A 1500-year multi-proxy record of subtropical mangrove dynamics in relation to sea level and climate changes on Babitonga Bay,Southern Brazil

Abstract

Climatic changes and sea level variations have had a significant impact on the mangroves along the Brazilian coast during the Holocene. The present study focused on understanding the specific factors that have determined the establishment and expansion of mangroves in a subtropical estuary of southern Brazil (Babitonga Bay, State of Santa Catarina-SC), as well as their response to climate change and sea level variations during the late-Holocene. In this study, we carried out sedimentary analysis, palynology, and radiocarbon dating (C-14) to paleoenvironmental reconstruction of the last 1500 cal. year BP. Three facies associations were identified, indicating a progradational succession where a tidal flat was developed at the margin of the estuary. During the first phase, between at least 1440 and ±1286 cal. year BP, the area was characterized by a subtidal environment. The presence of Laguncularia pollen grains since ± 1390 cal. year BP indicated favorable conditions for mangrove establishment in proximity to the study site. Subsequently, around ± 1286 cal. year BP, the tidal flat developed, reaching the present-day shoreline, facilitated by the relative sea level drop. Avicennia trees were established on the tidal flat since ± 1273 cal. year BP, and the establishment of Rhizophora trees occurred in the most recent decades. This mangrove succession developed in Babitonga Bay following a temperature gradient, associated with low-temperature tolerance, and likely its establishment is associated with a temperature increase during the late-Holocene, that caused a migration of the southern limit of the mangrove in the subtropical zone to higher latitudes. Furthermore, the relatively slow expansion of mangroves upstream of Babitonga Bay also may have been controlled by the suitable salinity and substrate conditions, which were favored by the relative sea-level fall during the late-Holocene.

Keywords

Babitonga Bay climate change late-Holocene palynology sea level

Introduction

Climate change and variations in relative sea level during the Holocene have had significant impacts on the distribution of coastal environments, particularly on mangroves occupying the intertidal zone. Mangroves are highly productive and biodiverse ecosystems of significant environmental and economic importance (Woodroffe et al., 2014), distributed in protected regions and along estuary margins (Duke et al., 1998; Tomlinson, 1986) in tropical and subtropical regions. The distribution of mangroves is influenced by various factors, such as temperature, substrate type, salinity, wave and tidal energy, flooding frequency, river dynamics, coastal geomorphology, salinity gradient, and nutrient availability (Cohen et al., 2012; Schaeffer Novelli et al., 2016). Therefore, these ecosystems are particularly sensitive to climate and environmental changes (Alongi, 2015), and are used as indicators to investigate coastal changes and sea level variations (Blasco et al., 1996).

Along the coast of Brazil, previous studies have revealed that during the early and middle Holocene, the global mean surface temperature increased (Kaufman et al., 2020), leading to a rise in sea level that resulted in the inundation of river valleys (Scheel-Ybert, 2000) and changes in deposition systems and mangrove areas (Angulo et al., 2006; Bezerra et al., 2003; Martin et al., 2003; Suguio et al., 1985). The mangroves along the tropical coast of Brazil (~2°N to 19°S) were established approximately 7000 cal. year BP, favored by the stabilization of sea level (Cohen et al., 2012; Fontes et al., 2017; França et al., 2013, 2015; Ribeiro et al., 2018). The gradual decrease in sea level during the late-Holocene (Angulo et al., 2006) and changes in river flow, with the contribution of sandy sediments, favored coastal progradation and the development of mangroves in tropical latitudes (Cohen et al., 2014; França et al., 2013, 2015). Holocene warming may have caused an expansion of mangroves from tropical to subtropical zones during the late-Holocene (Cohen et al., 2020; França et al., 2019; Pessenda et al., 2012; Rodrigues et al., 2022). In recent millennia, evidence indicates a gradual increase in temperature (Baker and Fritz, 2015; Neukom et al., 2011; Santos et al., 2013). Recent studies have observed a significant migration of mangroves toward the poles and the invasion of coastal marshes in North and South America in the past few decades (Cavanaugh et al., 2014, 2019; Cohen et al., 2020), due to rising temperatures and a reduction in extreme cold events (Cohen et al., 2020; Coldren and Proffitt, 2017; França et al., 2019; Osland et al., 2016; Quisthoudt et al., 2012; Soares et al., 2012; Yao et al., 2022).

The temperature increase creates more favorable conditions for the survival and growth of mangrove species. On the other hand, variations in sea level can have significant effects on the distribution, structure, and function of mangroves. For example, sea level change is a critical factor in coastal environments, as geomorphological variations have direct implications on mangrove dynamics (Cavanaugh et al., 2014). Additionally, geomorphological variations associated with sea level change, such as coastline migration and sedimentation, can alter flooding patterns and the availability of sediments necessary for mangrove growth (Cohen et al., 2014). Therefore, to predict the response of mangroves to climate change scenarios and sea level variations, it is essential to investigate past vegetation succession and understand the factors influencing their dynamics in specific regions.

