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Systematic Review ARTICLE

Front. Mar. Sci., 09 May 2019 | https://doi.org/10.3389/fmars.2019.00237

Systematic Review of Fish Ecology and Anthropogenic Impacts in South American Estuaries: Setting Priorities for Ecosystem Conservation

  • Laboratório de Ecologia e Gerenciamento de Ecossistemas Costeiros e Estuarinos, Departamento de Oceanografia, Universidade Federal de Pernambuco, Recife, Brazil

Research on estuarine ecology in South America (SA) increased quali-quantitatively since the early 1980 in search of consistent recommendations for estuarine conservation. The most important ecological theory achieved is that the seasonal fluctuation of the salinity gradient creates an ecocline influenced by gradual changes between river-dominated to marine-like waters. Estuarine fish fauna adapts to these changeable abiotic characteristics, including the spatial, and seasonal bioavailability of dissolved oxygen and numerous pollutants. However, studies on the influence of the estuarine ecocline are still missing for key estuarine systems. This study provides an overview of fish ecology and anthropogenic impacts within estuarine systems of SA and discusses priorities for environmental conservation. Research on fish reached important conclusions regarding essential habitats and fish interaction with other biological and abiotic compartments over spatio-temporal settings, including conditions of severe anthropogenic impacts. These impacts are related to unplanned urban settlements, industrial estates, ports, damming of major rivers, dredging activities, and deforestation for extensive farming. Changes in estuarine morphology alter natural flows and lead to habitat losses, disrupting the ecocline and impairing fishes from moving among formerly connected habitats, especially earlier ontogenetic phases. In addition, industrial, urban, and farming activities often result in high loads of metals and persistent organic pollutants, organic enrichment and oxygen depletion. Moreover, plastic debris, a ubiquitous contaminant with sources on every human activity, including fishing, when fragmented into microplastics, become preferably concentrated in semi-enclosed environments, as estuaries. Metals, POPs and microplastics are actually asserted to be persistent. When in high concentrations, they become bioavailable to the estuarine trophic web through bioaccumulation, being biomagnified or biotransfered toward higher trophic level organisms, such as top predator fishes. Therefore, research on environmental quality and fish ecology must be based on robust sampling designs along the whole ecocline using long-term approaches. In addition, basic sanitation, co-management, an improved licensing system and scientifically-based risk assessments/monitoring for all sorts of enterprise are also urgent. These conservation priorities need to be in place before human-driven changes surpass the ecosystem's capacity to produce resources and maintain services.

Introduction

Estuaries are characterized by gradual changes between freshwater inputs and marine waters intrusion (Barletta et al., 2017a). The encounter of these two water masses creates zones of mixing and vertical stratification of various strengths. Such stratification results in a variety of abiotic habitats that function as boundaries defining different faunal communities, which are influenced mainly by the seasonal fluctuation of the salinity gradient as induced by diel tidal variation and river runoff. Thus, an ecocline can be defined as a “gradation from one ecosystem to another when there is no sharp boundary between the two” (Attrill and Rundle, 2002). Usually, these boundaries are freshwater-oligohaline/upper, mesohaline-mixoeuhaline/middle, and euhaline-hyperhaline/lower reaches (Day et al., 2012). Each of these reaches can actually move horizontally, advancing seawards according to increased rainfall patterns or upstream under tidal influence (Barletta et al., 2005). Moreover, the seasonal balance of dissolved oxygen, suspended solids, pollutants, and microbiological contaminants are also ruled by the estuarine ecocline and temperature variability (Barletta et al., 2017a). Not surprisingly, this ecocline is the strongest forcing structuring physico-chemical conditions and fish communities within any estuarine ecosystems (Barletta et al., 2008).

