Biota of the Patos Lagoon estuary and adjacent marine coast: long-term changes induced by natural and human-related factors

In this Thematic Issue (TI) we present new results obtained in the framework of the Brazilian Long Term Ecological Research (BR-LTER) Programme for the Patos Lagoon estuary (PLE) and the adjacent marine coast in southern Brazil. The BR-LTER was established in 1997 and the rationale for the conception and delineation of the initial projects was based on previous knowledge of the ecosystems. Since the end of the nineteenth century, the high biological productivity and ecological complexity together with human interference have been recognized in the PLE (Von Ihering 1885). The favourable natural conditions promoted the development and led to the increased importance of economic activities associated with fisheries, the harbour and industrial growth up to the present time. In 1978, the Oceanography Base (currently the Institute of Oceanography) was established at the Federal University of Rio Grande, and since then biological and oceanographic systematic studies have been conducted in the estuary and on the continental shelf. Seeliger et al. (1997) synthesized results gathered over almost 20 years, and now we can present the state-of-the-art science on long-term changes induced by the natural and human-related factors in the PLE and the adjacent marine coast.

It is widely recognized that long-term information in subtropical and tropical environments, specifically, is deficient in the southern hemisphere and this represents a caveat that limits the achievement of a global synthesis about the biological variability and dynamics of aquatic ecosystems. Our purpose with this TI is to provide information on the long-term ecology of a coastal ecosystem located in the subtropical region of the southern hemisphere, at latitude 32°S, considering different components of the complex food web in this ecosystem. In the present issue, 10 original articles and one review article evaluate the mesoscale and long-term variability of primary producers such as micro- and macroalgae, consumers of low (e.g. zooplankton, ichthyoplankton, pink-shrimp, fishes) to high (fishes, birds, marine mammals) trophic levels and the effects of fisheries on the abundance and population dynamics of exploited species in the PLE and the adjacent marine coast. Altogether, this unprecedented information points to the importance of the large-scale climatic phenomenon El Niño Southern Oscillation (ENSO) on the functioning of the estuarine ecosystem, and contributes to the prediction of possible responses to future climate changes and to the conservation of coastal ecosystems. Moreover, it was observed that human-induced impacts played an important role in changing the community structure and dynamics in this environment. This information provides a better understanding of a complex coastal ecosystem in the southern hemisphere, and therefore helps to form consistent scenarios and hypotheses of the functioning of coastal ecosystems around the world.

Figure 1. Morning mood in the Patos Lagoon estuary in austral autumn (28 May 2014). Note the fisherman (left background) working with his fyke nets used for shrimp capture, while herons and gulls (Egretta thula (Molina, 1782), Ardea sp. and Chroicocephalus sp.) can be seen resting on poles on the right and on the water surface behind. Photographer: Franz Uiblein.

The Patos Lagoon (10,360 km²) is the receptor of an extensive watershed, the Patos-Mirim Lagoon system (≅ 200,000 km²) shared between southeastern Brazil and northeastern Uruguay in subtropical eastern South America. Due to the positive rainfall–evaporation water balance in the large watershed area, the larger part of the Patos Lagoon is predominantly fresh to oligohaline, with a high sediment load (Möller et al. 1996; Odebrecht et al. 2005). The estuarine region, with an area of 900 km², is located in the southernmost part of the Patos Lagoon. Most of the estuary (≅ 90%) is shallow, with a depth less than 2 m (Figure 1). Water exchange between the estuary and the coastal region occurs through a narrow channel and fluxes are mainly controlled by wind and rainfall, because tides are of small amplitude (40 cm). The adjacent marine coast presents a gentle slope and wide continental shelf, and it is strongly influenced by freshwater run-off from the Patos Lagoon and Rio de La Plata (Ciotti et al. 1995; Campos et al. 2008; Pimenta & Kirwan 2014). The oceanic beaches in this region are intermediate to dissipative with regard to wave energy and are characterized by the accumulation of surf-zone diatoms that produce an enormous biomass, especially following the passage of atmospheric fronts (Odebrecht et al. 2010a).

In the PLE, the primary producers are phytoplankton, benthic micro- and macroalgae and seagrasses, and they guarantee an important carbon contribution to the very productive food web, resulting in important fishery activities in the estuary and adjacent marine coast. The availability of light and nitrogen nutrients, but also predation, influences the estuarine primary producers. However, meteorological and hydrological forces such as the action of winds and rainfall cause most of the variability observed in the short, medium and long timescales. It was observed that the remote phenomenon ENSO strongly influences interannual variability of planktonic and benthic primary producers in the PLE, because during El Niño years the amount of rainfall increases considerably in the region and consequently the water flow from the estuary towards the coast (Odebrecht et al. 2010b). The opposite is observed during La Niña years, when drought conditions prevail in Southern Brazil, favouring the input of salt water into larger areas of the lagoon.