Along the Brazilian southern coast, mangroves are restricted to microtidal bays (tidal range less than2 m), lagoons, or estuary entrances, which are strongly controlled by climate and oceanographic characteristics (Soares et al., 2012). Therefore, this is a critical location to investigate the dynamics of subtropical mangroves near their latitudinal boundary in South America. Thus, in this study, we used paleoenvironmental reconstruction techniques such as facies analysis, palynology, and radiocarbon dating (C-14) on a 200 cm core (SF6) and compared it with the SF1 sediment core (França et al., 2019), to reconstruct the late-Holocene geomorphological and vegetation dynamics in Babitonga Bay. Through these approaches, we aim to gain a better understanding of the factors that have determined the establishment and dynamics of mangroves in subtropical estuaries of southern Brazil, as well as their response to climate change and sea level variations during the late-Holocene.

Modern setting of study area

Study area, geological and morphological setting

The study area is situated within the estuarine complex of Babitonga Bay, located on the north coast of Santa Catarina, in southern Brazil (Figure 1a). This estuarine complex encompasses approximately 160 km² (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), 1998). Babitonga Bay can be divided into three sections: the main channel in the northeast, the Palmital Channel in the north and the Linguado Channel in the south, which separates São Francisco do Sul Island from the continental (Vale and Schaeffer-Novelli, 2018). The Bay has an average depth of 6 m and an average salinity of 10‰. This estuary is influenced by four hydrographic basins: Cachoeira River basin (85 km²), Palmital River basin (358 km²), Cubatão River basin (484 km²), and Parati River basin (72 km²), furthermore receiving a contribution from several minor streams (Barros et al., 2010). The estuarine complex is strongly related to Quaternary sea-level oscillations (Tomazelli and Villwock, 2000; Villwock et al., 1986). Pleistocene sediments are characterized by intertidal marine and lagoon deposits (Horn Filho and Simó, 2008), and Holocene sediments consist of aeolian, fluvial, anthropogenic conchiferous (shell-middens named “sambaqui”), and marine and lagoon deposits (Horn Filho et al., 2014). During the Holocene, rising sea level flooded the river valleys (Mazzer and Gonçalves, 2012) and the coastal plains, followed by a relative sea-level fall until reaching the current mean sea level.

Figure 1.

Study area. (a) Brazil, State of Santa Catarina and Babitonga Bay location. (b) Vegetation map of Palmital Channel and location of the sampling site of core SF6 (this study) and SF1 (França et al., 2019).

The Babitonga Bay (São Francisco do Sul Bay) is located 300 km north of the current southern limit of mangrove distribution in South America. The bay is colonized by mangroves covering approximately 6200 ha (Figure 1b), which corresponds to 75% of the total mangrove ecosystem in the state of Santa Catarina (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), 1998), making it the last major remnant of this ecosystem at its distribution limit in the South Atlantic.

Climate and oceanographic setting

The Babitonga Bay region is characterized by a humid mesothermal subtropical climate (type Cfa according to the Köppen classification) (Alvares et al., 2013; Koehntopp et al., 2021), being influenced by polar and tropical Atlantic air masses (Viero, 2016). Currently, the average annual temperature ranges from 18°C and 20°C, with the warmest months being January and February, reaching 24.5°C, and the coldest month being July at 16.5°C (Ziffer-Berger, 2008). Annual precipitation typically ranges from 1500 to 2000 mm (Koehntopp et al., 2021), with the highest rainfall occurring between September and March (spring and summer), and a notable decrease in precipitation between April and August (winter) (Gonçalves et al., 2006). The average humidity level is around 80%. Babitonga Bay is characterized by microtidal regime (amplitude < 2 m), of mixed type, predominantly semidiurnal tide, with an average amplitude of 0.85 m, reaching a maximum of 1.28 m during the syzygy periods (new phase and full phase of moon), and a minimum of 0.27 m during the quadrature periods (Truccolo and Schettini, 1999). The estuarine circulation transports approximately 7.8 × 108 m³ of water, with a residence time of approximately 140 days (Mazzer and Gonçalves, 2012). These dynamics are primarily influenced by tides, hydrological conditions, and meteorological factors (Mazzer and Gonçalves, 2012). Flood tidal currents dominate the bay, with slightly higher speeds than ebb tide currents (Viero, 2016). The asymmetry in tidal wave propagation is determined by friction effects, and channel narrowing (Truccolo and Schettini, 1999). Water salinity ranges from 5.8‰ and 24‰ (Cunha et al., 2005). The coastal depositional system is wave-dominated with a tidal influence (Mazzer and Gonçalves, 2012). The shore can be classified as intermediate with an exposed beach (Klein and Menezes, 2001).

Vegetation

The modern vegetation in the study region is composed mainly of tropical ombrophilous forest, herbs, restinga, and mangroves (Figure 2). The tropical ombrophilous forest is the main type of vegetation in this region (Veloso et al., 1991), colonizing the higher land portions without tides influence (Cunha et al., 2005; Ziffer-Berger, 2008).

Figure 2.

The modern vegetation of tropical ombrophilous forest, herbs, restinga, and mangroves.

Material and methods

Fieldwork and image acquisition and processing

Fieldwork was carried out in September 2015. A sediment core, SF-6 (2.00 m depth; S 26° 6′ 48.30″/ W 48° 47′ 29.5″; 0.8 m above relative sea-level), was collected on the tidal plain dominated by mangrove along the margins of the Palmital Channel, upstream (Figure 1), using a peat sampler. PVC tubes were used sample collection and storage, and the samples were stored in a refrigerator at approximately 4°C to preserve the organic matter and prevent deterioration.