Human interventions, such as damming of major rivers and dredging of channels along the estuarine course, might weakens and even disrupt the ecocline, reducing the original ecological functions, impairing the sustainable use of estuarine resources and services (Blaber and Barletta, 2016). These modifications are also responsible for disrupting sediment flows, change bottom composition and impair freshwater flow seawards, leading to changes in habitat availability, biodiversity damages, and shifts in biogeochemical cycles of several chemicals and pollutants (Barletta et al., 2016, 2019). Moreover, entire river basins, estuarine courses, and adjacent coastal waters are subjected to the influence of industrial, urban and farming activities, which are responsible for high loads of wastewaters and solid wastes (Huang et al., 2014; Pereira et al., 2015). Thereby, plastic debris, metals, nutrients, POPs and emerging pollutants present high concentrations closer to their sources, usually urban settlements, industrial estaes, and farms. Their chemical behavior and bioavailability for fishes along the way to the sea are also influenced by the major annual water quality shifts. The solubilisation, speciation, sorption, precipitation, diffusion, advection, sinking toward sediments, complexation, and absorption by the estuarine food web is the result of the seasonal fluctuation of the estuarine ecocline. Overall, pollutants are entraped in estuaries when saline intrusion is great and flushed out to the sea when river runoff increases (Barletta et al., 2012, 2019; Lima et al., 2014). Metals, POPs and microplastics are all persistent in the environment. The bioaccumulation and biomagnification of metals and POPs (Lanfranchi et al., 2006; Cappelletti et al., 2015), as well as the trophic transfer of microplastics (Galloway et al., 2017) are common in estuarine trophic webs. In addition to habitat loss by water quality/volume changes and damming of major rivers, fishes are also subjected to fishing pressure and to compete for resources with introduced species, often resulting in decreased native fish biomass within estuaries (Neuhaus et al., 2016; Barletta et al., 2017b). Currently, it is asserted that if human-driven changes remain uncontrolled, estuaries may become increasingly vulnerable to co-working global changes (Costa and Barletta, 2016; Ríos-Pulgarín et al., 2016). However, despite these impacts, changes in local climate and hydrodynamic variability might contribute to reduce pollution through biodilution and transport of contaminants out of the system, especially during the rainy season, when river flow increases, in a process known as environmental homeostasis (Elliott and Quintino, 2007). On the other hand, systems that suffer with severe droughts may not be able to recover and will face long and lasting antropogenic modifications.

This work is an overview of estuarine fish research and anthropogenic influences on estuarine fishes and estuarine ecosystems of SA located in tropical, subtropical and warm temperate provinces (Figure 1 and Table 1; study areas are described as Supplementary Material). Whereas, the current knowledge of estuarine fish fauna are poorly understood in this continent, this review focused in the description of the available information on fish ecology and how human-driven contamination and modifications have affected several estuarine systems and fishes of commercial and subsistence importance. To gather and interpret all the relevant literature aiming at generating managerial information was a daunting task, but a unique opportunity to promote well-informed decision-making, especially considering the transition among environments from equatorial to temperate regimes (Costa and Barletta, 2016). However, the ecocline theory is hardly ever attempeted in most studies. Therefore, the review also discusses on how to work in favor of the seasonal fluctuation of the ecocline is important to understand the distribution pattern of dominant fish species and major contaminants along estuarine systems and food webs.

FIGURE 1
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Figure 1. Location and main conservation issues identified in South American estuaries. Tropical northwestern Atlantic [(1) Atrato River Delta; (2) Ciénaga Grande de Santa Marta Lagoon; (3) Orinoco River Delta]. North Brazil Shelf [(4) Amazon Estuarine Complex; (5) Curuçá Estuary; (6) Caeté Estuary]. Tropical southwestern Atlantic [(7) Parnaiba River Delta; (8) Potengi Estuary; (9) Goiana Estuary; (10) Itamaracá Estuarine System; (11) São Francisco River Estuary; (12) Paraguaçu Estuary; (13) Guanabara Bay; (14) Sepetiba Bay; (15) Santos Estuary]. Subtropical southwestern Atlantic [(16) Paranaguá Estuarine Complex; (17) Guaratuba Bay; (18) Babitonga Bay; (19) Laguna Estuarine Complex; (20) Patos Lagoon Estuary]. Warm temperate southwestern Atlantic [(21) Pando Sub-Estuary; (22) Río de La Plata Estuary; (23) Mar Chiquita Coastal Lagoon; (24) Bahía Blanca Estuary]. Tropical eastern Pacific [(25) Bahía Málaga Estuary; (26) Rio Palmar and Rio Javita Estuaries]. Temperate eastern Pacific [(27) Valdivia Estuary]. Source: Google Earth.