Information on phytoplankton variability in the PLE was mainly obtained at one station located in a shallow embayment (Abreu et al. 2010; Haraguchi et al. 2015). In the scope of the BR-LTER project in the Patos Lagoon and adjacent coastal waters, phytoplankton data are also obtained from the main navigation channel and the surf-zone of Cassino Beach. All three stations are no more than 10 km apart and are supposed to be subject to the same main forcing functions. In this TI, Abreu et al. (2017) conduct, for the first time, a comparative analysis of the phytoplankton chlorophyll a variability collected monthly over 22 years at the three stations. Despite the close proximity of the three stations, the authors observed distinct chlorophyll a patterns, with seasonal cycles out of phase between the estuarine and beach stations. In general, it is observed that meteorology/hydrology exert strong and localized effects on phytoplankton biomass. Such influences of the hydrology seem to surpass other forcing functions, such as light and temperature, which should influence the phytoplankton present at nearby stations in a similar way.

The study by Abreu and collaborators also demonstrates that the ENSO influences the three stations. However, what is noteworthy is the fact that the effects caused by excess (El Niño) or lack (La Niña) of rainfall last for some time until phytoplankton chlorophyll a reaches levels similar to those prior to the impact. Finally, the authors also show an interesting connectivity among the three stations with the transference of phytoplankton, mainly the surf-zone diatom Asterionellopsis guyunusae Luddington, from the coastal region towards the estuary, in an ‘inverted outwelling’ process.

In long-term studies, the use of technologies that allow the acquisition of data at low cost is an important issue. In phytoplankton studies, high-cost and time-consuming analyses are involved in species quantification and identification, requiring the dedication of trained personnel. The maintenance of such specialized professionals is even more difficult in long-term studies. Thus, the pigment-based taxonomic study in the PLE presented by Mendes et al. (2017) in this TI is very welcome. The authors compare the phytoplankton composition collected monthly over three years at the same three stations as the previous study, distributed between the estuary and the adjacent marine coast. Samples are evaluated simultaneously by light microscopy and high-performance liquid-chromatography (HPLC) pigment analysis, and the pigment composition was evaluated with CHEMTAX software, providing information on the phytoplankton composition. Both methods show good agreement in the determination of phytoplankton groups. For instance, CHEMTAX is able to reproduce the predominance of diatoms at the three stations, as well as the contribution of cryptophytes and of dinoflagellates. Poor agreement between the methods for cyanobacteria and green algae might be due to an underestimation by the microscope-based technique in samples with a large amount of detritus. However, the pigment analysis applied here allowed reliable tracking of the main changes in the general phytoplankton composition throughout the study period, proving to be an important and appropriate tool for long-term studies.

Ephemeral macroalgal blooms have been increasing in frequency and abundance worldwide and the macroalgal abundance found in the PLE is comparable to that in temperate eutrophic lagoons. In this TI, the influence of climate and hydrology on the onset and magnitude of drift macroalgal blooms in the PLE is investigated by Lanari & Copertino (2017) over three growth cycles, from January 2004 to May 2007. The authors show that the magnitude and persistence of macroalgal spring and summer biomass varies largely both on the annual and interannual scales. On an annual scale, macroalgal blooms, consisting mostly of Ulva species, follow the reduction in freshwater discharge, the lowering in water level, and the increase in salinity and water retention in the estuary. These hydrological parameters are controlled by precipitation, which is in turn affected by the ENSO, leading to interannual variability. At this scale, the largest blooms observed during a weak to moderate El Niño year coincided with a trend of increasing phosphorus concentration. It is also shown that the action of wind affects algal transport and distribution in shallow areas, thereby controlling the magnitude and persistence of the blooms under favourable growing conditions.

The zooplankton of estuarine regions plays an important role in transferring energy and matter from the planktonic primary producers to organisms of higher trophic levels. However, due to methodological constraints, little information is available about the zooplankton secondary production, especially with continuous measurements over time. In this TI, Teixeira-Amaral et al. (2017) present results of monthly measurements of zooplankton secondary production over four years at two stations in the PLE and identify large changes in the secondary production levels related to modifications in the hydrology. The highest secondary production values (1.17 mg C m⁻³ day⁻¹) are mainly associated with the calanoid copepod Acartia tonsa Dana, 1849 in salt/brackish water. However, changes in the hydrology of the PLE, with the input of fresh water, lead to the massive presence of the freshwater copepod Notodiaptomus incompositus (Brian, 1925) and a reduction in the secondary production level to 0.13 mg C m⁻³ day⁻¹. These changes represent relevant information on the ecology of this ecosystem, considering that the hydrology of the PLE is highly influenced by the ENSO, which generates a dominance of fresh water in the region during El Niño years as a consequence of higher rainfall levels in the watershed, and the opposite, i.e. a dominance of salt water during La Niña years. Thus, changes in the hydrology with increased rainfall may lead to a decrease in energy transfer through the estuarine food web, affecting the whole ecosystem functioning with repercussions to fisheries.