To discriminate different vegetation types and geomorphological features in the study area, medium-resolution optical image (30 m) from Landsat 8 OLI acquired in July-2021 was obtained by the Google Earth Engine platform database. The highest available pre-processing level, “Surface Reflectance Tier 1” was selected. A false-color band composition (RGB 564) was utilized to enhance the contrast between different vegetation types and mangroves, facilitating the mapping process. High-resolution images from Google Earth Pro were used to collect sample points for classifier training and validation. The sampling model used in this study consisted of six land cover classes: mangroves, ombrophilous forest, water bodies, herbaceous vegetation, agriculture and pasture, and infrastructure. Vegetation mapping was performed on the cloud computing platform Google Earth Engine, applying the Random Forest classifier. Topographic data were derived from Shuttle Radar Topography Mission (SRTM) and downloaded from USGS. Image interpretation of elevation data was carried out using the software Global Mapper.

Facies analysis

The SF-6 core was X-rayed to identify sedimentary structures. Samples were selected at a 5 cm interval for grain size analysis following the standard procedures described in Zhang et al. (2021). Grain size was determined by laser diffraction using a Laser Particle Size SHIMADZU SALD 2101 in the Laboratory of Chemical Oceanography/UFPA. Prior to grain size identification, approximately 0.5 g of each sample was immersed in H₂O₂ to remove organic matter; immersed in HCl 10% to remove carbonates; and residual sediments were disaggregated by ultrasound. The sediment grain size distribution was determined following the methods of Wentworth (1922), with fractions of sand (2–0.0625 mm), silt (62.5–3.9 µm), and clay (3.9–0.12 µm). Facies analyses involved a description of lithology, texture and structure, following the methods of Walker and James (1992).

Palynological analysis

Sediment samples of 1.0 cm³ were taken at 5 cm intervals along the studied core. Samples were prepared using standard pollen analytical techniques (Faegri and Iversen, 1989), which include the elimination of humic substances by potassium hydroxide, cellulose by acetic anhydride mixture (acetic anhydride and sulfuric acid), and silicate minerals by the action of hydrofluoric acid. A tablet of exotic Lycopodium spores was added to each sample to calculate the pollen concentration (grains.cm⁻³). Pollen and spores were identified by comparison with reference collections of various pollen keys (Roubik and Moreno, 1991), jointly with the reference collection of the Laboratory of Coastal Dynamics (LADIC-UFPA) and the C-14 Laboratory of the Center for Nuclear Energy in Agriculture (CENA/USP). A minimum of 300 pollen grains were counted for each sample (except when pollen concentration was too low) to ensure the results are statistically significant. Pollen and spore data are presented in pollen diagrams as percentages of the total pollen sum. The pollen taxa were grouped according to the source: mangrove, trees and shrubs, herbs, and palms pollen, as well as the marine source (Foraminifera), ferns, and fungi. The software TILIA was used for calculation and to plot the pollen diagram (Grimm, 1990). CONISS was used for cluster analysis of pollen taxa, permitting the zonation of the pollen diagram (Grimm, 1987).

Chronology (C-14)

Three sediment samples (10 g) were collected for radiocarbon dating. Samples were selected based on stratigraphic discontinuities that suggest changes in the tidal inundation regime. Sedimentary organic matter was treated as described by Pessenda et al. (2012). To avoid natural contamination by shell fragments, roots, seeds, etc., sediment samples were checked and cleaned under the stereoscopic microscope. The organic matter was chemically treated to eliminate the presence of a younger organic fraction and remove adsorbed carbonates by placing the samples in 2% HCl at 60°C for 4 h, followed by rinsing with distilled water to neutralize the pH. Finally, the samples were dried at 50°C and taken for analysis at the CENA/USP C-14 Laboratory. The chronology for the sedimentary sequence was provided by accelerator mass spectrometer (AMS) at the Center for Applied Isotope Studies of Georgia University (UGAMS). Radiocarbon ages were normalized to the δ¹³C value of −25‰ VPDB and calibrated using the SHCal20 calibration curve (Hogg et al., 2020) in CALIB 8.2 software (Stuiver et al., 2021) (Table 1). Results were reported as years before present (cal. year BP), with 0 cal. year BP equivalent to 1950 AD (Reimer et al., 2013). Dates are reported as the median of calibrated ages.

Table 1.

Mangrove samples selected for radiocarbon dating and results with code site, laboratory number, depth (m), material, ages C-14 year BP (1σ), calibrated ages (cal. year BP, 2σ deviation), and median of calibrated ages (cal. year BP), according to Hogg et al. (2020), SHCal20.