TABLE 1
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Table 1. Ecoregions, geographical regions, and total area of key estuarine systems in South America based on available published data.

Methods

To address fish ecology and environmental quality of SA estuaries into a single manuscript, we performed a vast scientific search aiming at collect the greatest amount of studies in estuarine systems of every coastal country sourrunding the continent. We compiled information of nearly 420 articles found in the databases Web of Science, Scopus, and Google Scholar.

Results

Western Atlantic Estuaries

Tropical Northwestern Atlantic

Ciénaga Grande de Santa Marta Lagoon: Colombian Caribbean Coast

A complete description on the influence of the seasonal fluctuation of the estuarine ecocline on fish assemblages is available encompassing two annual cycles of 1993–1994 and 1997 within the Ciénaga Grande de Santa Marta Lagoon (Rueda and Defeo, 2003; Figure S1). The most contrasting seasons (major rainy and major dry), were used as temporal factors to reveal a strong relation between salinity variability and fish density ruled by seasonal shifts. Three distinct assemblages were determined by the salinity gradient, changing from freshwater to marine-estuarine and marine assemblages (Rueda and Defeo, 2003). Eugerres plumieri, Diapterus rhombeus (Gerreidae), Micropogonias furnieri (Sciaenidae), Mugil incilis (Mugilidae), Cathorops spixii (Ariidae), Elops saurus (Elopidae), and Anchovia clupeoides (Engraulidae) were the most frequent species. Anchovia clupeoides typified the rainy season of 1997; Cathorops spixii and E. saurus typified the dry season; and M. incilis and M. furnieri the rainy season in both annual cycles. D. rhombeus and E. plumieri typified the dry and rainy seasons of 1993–1994 (Rueda and Santos-Martínez, 1999; Rueda and Defeo, 2003). The highest densities of E. plumieri and M. incilis; and a peak of C. spixii occurred during the rainy season, near the opening of the lagoon (Rueda, 2001).

Regarding biological studies, the feeding ecology of A. clupeoides (Duque and Acero, 2003) and Oligoplites spp. (Carangidae) (Duque-Nivia et al., 1996) were described using spatio-temporal patterns along the salinity ecocline. The reproduction of Bairdiella ronchus (Sciaenidae) was also described according to the relationship between monthly gonadosomatic index and salinity variability, however no relationship was identified (Castro et al., 1999).

North Brazil Shelf

Amazon Estuarine Complex: North Brazil/Amazonia

In the Amazon Estuarine Complex (Figure S2), ecological guilds and fish diversity were assessed according to spatial and sesonal structures within the main channel and tidal creeks of the Pará River estuary (Mourão et al., 2014, 2015). Fish composition, abundance, and the use of estuarine habitats as nursery and reproduction grounds were mainly structured by salinity. The highest diversity and abundance of fishes occurred during the dry season in the main channel, while tidal creeks were used for reproduction. Migrants and freshwater stragglers were dominant in the lower estuary (Guamá River and Guajará Bay), while estuarine, marine stragglers and migrants predominated along the main channel (Mourão et al., 2014). Piscivorous and zoobenthivorous were the dominant feeding groups in all studied areas. Most species were occasional, characterizing the estuary as a transition zone (Mourão et al., 2015).

