1899/10-121.1

lP

freshwater and marine ecosystems. J. N. Am. Benthol. Soc. 30, 770–778. Doi:

na

Montagna, P.A., Kalke, R.D., Ritter, C. 2002. Effect of Restored Freshwater Inflow on Macrofauna and Meiofauna in Upper Rincon Bayou, Texas, USA. Estuaries 25, 6B,

Jo ur

1436–1447 p. Doi: 10.1007/BF02692237 Muelbert, J.E., Nidzieko, N.J., Acosta, A.T.R., Beaulieu, S., Bernardino, A.F. et al., 2019. ILTER - the International Long-Term Ecological Research Network as a platform for global coastal and ocean observation. Frontiers in Marine Science. Doi: 10.3389/fmars.2019.00527 Norkko, A., Rosenberg, R., Thrush, S.F., Whitlatch, R.B. 2006. Scale- and intensitydependent disturbance determines the magnitude of opportunistic response. Journal of

Experimental

Marine

Biology

and

Ecology,

330,

195–207.

Doi:

10.1016/j.jembe.2005.12.027 Olsen, Z. 2019. Quantifying the Spatial Extent and Distribution of Estuarine Habitat with Changing Salinity: Do Positive, Neutral, and Negative Estuaries Respond Differently to Salinity Variation?. Estuaries and Coasts. Doi: 10.1007/s12237-01900528-y

17

Journal Pre-proof Pillay, D., Perissinotto, R. 2008. The benthic macrofauna of the St. Lucia Estuary during the 2005 drought year. Estuarine, Coastal and Shelf Science, 77, 1, 35-46. Doi: 10.1016/j.ecss.2007.09.004 Pollack, J.B., Palmer, T.A., Montagna, P.A. 2011. Long-term trends in the response of benthic macrofauna to climate variability in the Lavaca-Colorado Estuary, Texas. Marine Ecology Progress Series, 436: 67–80. Doi: 10.3354/meps09267 Pratt, D.R., A.M. Lohrer, C.A. Pilditch, S.F. Thrush. 2014. Changes in ecosystem function across sedimentary gradients in estuaries. Ecosystems 17: 182–194. Doi: 10.1007/s10021-013-9716-6

of

Queirós, A.M., Birchenough, S.N., Bremner, J., et al., 2013. A bioturbation classification of European marine infaunal invertebrates. Ecology and Evolution 3,

ro

3958–3985. Doi: 10.1002/ece3.769

-p

Queirós, A.M., Stephens, N., Cook, R., Ravaglioli, C., Nunes, J., Dashfield, S., Harris, C., Tilstone, G.H., Fishwick, J., Braeckman, U., Somerfield, P.J., Widdicombe, S.

re

2015. Can benthic community structure be used to predict the process of bioturbation in real ecosystems?. Progress in Oceanography, 137 (B), Pages 559-

lP

569. Doi: 10.1016/j.pocean.2015.04.027

Quintana, C.O., Bernardino, A.F., Moraes, P.C., Valdemarsen, T., Sumida, P.Y.G.

na

2015. Effects of coastal upwelling on the structure of macrofaunal communities in SE Brazil. J. Mar. Syst. 143, 120–129. Doi: 10.1016/j.jmarsys.2014.11.003

Jo ur

Rodrigues, R.R., Taschetto, A.S., Gupta,A.S., Foltz, G.R. 2019. Common cause for severe droughts in South America and marine heatwaves in the South Atlantic. Nature Geoscience, 12, 620–626. Doi: 10.1038/s41561-019-0393-8 Servino, R.N., Gomes, L.E.O, Bernardino, A.F. 2018. Extreme weather impacts on tropical mangrove forests in the Eastern Brazil Marine Ecoregion. Science of the Total Environment, 628–629, 233-240. Doi: 10.1016/j.scitotenv.2018.02.068 Sippo, J.Z., Lovelock, C.E., Santos, I.R., Sanders, C.J., Maher, D.T., 2018. Mangrove mortality in a changing climate: An overview. Estuar. Coast. Shelf Sci. 215, 241– 249. https://doi.org/10.1016/j.ecss.2018.10.011 Solan, M., Cardinale, B.J., Downing, A.L., Engelhardt, K.A.M., Ruesink, J.L., Srivastava, D.S. 2004. Extinction and ecosystem function in the marine benthos. Science 306: 1177–1180. Doi: 10.1126/science.1103960 Thrush, S.F., Hewitt, J.E., Norkko, A., Nicholls, P.E., Funnell, G.A., Ellis, J.I. 2003. Habitat change in estuaries: predicting broad-scale responses of intertidal 18