Sediment core	Cody site and laboratory number	Depth (m)	Material	Ages (C-14 year BP, 1σ)	Ages (cal. year BP, 2σ deviation)	Median of age range (cal. year BP)	Reference
SF1	UGAMS-28368	0.75–0.80	Bulk sed.	1070 ± 20	916–960	938 ± 22	França et al. (2019)
SF1	UGAMS-28372	1.10–1.15	Bulk sed.	950 ± 20	763–822	793 ± 30	França et al. (2019)
SF1	UGAMS-28848	1.60–1.65	Bulk sed.	1570 ± 20	1353–1432	1393 ± 40	França et al. (2019)
SF1	UGAMS-31233	2.30–2.35	Bulk sed.	1870 ± 30	1700–1833	1767 ± 67	França et al. (2019)
SF6	UGAMS-39926	0.80–0.85	Bulk sed.	497 ± 24	507–542	525 ± 18	This study
SF6	UGAMS-39925	1.25–1.29	Bulk sed.	1303 ± 24	1226–1289	1258 ± 32	This study
SF6	UGAMS-39924	1.90–2.00	Bulk sed.	1536 ± 30	1360–1522	1441 ± 81	This study

Results

Vegetation and topography

The study focused on a 270 km² area under the influence of the Palmital Channel (Figure 1b). The brackish water along the channel allows mangrove development on tidal flats with salinities between 7‰ and 20‰. The mangroves (8 km²) are characterized by Laguncularia, Avicennia, and Rhizophora, occupying areas between 0.2 and 1.0 m above mean sea level. Herbaceous vegetation (5.48 km²), dominated by Poaceae, Cyperaceae, and Acrostichum, is located in a topographic zone between mangrove and ombrophilous forest, but some herbs also colonize low topographic levels, colonizing riverbanks. Ombrophilous forest (154 km²) is found on elevated substrates without fluvial or tidal influence.

Chronological results and accumulate substrate rates

Three radiocarbon dates are used to provide a chronological framework to interpret the paleoecological data (Table 1). The results represent a sedimentary record covering approximately 1500 years BP (Figure 3).

Figure 3.

Age-depth model based on the Bayesian statistics and three C-14 dates from core SF-6.

The ages displayed in cal. year BP (2σ) revealed for each depth were 1441 ± 81 cal. year BP (190–200 cm), 1258 ± 32 cal. year BP (125–129 cm), and 525 ± 18 cal. year BP (80–85 cm). The estimated accumulation rates were 3.8 mm/year (200–195 to 129–125 cm depth), 0.6 mm/year (129–125 to 85–80 cm depth), and 1.6 mm/year (85–80 cm depth to the surface). The accumulation rates were within the range recorded in other cores sampled on tidal flats in Babitonga Bay (França et al., 2019). The rates in the muddy segment (130–0 cm) were lower (1.6 and 0.6 mm/year) than in the sandy interval (200–140 cm). In addition to radiocarbon dating core SF6, we also used core SF1 C-14 ages (França et al., 2019), to compare the mangrove content of both records. The sediment core SF1 was collected downstream SF6 in the Palmital Channel (Figure 1), in a typical currently mangrove ecosystem, with range since 1630 year BP (França et al., 2019).

Facies association

The mangrove ecosystem and coastal environment in Babitonga Bay were reconstructed using a combination of paleoecological indicators consisting of stratigraphical analysis, pollen analysis, and radiocarbon dating. The SF6 record is divided into three facies association according to the main changes in palynological composition based on the cluster analysis and stratigraphic profile (Figure 4): subtidal flat (A), mixed intertidal flat (B), and muddy intertidal flat (C).

Figure 4.

Summarized results for SF6 core, with variation in core depth showing chronological and lithological profiles with sedimentary facies, as well as ecological pollen groups.

Facies association A (subtidal flat)

This facies association (FA), characterized by FA-A1 and FA-A2 (Figure 4), corresponds to the lower core section of 200 -140 cm, accumulated before 1441 ± 81 until around 1258 ± 32 cal. year BP. It consists of coarse to medium sand deposits, with massive deposits (Sm) and some cross-laminated sand levels (1.9 m depth), presenting a fining upward succession. Fragments of leaves, roots, and shells are present. Samples from facies association A contain the lowest pollen concentrations. This zone is further divided into Zone A1 (200–180 cm; ±1440–1390 BP) and Zone A2 (180–140 cm; ±1390–1286 BP), according to the changes in vegetation composition (Figure 4). In Zone A1 pollen analysis revealed three ecological groups: herbs (18%–40%), trees, and shrubs (50%–70%) and palms (3%–22%). No mangrove pollen is counted in Zone A1 (Figures 4 and 5). In Zone A2 mangrove pollen was found represented only by Laguncularia (0%–3%) (Figure 4). Herbs were mainly represented by Poaceae (7%–27%), Asteraceae (3%–15%), and Cyperaceae (0%–5%). Tree and shrubs were mainly represented by Euphorbiaceae (1%–22%), Myrtaceae (3%–14%), Fabaceae (2%–9%), Myrsine (2%–8%), and Moraceae (0%–9%) (Figure 4).

Figure 5.

Pollen diagram record for SF6 core, with percentages of the most frequent pollen taxa, samples age, zones, and cluster analysis.

Facies association B (intertidal flat with Laguncularia and Avicennia)

Facies association B (FA-B) corresponds to the depth interval from 140 cm (±1286 years BP, extrapolated age) to 65 cm (±431 years BP), according to Figure 4. The deposits are characterized by silty-sandy and silty-clayey sediments, distributed in layers with heterolitic flaser stratification (Hf), wavy heterolitic stratification (Hw), lenticular heterolitic stratification (Hl), and massive layers. In addition, plant/trunk and shell fragments can be identified. Four ecological groups were identified (Figures 4 and 5), represented by herb pollen (13%–42%), trees and shrubs (45%–67%), palms (10%–19%), and mangroves (0%–3%), characterized by Zone B. Tree and shrubs were mainly represented by Euphorbiaceae (7%–18%), Myrtaceae (4%–10%), Fabaceae (3%–10%), Myrsine (3%–7%), and Moraceae (2%–9%). Herbs were mainly characterized by Poaceae (4%–22%), Cyperaceae (0%–5%), Asteraceae (6%–9%), Amaranthaceae (0%–3%), and Borreira (±1%). The mangrove is represented initially by Laguncularia (0%–3%), and later by Avicennia (0%–2%) at around 135 cm.