Starting from this estuary and traveling all the way to the Andes foothills, Amazonian catfishes (Brachyplatystoma spp.) perform one of the longest fish migrations in the world. They are commercially important and utilize the entire Amazon Basin to complete their life cycles. Populations are declining due to overfishing and to the presence of dams in the upper reaches of the migration range, which impairs spawning (Barthem et al., 1991). Otolith microchemistry revealed that larvae migrate downstream from the Andean piedmont to the lower Amazon (Duponchelle et al., 2016), while juveniles exhibit diverse strategies, rearing upstream, or downstream (Hegg et al., 2015).

Studies on the ecology of Amazonian freshwater stingrays (Potamotrygonidae) were performed within the Amazon complex. Potamotrygon motoro is a predominant species in Marajó Island (between the Amazon and Pará estuaries) showing preference for intermediate salinities and being resistant to critical conditions of pH, dissolved oxygen and temperature (Almeida et al., 2009). Paratrygon aiereba was studied according to cytogenetic approaches. The results revealed that their populations are structured within each one of the five rivers of the Amazon Basin, with no gene flow. Thus, the species is acknowledged as three distinct biological species, emphasizing that the management of their exploitation needs to focus on each river, rather than the entire river basin (Frederico et al., 2012).

In the Pará River Estuary, length–weight relationships of fish species (Loureiro et al., 2017), as well as the reproductive biology of commercial sciaenids are available (Santos et al., 2010; Barbosa et al., 2012). Plagioscion squamosissimus (sciaenidae) reproduces primarily in February/March and August/September (Barbosa et al., 2012), while Plagioscion magdalenae (Sciaenidae) spawns mainly from August to February (Santos et al., 2010).

Curuçá Estuary: North Brazil/Eastern Amazon

In Curuçá Estuary (Figure S3), forty intertidal fish species had their weight-length relationship studied by Giarrizzo et al. (2006). Moreover, the ontogenetic and seasonal diet shifts of Sciades herzbergii (Ariidae) (Giarrizzo and Saint-Paul, 2008), Lutjanus jocu (Lutjanidae) (Monteiro et al., 2009), and Colomesus psittacus (Tetraodontidae) (Giarrizzo et al., 2010) were also assessed for tidal creeks. The seasonal availability of food was more important than ontogenetic diet shifts; and stable isotope approaches revealed different types of food webs within the same ecosystem (Giarrizzo et al., 2011; Schwamborn and Giarrizzo, 2015).

The seasonal changes in the composition of intertidal fish assemblages inhabiting four creeks of the same salinity zone in the upper and middle reaches were investigated (Giarrizzo and Krumme, 2007). Fish composition changed seasonally, while density and biomass differed spatially, suggesting that spatial composition within habitats of homogenous salinity are dependent on landscape features.

Caeté River Estuary: North Brazil/Eastern Amazon

In the Caeté Estuary (Figure S4), fluctuations of the salinity gradient were the main forcing structuring fish assemblages over the annual cycle of 1996–1997 (Barletta et al., 2005). Stellifer rastrifer, Stellifer microps (Sciaenidae), C. spixii, and Aspredo aspredo (Aspredinidae) were the most abundant species. The species S. rastrifer was found along the entire main channel, regardless seasons; S. microps and A. aspredo were abundant in the upper estuary over the year, while C. spixii peaked in the middle and lower reaches in the early-rainy season. Larval phases of these four frequent species were also found in the main channel (Barletta-Bergan et al., 2002a). In addition, larvae of Stellifer and Cathorops genera were also found in mangrove creeks, emphasizing the importance of the system for the life cycle of subsistence species (Barletta-Bergan et al., 2002b).