Journal Pre-proof macrofauna to sediment mud content. Mar. Ecol. Prog. Ser., 263, 101–112. Doi: 10.3354/meps263101 Vaquer-Sunyer R., Duarte, C.M. 2008. Thresholds of hypoxia for marine biodiversity. PNAS 105(40):15452-15457. Doi: 10.1073/pnas.0803833105 Varzim, C.S., Hadlich, H.L., Andrades, R., Mazzuco, A.C.A., Bernardino, A.F. 2019. Tracing pollution in estuarine benthic organisms and its impacts on food webs of the Vitoria Bay estuary. Estuarine Coastal and Shelf Science, 229: 10640. Doi: 10.1016/j.ecss.2019.106410 Worm, B., Barbier, E.B., Beaumont, N., Duffy, J.E., Folke, C., Halpern, B.S., Jackson,

of

J.B.C., Lotze, H.K., Micheli, F., Palumbi, S.R., Sala, E., Selkoe, K.A., Stachowicz, J.J., Watson, R. 2006. Impacts of biodiversity loss on ocean ecosystem services.

ro

Science, 314(5800), 787-790p. Doi: 10.1126/science.1132294

-p

Ysebaert, T., Herman, P.M.J. 2002. Spatial and temporal variation in benthic macrofauna and 330 relationships with environmental variables in an estuarine,

Jo ur

na

lP

124. Doi: 10.3354/meps244105

re

intertidal soft-sediment environment. Marine Ecology Progress Series, 244, 105–

19

Journal Pre-proof 8. Table captions Table 1. PERMANOVA results of water temperature, sediment total mud content and biological variables (total macrofaunal density and their dominant taxa (Mageloniadae, Sternaspidae, Capitellidae, Paraonidae and Oligochaeta), community bioturbation potential (BPc) and macrofaunal composition) for the monitoring period in the PAM estuary. Bold F-values indicate significant p values. Table 2. Total mud content (%), total organic content (%), carbonate (%), chlorophyll-a

of

(μg.g-1) and phaeopigments (μg.g-1) during the dry and wet seasons in 2015 and dry

ro

season in 2016 at each site of the polyhaline sectors A and B of the PAM estuary. Table 3. BEST correlations between macrobenthic assemblages, total mud content, total

re

weighted Spearman coefficients.

-p

organic content, carbonate, chlorophyll-a and phaeopigments in the PAM estuary. Pw =

lP

Table 4. Distance-based linear model (DistLM) of Bray-Curtis similarity in macrobenthic assemblages, total mud content, total organic content, carbonate,

na

chlorophyll-a and phaeopigments between seasons (dry and wet seasons in 2015 and

Jo ur

dry season in 2016) in the PAM estuary. Bold F-values indicate significant p values.

20

Journal Pre-proof 9. Figure captions Figure 1. Study area indicating the polyhaline sectors A (lower estuary) and B (upper estuary) and their sampling sites (S1 and S2 of each sector). Figure 2. Standardized Precipitation Index (SPI) from 2014 to 2018 evidencing the sampling during the El Niño drought period in 2015 and 2016 (May of 2015 to June of 2016, gray area) in the PAM estuary. ≥ 2 SPI = extreme wet and ≤ −2 SPI = extreme

of

dry; McKee et al., (1993). Figure 3. Changes in water salinity and temperature (ºC) in spring and neap tides of the

-p

ro

polyhaline sectors (A and B) across the El Niño period in the PAM estuary. Figure 4. Total macrofaunal density and their community bioturbation potential (BPc) with

re

related SPI during the dry and wet seasons in 2015 and dry season in 2016 in the PAM

lP

estuary. Vertical lines indicate the Standard Error.

Figure 5. Total mud content, macrofaunal richness, dominant taxa density

na

(Mageloniadae, Sternaspidae, Capitellidae, Paraonidae and Oligochaeta) and Deposit feeders with related SPI during the dry and wet seasons in 2015 and dry season in 2016

Jo ur

in the PAM estuary. Vertical lines indicate the Standard Error. Figure 6. DistLM distance-based redundancy analysis (dbRDA) plot based on total mud content (Mud), total organic content (TOC), carbonate (Carb), chlorophyll-a (Chl-a) and phaeopigments (Phae) that best explained the benthic macrofauna in the PAM estuary.

21

Journal Pre-proof Conflict of interest

Jo ur

na

lP

re

-p

ro

of

The authors declare no actual or potential conflict of interest.

22

Jo ur

na

lP

re

-p

ro

of

Journal Pre-proof

23

Journal Pre-proof Credit Luiz Eduardo de Oliveira Gomes (LEOG) and Angelo Fraga Bernardino (AFB) participated in all process related to the article construction (e.g. sampling, analyzed

Jo ur

na

lP

re

-p

ro

of

data, wrote the manuscript and approved the final article).