Facies association C (intertidal flat with Laguncularia, Avicennia and Rhizophora)

This facies association (FA-C) constitutes the substrate deposits from 65 cm (±431 cal. year BP) to the surface (Figure 4). These deposits consist of silty-clayey sediments with massive stratification, and deposits with sand lenses. Plant fragments are present. Compared to FA-B, we observe a decrease in trees and shrubs (56%–63%), herbs (23%–32%), palm trees (5%–12%), and spores (Zone C, Figure 4). The mangrove is mainly composed of Laguncularia (0%–3%), with the presence of Avicennia (1%) and Rhizophora (1%) on top. Tree and shrubs were mainly represented by Euphorbiaceae (5%–14%), Myrtaceae (3%–14%), Fabaceae (2%–6%), Myrsine (1%–7%), and Moraceae (2%–9%). Herbs were mainly characterized by Poaceae (12%–34%), Cyperaceae (3%–6%), Asteraceae (3%–9%), Amaranthaceae (0%–2%), and Borreria (±1%).

Interpretation and discussion

Dynamic vegetation and coastal morphological change

The vegetation and coastal environment in Babitonga Bay were studied using a combination of paleoecological indicators, including stratigraphic analysis, pollen analysis, and radiocarbon dating (C-14). Our data show a progradational fining upward succession where a mangrove-inhabited tidal flat was developed on the Palmital Channel margin during the late-Holocene (±1440 years BP to present, see Figure 6).

Figure 6.

Paleoenvironmental reconstitution of the northeastern margin of the Palmital Channel, Babitonga Bay (southern Brazil). From a to d, the blocks show the evolution of the study area.

The first phase (Figure 6), at the base of the SF6 core (FA-A1 and FA-A2, 1441 ± 81, and ±1286 cal. year BP), is characterized by massive, cross-stratified sandy deposits. These deposits are formed in medium to high-energy environments, where high-flow energy induces the migration of sand waves and sandy sheets under unidirectional flow (Reineck and Singh, 1980). The layers transition from coarser to finer sand, indicating a gradual decrease in current energy. This section can be interpreted as a sandbar of a tidal channel that was exposed to gradually diminishing flow energy. The pollen record revealed that initially the estuary margin was occupied by herbs, palms, trees, and shrubs (Figures 4 and 5). However, since ±1390 year BP the presence of mangrove vegetation (specifically Laguncularia) was recorded, indicating that environmental conditions became favorable for its development in the vicinity of the SF-6 sampling site. Laguncularia normally cover tidal planes pioneering on southern Brazilian coastal region (Cohen et al., 2020; França et al., 2019; Soares et al., 2012), due to a faster recovery to physiological adaptions, for instance shade intolerance, high photosynthesis rates, and salinity tolerance (Twilley et al., 1999).

The second phase is characterized by the deposition of heterolithic sediments as a result of alternation between suspension and traction processes (Figure 6), indicating the development of an intertidal environment in the study area, where the regular low-energy tides favored mud deposition (Dalrymple et al., 2003). Thus, the beginning of the intertidal flat in the study area is marked by favorable conditions such as muddy substrate allowing the expansion of the mangrove forest. This phase was characterized by the establishment of Avicennia trees around ± 1273 years BP, together with the presence of Laguncularia, presenting continuity throughout this succession. Therefore, during this period, the mangrove forest of Laguncularia and Avicennia expanded on the tidal flat previously colonized by herbs. The mangrove colonization and sediment succession indicate that the coastline reached a similar level to the present, which may be related to the sea level fall at the end of the Holocene and its stabilization registered around 1000 year BP (Angulo et al., 2006), as well as the natural vertical accumulation of sediments contributing to the formation of the tidal flat and mangrove expansion. Additionally, there was an increase in fern spores, a typical indicator of freshwater environment (Rodrigues et al., 2022), suggesting a greater freshwater influence in the estuary. There was also a higher concentration of pollen grains, mainly from trees, shrubs, and palms, and a lower percentage of herbs, likely indicating warmer and more humid conditions. Mainly tree pollen record shows forest expanding, indicating wetter and warmer conditions (Behling et al., 2002; Portes et al., 2020).

The most recent phase is characterized by the accumulation of muddy sediments, with some sandy levels on the intertidal flat, resulting from medium and low energy flows. These sediments occur in massive layers with higher organic matter content. The concentration of pollen grains was slightly lower than in the second phase, mainly from palms, trees and shrubs, and mangroves, mainly Avicennia, and an increase in the percentage of herbs. However, at the top of the core, mangrove expansion was again observed with the establishment of the Rhizophora in recent decades. This final phase as well as the second phase is the result of the drop and stabilization of the relative sea level (Angulo et al., 2006, 2022; Pereira et al., 2023), allowing for continuous sediment accumulation, and the expansion of Rhizophora was likely favored by recent climatic changes, with warming for Southern Brazil in the minimum temperature range at annual timescales (+0.5 °C per decade) and in winter (+0.4 °C per decade), for instance between 1960 and 2002 (Marengo, 2006; Marengo and Camargo, 2008).