Larval A. Clupeoides and S. microps were abundant in the main channel, peaking in the upper estuary in the dry season (Barletta-Bergan et al., 2002a). Guavina guavina (Eleotridae) and A. clupeoides were also frequent in the creeks, peaking in August (Barletta-Bergan et al., 2002b). Larval Cynoscion acoupa (Sciaenidae) was the most abundant commercial species in terms of density in both main channel and creeks. However, later stages were not frequent in the main channel (Barletta et al., 2005) or even in creeks (Barletta et al., 2003), placing this species as marine-estuarine dependent. Moreover, in a mangrove lake at the middle estuary, Achirus achirus (Achiridae), and the commercial taxa Centropomus pectinatus, Centropomus undecimalis (Centropomidae) and M. curema, accounted for 82% of the total catch in weight along 24 h sampling-cycles in wet and dry months, reinforcing the importance of the connectivity among estuarine habitats for fishes (Goch et al., 2005).

Tropical Southwestern Atlantic

Goiana River Estuary: Northeast Brazil

The main channel of the Goiana Estuary (Figure S5) was year-round characterized along its ecocline. In a rare effort, the influence of the ecocline on the movement patterns of fishes have been assessed throughout their ontogeny, from larval to adult phases along the annual cycles of 2005–2006 and 2012–2013. Fluctuations of the salinity ecocline and levels of dissolved oxygen structured the ariids C. spixii and Cathorops agassizii (Dantas et al., 2012). Juveniles peaked in the middle estuary in the early-rainy season (March–May), characterizing their nursery ground. For C. spixii, the nursery shifted to the lower estuary during the late-rainy season (June–August), while for C. agassizii it remained in the middle estuary. Sub-adults and adults peaked in the upper estuary in the rainy season. High densities of mouth-brooder males, free embryos and young juveniles were observed in the upper estuary during the late-dry season (December–February), characterizing their reproductive grounds. Mangrove creeks are important grounds only for later phases of these species, since earliest phases receive parental care (Ramos et al., 2011; Lima et al., 2012, 2013).

Salinity and water temperature shifts structured the patterns of estuarine use by Stellifer brasiliensis and Stellifer stellifer (Sciaenidae) along the system (Dantas et al., 2015). The middle estuary was an important nursery ground for juveniles and a feeding ground for sub-adults and adults of both species in the late-rainy season (June–August), except for adult S. stellifer, which peaked in the early-dry season (September–November). Later phases and larval S. brasiliensis were also found in mangrove creeks (Ramos et al., 2011; Lima et al., 2016), but were absent in the main channel, while larval S. stellifer were only recorded in the main channel (Lima et al., 2015). The species C. acoupa uses the upper estuary as a nursery in the early-rainy season (Ferreira et al., 2016). Sub-adults peak in the upper estuary during the entire annual cycle and migrate to the middle estuary in the late-rainy season, while adults inhabit adjacent coastal waters. Larval C. acoupa peaks in the lower estuary over the entire year (Lima et al., 2015), suggesting that spawning occurs in coastal waters; and later, larval and sub-adult phases inhabit the estuary (Ramos et al., 2011; Ferreira et al., 2016; Lima et al., 2016).

The patterns of estuarine use by Gerreidae species were influenced by changes in salinity gradient and dissolved oxygen (Ramos et al., 2016). Juvenile Eugerres brasilianus uses the upper estuary and the middle estuary as nursery grounds during the late-dry and early-rainy seasons, respectively. Sub-adults peaked in the upper estuary in the early-dry season, while adults were abundant over the entire year. On the other hand, juvenile Eucinostomus melanopterus uses estuarine beaches as nursery in the early-rainy and dry seasons. Independent of seasons, the abundance of sub-adults and adults at beaches toward the north of the estuarine mouth points to a degree of competition for estuarine resources, since both phases rely on the same food items (Ramos et al., 2016). Both species were found in tidal creeks (Ramos et al., 2011), but the larval phase of E. brasilianus was recorded in the main channel (Lima et al., 2015).