24

Journal Pre-proof Declaration of 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.

Jo ur

na

lP

re

-p

ro

of

☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

25

Journal Pre-proof

Table captions Table 1. PERMANOVA results of water temperature, sediment total mud content and biological variables (total macrofaunal density and their dominant taxa (Mageloniadae, Sternaspidae, Capitellidae, Paraonidae and Oligochaeta), community bioturbation potential (BPc) and macrofaunal composition) for the monitoring period in the PAM estuary. Bold F-values indicate significant p values. Unique Unique Variables df SS MS Pseudo-F p Variables df SS MS Pseudo-F p perms perms Water temperature Magelonidae density ºC Sea 2 71.275 35.637 Sea 2 13806.00 6903.00 29.074 6.607 0.026 998 0.005 999 Sec 1 0.94605 0.94605 1.754 0.206 995 Sec 1 96.74 96.74 0.179 0.704 3 SeaxSec 2 3.11E-02 1.55E-02 0.029 0.980 998 Si(Sec) 2 1079.80 539.91 3.203 0.045 999 Res 8 43.149 0.53936 SeaxSec 2 488.12 244.06 1.028 0.465 999 Total 13 13 SeaxSi(Sec) 4 949.72 237.43 1.409 0.250 999 Total mud content Res 324 54616.00 168.57 Sea 2 48.059 24.029 Total 335 71242.00 483.310 0.001 999 Sec 1 0.54978 0.54978 63.090 Sternaspidae density 0.019 6 Si(Sec) 2 1.72E-02 8.59E-03 0.014 0.989 999 Sea 2 11532.00 5766.20 36.923 0.004 998 SeaxSec 2 12.345 0.61725 12.415 Sec 1 1173.50 1173.50 13.199 0.077 3 0.013 999 SeaxSi(Sec) 4 0.19757 4.94E-02 0.081 0.988 999 Si(Sec) 2 177.81 88.91 0.649 0.513 998 Res 100 60.941 0.60941 SeaxSec 2 448.94 224.47 1.437 0.349 997 Total 111 111 SeaxSi(Sec) 4 624.67 156.17 1.140 0.328 999 Total macrofaunal density Res 324 44403.00 137.05 Sea 2 23679.00 11840.00 26.573 Total 335 58789.00 0.007 999 Sec 1 1463.60 1463.60 2.341 0.276 3 Paraonidae density Si(Sec) 2 1250.20 625.10 Sea 2 2335.50 1167.70 68.666 3.148 0.035 997 0.001 998 SeaxSec 2 133.85 66.93 0.150 0.860 999 Sec 1 295.68 295.68 59.617 0.014 3 SeaxSi(Sec) 4 1782.20 445.55 2.244 0.067 997 Si(Sec) 2 9.92 4.96 0.172 0.849 998 Res 324 64340.00 198.58 SeaxSec 2 219.40 109.70 6.451 0.055 999 Total 335 92618.00 SeaxSi(Sec) 4 68.03 17.01 0.591 0.666 999 Macrofaunal composition Res 324 9326.70 28.79 Sea 2 60413.00 30207.00 5.660 Total 335 12373.00 0.001 997 Sec 1 5061.30 5061.30 0.744 0.616 3 Oligochaeta density Si(Sec) 2 13605.00 6802.30 3.328 Sea 2 272.31 136.16 24.954 0.001 998 0.012 547

f o

l a

o r p

r P

e

n r u

o J

26

Journal Pre-proof

SeaxSec 2 6004.30 3002.10 SeaxSi(Sec) 4 21346.00 5336.60 Res 324 662240.00 2043.90 Total 335 765010.00 Community bioturbation potential (BPc) Sea 2 67.87 33.94 Sec 1 8.21 8.21 Si(Sec) 2 0.13 0.07 SeaxSec 2 11.66 5.83 SeaxSi(Sec) 4 9.18 2.29 Res 324 235.34 0.73 Total 335 335.00

0.563 2.611

0.849 0.001

997 998

14.794 123.090 0.092 2.541 3.158

0.011 0.013 0.926 0.179 0.020

999 3 998 997 999

l a

Sec 1 Si(Sec) 2 SeaxSec 2 SeaxSi(Sec) 4 Res 324 Total 335 Capitellidae density Sea 2 Sec 1 Si(Sec) 2 SeaxSec 2 SeaxSi(Sec) 4 Res 324 Total 335