The analysis of a sediment core (SF1), collected in a tidal flat 10 km downstream from SF6 in the Palmital Channel, conducted by França et al. (2019), revealed the development of the same mangrove succession found in core SF6 (Figure 4). However, stratigraphic and pollen data indicate that during the first phase, spanning at least from 1815 ± 74 to ~1630 cal. year BP (SF1 core), no mangroves were recorded at the study site, despite the marine influence and adequate accumulation of muddy sediments during this period. The estuarine margin was occupied by herbs, palms, trees, and shrubs. In later stages, after ~1630 cal. year BP, Laguncularia became established in the intertidal flat, followed by Avicennia approximately 853 ± 44 cal. year BP. Finally, Rhizophora became established in recent decades. The temporal difference of approximately 240 years for mangrove establishment between SF1 and upstream of the Palmital Channel in SF6 suggests that the mangrove migrated toward upstream areas that eventually reached favorable conditions for its development, mainly considering the greater abundance and biomass. Therefore, the expansion of mangroves, greater abundance, in the Palmital Channel region was likely favored by the geomorphological and physicochemical conditions of the substrate, related to the decrease in relative sea level and recent climatic changes. Therefore, considering especially the climate changes that affected the mangrove forests during the late-Holocene, the mangroves have probably responded to Holocene air and water warming (França et al., 2019), because that ecosystem has better development in regions with mean temperature above 20ºC and the annual thermal amplitude less than5ºC (Chapman, 1975; Tomlinson, 1986).

Sea-level changes and mangroves

The change in sea level is a fundamental driver in coastal dynamics and mangrove ecosystems. The relative impact of this factor on vegetation and the coastal system depends on the specific characteristics of the study site, such as geomorphology, sediment supply, and tidal and fluvial action (Cecil, 2013; Roe and van de Plassche, 2005; Woodroffe and Murray-Wallace, 2012).

In the northern region of Santa Catarina, southern Brazil, it has been estimated that during the Holocene, the maximum sea level reached approximately 2.1 m (Angulo et al., 2006), according to Figure 7. It remained stable for several centuries, between 5800 and 5000 cal. year BP (Martin et al., 2003), and then gradually declined to the present level (Angulo et al., 2006). During the late-Holocene, the sea level was between 0.6 and 0.9 m above the current sea level (Angulo et al., 2006; Chua et al., 2021; França et al., 2019; Milne et al., 2005; Tam et al., 2018).

Figure 7.

Sea-level envelope for the Brazilian coast south during the Holocene, according to Angulo et al. (2006), with comparative pollen diagrams from Subtropical mangroves, and comparison of facies associations between core SF6 (this study) and SF1 (França et al., 2019).

Isotopic analysis and organic matter studies conducted in SF1 suggest a higher marine influence in this area before ± 1815 cal. year BP (França et al., 2019). Furthermore, a study involving diatom analysis in a sediment core collected from the right margin of the Palmital Channel near SF6 also revealed a greater marine influence in that region during this phase of the late-Holocene (Figures 6 and 7), and also according to Rodrigues et al. (2022). Therefore, the analysis of the stratigraphic succession in the present study likely reflects the scenario of relative sea level fall in the southern region of Brazil during the late-Holocene. The relative sea level drop in the study area is estimated to have occurred during the late-Holocene (Angulo et al., 2006), resulting in the development of an intertidal flat colonized by mangroves.

The data from the study site suggests that this was a submerged zone until ±1286 year BP (Figures 6 and 7). Likely, the coastline was further inland due to a higher relative sea level than the current one. The pollen record in SF6 indicates that mangrove colonization in the area began during the first phase at ± 1390 years BP (180 cm depth) with Laguncularia trees. This indicates that, despite being a submerged area, Laguncularia was colonizing areas near the SF6 point, leaving a pollen record. According to the analysis in SF1, before ±1286 year BP, Laguncularia trees had already colonized the downstream area of the Palmital Channel. In the SF1 area, a well-developed tidal flat with estuarine conditions already existed, facilitating the establishment of mangroves. Therefore, the presence of Laguncularia pollen in SF6 before the development of the tidal flat at this point indicates that, with the gradual fall in sea level, the physicochemical conditions of the substrate and the geomorphology of the terrain favored upstream migration of the Palmital Channel (França et al., 2019; Rodrigues et al., 2022).

As the relative sea level falls, changes occur in the topography and hydrodynamics of the estuary, resulting in increased sediment accumulation and the formation of more suitable areas for mangrove establishment, as well as to increase in accommodation space. The decrease in relative sea level also exposes previously inundated areas, creating new surfaces for mangrove seedlings to settle and take root. Many mangrove species are tolerant to low salinities and can colonize areas with less marine influence (Menezes et al., 2008). This decrease in salinity may be due to the reduced intrusion of seawater resulting from the decrease in sea level and changes in water flow patterns in the estuary (Xie et al., 2022).