The PLE is an important nursery ground for many species that are relevant for the Brazilian fisheries. Here, Noleto-Filho et al. (2017) examine the spatial and temporal variation in size distribution of the pink shrimp Penaeus paulensis (Pérez Farfante, 1967), a species that represents 40% of fisheries landings in southern Brazil, to assess whether long-term exploitation of the shrimp stock has resulted in the erosion of large size classes. Furthermore, they investigate whether the size distribution of shrimps in this estuary is influenced by the unpredictability of environmental shifts that could change the life strategy during the recruitment process. With a 16-year time series, they show the influence of the dynamics and variable nature of saltwater penetration and freshwater discharge on a nearly unpredictable size distribution pattern. Despite the erratic nature in size distribution, regions are distinguished by greater size diversity and thus favourable for catching large-size individuals from regions with a high frequency of small individuals, which should be considered when establishing restricted fishing areas. The long-term analysis of size structure indicates a decrease of approximately 25% in the mean size of pink shrimp after the first four years of the survey, suggesting overexploitation of this species in the region and that fishery is removing an important fraction of the population. The conservation of large individuals and the establishment of restricted areas is vital for the shrimp stock recovery and an important step towards conservation of the PLE.

Conservation management strategies must incorporate the high spatial and temporal variability and the dynamic features of estuaries to be efficient. In this TI, Costa & Muelbert (2017) use long-term information on temporal variability to assess whether distinct spatial patterns of fish egg and larval distribution can be helpful to conservation planning. As demonstrated by Noleto-Filho and collaborators (also see above) for the pink shrimp larvae, fish eggs and larvae also exhibit high variability, but their temporal occurrence and spatial distribution are mainly associated with salinity. Fish eggs and larvae in the PLE present distinct spatial patterns that are different between years and characterized by the dominance of distinct genera. Costa and Muelbert demonstrate the importance of such information in supporting management decisions about which species and temporal scale should be studied in detail and incorporated in environmental planning. Spatial conservation planning incorporating fluctuations in abundance and assemblage structure over time may help to ensure conservation for biodiversity persistence in highly dynamic ecosystems such as the PLE.

Conservation planning may also benefit from a better understanding of the seasonal spatial shifts of the nektonic assemblages. In this TI, Martins & Haimovici (2017) present a novel pattern of mesoscale seasonal shifts of teleost fish and cephalopod assemblages along the shelf and upper slope of southern Brazil. Along the SW Atlantic, coastal and shelf environments are influenced by the freshwater run-off of the La Plata River and Patos Lagoon, which produce large areas of sand and mud bottoms and of low-salinity water. The authors reveal four consistent groups with the dominance of sciaenid fishes: coastal, warm-shelf, cold-shelf and upper-slope assemblages. These groups present characteristic temporal and spatial patterns of distribution, and significant changes in their composition. The warm-shelf and upper-slope assemblages are present year-round, whereas the cold-shelf assemblage occurs almost exclusively in the cold season, and the coastal assemblage expands toward the south in the warm season. Such information is crucial for determining seasonal or spatial fisheries closures in the region and for planning of marine protected areas.

The food assimilation of an omnivorous fish also shows temporal variation in the PLE, as demonstrated here by Garcia et al. (2017) using stable isotopes (δ13C and δ15N). The authors investigate intra- and interannual variability in trophic links between basal food sources (seagrass, macroalgae, saltmarsh, particulate organic matter in suspension and in the sediment) and the omnivorous fish Jenynsia multidentata (Jenyns, 1842). Basal food sources and the consumer were sampled seasonally, from 2010 to 2014, in a mudflat. Significant interannual variation is observed in the trophic links between J. multidentata and primary producers. In most seasons and years, consumers rely heavily on benthic-associated food resources, seagrass being the most assimilated benthic basal food source. However, shifts to pelagic food resources might occur during certain periods, as was observed in spring 2013. These results suggest that the intensity of benthic and pelagic trophic pathways sustaining estuarine consumers are not characterized by a static architecture in time, but rather, they can be dynamically driven by intra- and interannual variation in availability of basal production sources, which should be taken into account when modelling estuarine food web dynamics.