0.18 6.61 0.15 5.46 8.87

0.028 0.745 0.028 0.615

0.888 0.446 0.970 0.648

2 999 559 996

523.85 6.32 503.15 155.37 65.96 23208.00 24425.00

f o

15.885 0.025 3.512 4.711 0.230

0.014 0.888 0.034 0.086 0.929

999 3 999 998 999

o r p

e

r P

0.18 13.23 0.30 21.83 2875.30 3175.70

261.93 6.32 251.58 77.69 16.49 71.63

n r u

o J

27

Journal Pre-proof

Table 2. Total mud content (%), total organic content (%), carbonate (%), chlorophyll-a (μg.g-1) and phaeopigments (μg.g-1) during the dry and wet seasons in 2015 and dry season in 2016 at each site of the polyhaline sectors A and B of the PAM estuary. Sectors Sites Seasons Total mud content Total organic content Carbonate Chlorophyll-a Phaeopigments Dry season of 2015 74.1 ± 11.4 13.8 ± 6.3 12.0 ± 8.6 8.2 ± 3.5 4.4 ± 1.4 Site 1 Wet season of 2015 76.2 ± 10.0 9.1 ± 3.2 8.8 ± 7.9 15.1 ± 5.9 2.7 ± 1.4 Dry season of 2016 98.9 ± 37.5 8.7 ± 4.1 11.6 ± 8.8 4.9 ± 2.9 3.3 ± 1.3 Polyhaline sector A Dry season of 2015 70.9 ± 19.1 14.1 ± 10.1 26.8 ± 13.7 11.6 ± 4.9 4.0 ± 1.9 Site 2 Wet season of 2015 76.7 ± 12.3 11.0 ± 4.1 8.6 ± 8.3 8.7 ± 3.5 3.4 ± 1.4 Dry season of 2016 97.4 ± 37.0 11.6 ± 5.9 12.9 ± 10.6 5.1 ± 3.0 4.2 ± 2.1 Dry season of 2015 63.2 ± 21.4 11.6 ± 5.0 9.8 ± 4.1 9.2 ± 4.0 3.6 ± 0.8 Site 1 Wet season of 2015 60.0 ± 22.4 13.5 ± 7.8 17.6 ± 5.9 9.8 ± 3.1 3.9 ± 0.8 Dry season of 2016 75.8 ± 12.0 9.4 ± 3.8 8.7 ± 6.5 11.9 ± 3.7 3.5 ± 2.4 Polyhaline sector B Dry season of 2015 74.3 ± 12.0 9.5 ± 3.0 8.2 ± 5.4 7.1 ± 4.5 2.8 ± 2.3 Site 2 Wet season of 2015 99.3 ± 1.8 12.0 ± 4.1 10.1 ± 7.9 5.1 ± 3.5 3.8 ± 1.0 Dry season of 2016 100.0 ± 0.0 10.4 ± 3.7 18.0 ± 14.2 8.0 ± 6.2 3.8 ± 0.6

f o

l a

o r p

r P

e

n r u

o J

28

Journal Pre-proof Table 3. BEST correlations between macrobenthic assemblages, total mud content, total organic content, carbonate, chlorophyll-a and phaeopigments in the PAM estuary. Pw = weighted Spearman coefficients. Nº of variables Pw Variables 1 0.105 Total mud content 2 0.103 Total mud content, Carbonate 3 0.066 Total mud content, Total organic content, Carbonate 3 0.061 Total mud content, Carbonate, Chlorophyll-a 1 0.050 Carbonate

Jo ur

na

lP

re

-p

ro

of

Table 4. Distance-based linear model (DistLM) of Bray-Curtis similarity in macrobenthic assemblages, total mud content, total organic content, carbonate, chlorophyll-a and phaeopigments between seasons (dry and wet seasons in 2015 and dry season in 2016) in the PAM estuary. Bold F-values indicate significant p values. Variables SS (trace) Pseudo-F p Prop. Total mud content 13473 0.10721 13.209 0.001 Total organic content 1852.2 1.6455 0.117 1.47E-02 Carbonate 1419.7 1.2569 0.251 1.13E-02 Chlorophyll-a 1974.8 1.7562 0.098 1.57E-02 Phaeopigments 1452.2 1.286 0.256 1.16E-02

29

Journal Pre-proof Graphical abstract

Highlights

na

lP

re

-p

ro

of

Drought period has decreased dissolved oxygen and mean sediment grain size Macrofaunal structure and bioturbation decrease linked to drought Predominance of opportunistic taxa during the drought intensification Climate change can impact benthic fauna and their functions in tropical estuaries Drought lead to loss of community mobility, re-working and sediment ventilation

Jo ur

    

30

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6