Laguncularia is usually associated with sandy substrate areas in coastlines influenced by low salinity water (Schaeffer-Novelli et al., 2000), but it can also develop in muddy substrates, and its predominance is conditioned to early or middle stages of mangrove succession (Kilca et al., 2010; Menghini, 2004; Soares, 1999). Therefore, it is likely that Laguncularia, the least salt-tolerant species, establishes first in upper estuary areas where freshwater outflow from rivers exerts a much greater influence than Atlantic Ocean water, and gradually colonized upstream of the Palmital Channel as the relative sea level declined. After the fall and subsequent stabilization of the sea level, the species extended to previously submerged areas or tidal flats with lower marine influence. The increase in fern spores, a typical indicator of freshwater (Rodrigues et al., 2022), suggests an increase in freshwater influence on the environment.

Mangroves succession and temperature

Considering climatic factors, studies have shown that temperature can act as a limiting factor for the development and distribution of mangroves in subtropical latitudes (Alongi, 2015; Osland et al., 2016; Quisthoudt et al., 2012; Stuart et al., 2007). Particularly, the increase in temperature during the late-Holocene and Anthropocene has been demonstrated to have a significant effect on facilitating the colonization of mangrove species toward more subtropical latitudes (Cohen et al., 2020). The temperature increase creates more favorable conditions for the survival and growth of mangrove species in these areas. Mangrove trees exhibit different temperature ranges and salinity tolerance (Quisthoudt et al., 2012) and develop on different substrate types. In a typical succession where the temperature is not a limiting factor trees of the genus Laguncularia are the first to be established on sandier substrates. This creates hydrodynamic conditions for the accumulation of mud that allows Rhizophora trees to colonize the area. Subsequently, this sediment accumulation creates conditions of low-frequency tidal inundation and relatively high salinity, ideal for the growth of Avicennia trees (Tomlinson, 1986).

In the study area, the establishment of Laguncularia in the intertidal flat created suitable conditions for mud deposition, which allowed the establishment of Avicennia. Rhizophora was only identified in the upper part of the studied core. This species is mainly wind pollinated (Kathiresan and Bingham, 2001), and its pollen is often abundant and outnumbered compared to pollen from other genera (Li et al., 2008; Somboon, 1990). Thus, the presence of Rhizophora pollen in the upper part of the stratigraphic profile studied indicates recent colonization of the Palmital Channel area, as suggested by França et al. (2019) in their study of SF1 core.

The mangrove succession found in the study area follows the temperature gradient, as Avicennia and Laguncularia have higher cold tolerance than Rhizophora (Stuart et al., 2007). Therefore, we believe that the establishment and expansion of Laguncularia, along with Avicennia and Rhizophora in the Babitonga Bay, were due to the trend of rising temperature during the late-Holocene, which has led to mangrove migration toward southern latitudes along the Brazilian coast.

In this context, we conclude that the mangrove succession developed in Babitonga Bay followed a temperature gradient because of climate change related temperature increase during the late-Holocene. Furthermore, the migration of mangroves in Babitonga Bay occurred because of sea-level fall during the late-Holocene, gradually creating a favorable substrate for mangrove development.

Factors influencing Holocene sub-tropical mangrove expansion along the southern Brazilian coast

On the Brazilian coast, the spatial distribution of mangroves during the Holocene was mainly controlled by climate variations, river flow, and sea level fluctuations (Cohen et al., 2012; Ellison, 2008), causing changes in depositional systems and mangrove areas (Amaral et al., 2012; Cohen et al., 2005; Do Amaral et al., 2006; Guimarães et al., 2012; Prado et al., 2013; Quisthoudt et al., 2012; Scheel-Ybert, 2000; Smith et al., 2012). During the late-Holocene, the relative sea level gradually decreased along the southern Brazilian coast (Angulo et al., 2006). This resulted in coastal progradation with mangroves at subtropical latitudes. However, only after approximately 2200 cal. year BP, subtropical mangroves became established, despite similar trends in relative sea-level changes for both tropical and subtropical coasts of Brazil (Cohen et al., 2020; França et al., 2019; Pessenda et al., 2012; Rodrigues et al., 2022). A core sampled from the São Paulo coast (400 km north of the study area) recorded mangroves in marshes at least since ~2200 cal. year BP (Pessenda et al., 2012). Mangroves in the northern coast of Santa Catarina were established around ± 1630 year BP (França et al., 2019) and expanded to reach the current southern limit of South American mangroves in Laguna, southern Santa Catarina, in recent decades (Cohen et al., 2020) (Figure 5). The establishment of these subtropical mangroves followed a migration pattern similar to that found in the study area in SF6, where Laguncularia trees were the first to establish, followed by Avicennia and then Rhizophora. The density of Rhizophora trees decreases southward until they are completely absent at the current limit of South American mangroves (Soares et al., 2012; Yao et al., 2022). This distribution of mangrove genera along the subtropical coast suggests a gradual tolerance to low winter temperatures, where Laguncularia would be more tolerant and Rhizophora less adapted to low winter temperatures. The chronological difference between the establishment of Laguncularia and Avicennia may have been caused by the different physiological adaptation to more frequent winter freezing events at higher latitudes between the two species (Osland et al., 2016; Rodrigues et al., 2022), as Avicennia does not germinate if the sea-surface temperature (SST) is below 15°C, but Laguncularia propagules can survive under SST below 15°C (Oliveira, 2005). Therefore, the migration of the southern limit of the mangrove to more temperate zones is a result of the warming trend during the late-Holocene.