The bird assemblages of the upper and lower PLE and the adjacent marine coast are analysed by Dias et al. (2017). In addition, the main environmental factors determining variations in species richness along the limnetic–marine gradient are identified, changes in species composition along this gradient are evaluated and the role of the estuary for bird conservation is discussed. Overall, 268 bird species are detected at eight sites along the estuary. The species richness is similar in spring–summer (247 species) and autumn–winter (n = 244). Nevertheless, a strong seasonal component influencing bird composition due to migrants is observed. Species richness decreases markedly towards the lower estuary, where the number of threatened seabirds and shorebirds predominates. The avifauna of the upper estuary, on the other hand, is dominated by forest passerines and waterbirds. This study highlights the importance of estuaries for the conservation of birds, especially migratory sea- and shorebirds, and resident salt marsh dependent species.

In the last original article of this TI, Secchi et al. (2017) evaluate the long-term (35 years) and gender-related variation in the feeding ecology of common bottlenose dolphins (Tursiops truncatus (Montagu, 1821)) inhabiting the PLE and the adjacent marine coast of the western South Atlantic. The authors combine two analytical approaches, stomach content and stable isotope (δ13C and δ15N) analyses, and use these data to assess the magnitude of trophic overlap between males and females. The lack of variation in utilization of resources between sexes indicates that resource-sharing or potential competition might exist between males and females. In addition, the results show that bottlenose dolphins from this area are opportunistic feeders, confirming the plasticity of this species, which preys upon the most available demersal and demersal–pelagic teleost fish. Seasonal differences and long-term changes in diet are observed. The authors point out that long-term changes might be linked to fishing-related changes in fish abundance.

Fishing is one of the most important economic activities in the region surrounding the PLE, and as a consequence it is one of the main human-related drivers of environmental change in coastal ecosystems in southern Brazil. Changes in the life cycle, fisheries and management of the main fishing resources in PLE and adjacent coastal waters are the subject of the review by Haimovici & Cardoso (2017). Over recent decades, fish landings in Rio Grande have decreased by over 60%. The stocks of the large-sized, slow-growing catfishes Genidens barbus (Lacepède, 1803) and G. planifrons (Higuchi, Reis & Araújo, 1982), black drum Pogonias cromis (Linnaeus, 1766) and the guitar shark Rhinobatos horkelii Müller & Henle, 1841 collapsed in the early 1980s. The pink shrimp Penaeus paulensis stock was reduced due to intense fishing of subadults in the estuary and of adults at sea. Despite their resilience to intense fishing, sciaenids like the whitemouth croaker Micropogonias furnieri (Desmarest, 1823), the southern king weakfish Macrodon atricauda (Günther, 1880), the argentine croaker Umbrina canosai Berg, 1895 and the striped weakfish Cynoscion guatucupa (Cuvier, 1830), which together represent more than half of local marine fish landings, are overexploited. The pelagic migrant bluefish Pomatomus saltatrix (Linnaeus, 1766), the Lebranche mullet Mugil liza Valenciennes, 1836 and the blue crab Callinectes sapidus Rathbun, 1896 are at the limit of exploitation. Present enforcement has proven to be insufficient and intense fishing is still carried out by a large number of industrial and small-scale fishing boats. According to the authors, the future of the estuarine and coastal fishing resources is uncertain and the recovery of the large, long-living species of the higher trophic levels is unlikely. The recovery of these stocks will depend on diminishing the fishing pressure they have suffered in recent decades.

The collection of articles in this TI demonstrates the importance of long-term environmental data. Accurate description of changes in the ecosystem, robust monitoring of cycles and trends and adequate evaluation of the status of living resources for proper conservation strategies can only be achieved through long-term studies. The examples from the Patos Lagoon estuary presented in this TI should advance studies that are under way and encourage the implementation of new long-term research programmes.

Editorial board note

Cordial thanks to Sharon Appleyard, Kjellrun Hiis Hauge, and Ingo Wehrtmann, who recently left us as MBRJ subject editors, and a warm welcome to our new subject editors Paco Cardenas, Department of Medicinal Chemistry, Uppsala University, Sweden (Marine Sponges), and Audrey Geffen, Biology Department, University of Bergen, Norway (Fisheries and Coastal Management)!

Additional information

Funding

This research was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico [Proc. no. 403805/2012-0] and the Fundação de Amparo a Pesquisa do Rio Grande do Sul [Proc. no. 3122-2551/12-7].