Late-Holocene warming may be associated with the Medieval Climate Anomaly (MCA, 1050-850 years BP) and the Current Warm Period (CWP, last ± 100 years) (Novello et al., 2012; Vuille et al., 2012). In addition, several records point to an increase in SST in the South Atlantic Ocean (Chiessi et al., 2014), especially during the middle and late-Holocene that may be related to changes in insolation distribution (Santos et al., 2013). In recent centuries, human-induced greenhouse gas concentrations have gradually increased (Kaufman et al., 2020; Marengo, 2006), contributing to a temperature increase of approximately 1°C in global temperatures (Kaufman et al., 2020; Marengo, 2006) compared to pre-industrial levels (Allen et al., 2018). Additionally, studies indicate that global minimum temperatures have been increasing faster than maximum temperatures (Easterling et al., 2000; Walther et al., 2002). This temperature change has been observed in southern Brazil, where the frequency of low-temperature events has decreased (Soares et al., 2012). Therefore, it is likely that the recent establishment of Rhizophora in the region was favored by the temperature increase caused by the Current Warm Period (CWP, since the early 20th century).

Currently, the global temperature is rising at an alarming rate of 0.18°C per decade since the early 1980s (Dunn et al., 2020), leading to changes in biome distribution worldwide (Pecl et al., 2017). This temperature increase has caused the melting of the polar ice sheets in Greenland and the Antarctic (Shepherd et al., 2020) thus accelerating the current sea-level rise (Oppenheimer et al., 2019). In Brazil, studies have revealed that coastal regions exhibit a higher proportion of positive temperature anomalies (Bernardino et al., 2015), and estimates by Marengo (2006) indicate a temperature increase of 3°C–5°C by 2080 because of increasing greenhouse gas concentrations.

As a result of modern climate change and sea level rise, we believe that mangroves along the Brazilian coast may migrate inland and expand toward higher latitude coastal regions. These processes may gradually replace herbaceous vegetation on tidal flats if suitable and favorable habitats exist for mangrove colonization. However, further studies are still needed in order to determine the mangrove dynamics in the Babitonga Bay during the Holocene, as proposed in previous publications (e.g. Azevedo et al., 2021; França et al., 2019; Rodrigues et al., 2022), mainly considering more sediment cores to provide the coastal paleoenvironmental reconstruction.

Conclusions

Sedimentary, pollen, and C-14 analyses of the SF6 core allowed the paleoenvironmental reconstitution in the Palmital Channel, Babitonga Bay (SC) during the late-Holocene. Three facies associations were identified, indicating a progradational succession where a tidal flat developed on the margin of the Palmital Channel. During the first phase, between at least 1440 and ±1286 cal. year BP, the area was characterized by a subtidal environment. The presence of Laguncularia pollen grains since ± 1390 cal. year BP indicated favorable conditions for mangrove establishment in proximity to the study site. Subsequently, around ± 1286 cal. year BP, the tidal flat developed, reaching the present-day shoreline, facilitated by the relative sea level drop. Avicennia trees were established on the tidal flat since ± 1273 cal. year BP, and the establishment of Rhizophora trees occurred in the most recent decades. The mangrove succession found was likely favored by the temperature increase during the late-Holocene that caused a migration of the southern limit of the mangrove in the subtropical zone to higher latitudes. In addition, a comparison between our palynological data and those obtained from the SF1 core in a previous study revealed the development of the same mangrove succession, but in this core the colonization of the mangrove with Laguncularia began around ±1630 year BP. The difference in colonization time suggests that the mangrove migrated to areas upstream of the Palmital Channel controlled by suitable salinity and substrate conditions, which were favored by the relative sea level during the late-Holocene.

Footnotes

Acknowledgements

We want to thank the members of the Laboratory of Coastal Dynamic (LADIC/UFPA), Laboratory of Oceanography and Climate (LAOC/Ifes-Campus Piúma), and C-14 Laboratory (CENA-USP) for their support. This research received support from the resources of the project “EFFECTS OF CLIMATE CHANGE ON THE DISTRIBUTION OF MANGROVES IN SOUTHERN BRAZIL” (Process 445111/2014-3/CNPq), Espírito Santo Research and Innovation Support Foundation-FAPES (282/2021; 2021-X7HT9), São Paulo Research Foundation-FAPESP (2020/13715-1), Brazilian Council for Technology and Science-CNPq (Project 403239/2021-4), and in part by the Coordination of Superior Level Staff Improvement, Brazil (CAPES), Federal Government Agency under the Ministry of Education (Finance Code 001). The second author would like to thank CNPq for research scholarship (309618/2020-7). We also thank Dr. Luiza S. Reis for her assistance.

Data availability statement

All data generated or analyzed during this study are included in this published article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Espírito Santo Research and Innovation Support Foundation-FAPES (282/2021; 2021-X7HT9), São Paulo Research Foundation-FAPESP (2020/13715-1), Brazilian Council for Technology and Science-CNPq (Projects 309618/2020-7 and 403239/2021-4), Coordination of Superior Level Staff Improvement, Brazil (CAPES), Federal Government Agency under the Ministry of Education (Finance Code 001).

ORCID iDs

Angela EC Torres

Marlon C França

Kita Macario

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