São Francisco River Estuary: Northeast Brazil

Flood pulses and river flow dynamics structured fish movement in the São Francisco River basin (Nestler et al., 2012). However, the estuarine portion is severely affected by eight upstream hydroelectric power dams that control flood pulses and alternative fish habitats (Coimbra et al., 2017; Figure S6). Alterations in flow regime facilitated the establishment of the non-native Metynnis lippincottianus (Serrasalmidae), while some endemic fishes disappeared (Assis et al., 2017). Restocking programs for the endemic Prochilodus argenteus (Prochilodontidae) were successful, but are no further recommended because the low allelic richness of the hatchery stock can minimize genetic diversity and increase the divergence from ancestral generations (Coimbra et al., 2017). Restocking programs were also tried for Brycon orthotaenia (Bryconidae), and now, after 40 years, they are recorded in the system (Brito et al., 2016).

The estuary, however, still maintains important ecological functions regarding connectivity. Its mouth is an important ground for the gonadal maturation of E. brasilianus (Rodrigues et al., 2017). Moreover, coastal demersal fishes are also influence by changes in abiotic conditions. The freshwater flux during the rainy months increases the functional diversity of fishes at shallower depths along the coast and estuarine-adapted fishes invade shallow coastal regions in a process known as estuarization of the coast (Passos et al., 2016).

Paraguaçu River Estuary: Northeast Brazil

Fish assemblages and functional guilds in the Paraguaçu Estuary are distributed according to differences in the salinity gradient (Reis-Filho et al., 2010; Figure S7). The middle estuary was dominated by S. rastrifer and Cynoscion microlepdotus (Sciaenidae). Eucinostomus argenteus (Gerreidae), Pellona harroweri (Pristigasteridae), and D. rhombeus were frequent in the middle and lower estuaries, while Sphoeroides greeleyi (Tetraodontidae) was frequent over the main channel. Deep-water and estuarine-resident fishes were abundant in the middle estuary, while shallow-water fishes were common in more saline areas. Marine-migrants were found in all sectors, while marine-stragglers were common from the middle to the mouth of the estuary (Reis-Filho et al., 2010). Organic matter and salinity were the main factors influencing overall fish distribution. Dissolved oxygen and organic matter structured the distribution of Eleotris pisonis (Eleotridae), Trinectes paulistanus, Achirus declives (Achiridae), Sphoeroides testudineus (Tetraodontidae), D. rhombeus, Citharichthys spilopterus (Paralichthyidae), Ctenogobius stomatus and Ctenogobius stigmaticus (Gobiidae) in habitats unaffected by aggardation, and Dormitator maculatus (Eleotridae), E. argenteus and Atherinella brasiliensis (Atherinopsidae) in affected habitats of the upper estuary.

Guanabara Bay: Southeast Brazil

In Guanabara Bay, the influence of the seasonal variability of local environmental factors on spatial patterns of demersal fishes was assessed in a fortnightly survey among 2005–2007 (Silva et al., 2016; Figure S8). Salinity, dissolved oxygen, ammonium, and phosphorus were responsible for quali-quantitative changes in spatio-temporal estuarine use. Chilomycterus spinosus (Diodontidae), G. genidens, E. argenteus, and M. furnieri were abundant species. The species C. spinosus were concentrated in the middle bay exhibiting high tolerance to eutrophic conditions and variations in salinity and temperature (Santos S. R. et al., 2015). A rise in the abundance of small specimens were observed when rainfall increased. The species G. genidens had strong association with the upper bay, where ammonium, total phosphorus and temperatures were higher (Silva et al., 2016).

The species M. furnieri (Mulato et al., 2015) and E. Argenteus (Corrêa and Vianna, 2016) were also frequent throughout the year. Juveniles had higher frequency in the upper and middle bays, while larger fishes were frequent in the lower bay. Recruitment of M. furnieri is observed in late fall, winter and spring (Mulato et al., 2015), and E. argenteus recruits in the first semester of each year (Corrêa and Vianna, 2016).

At the seawards end of the bay, Haemulidae, Pomacentridae and Labrisomidae were the richest families, and Diplodus argenteus (Sparidae), Haemulon aurolineatum (Haemulidae), Stephanolepis hispidus (Monacanthidae), and Abudefduf saxatilis (Pomacentridae) were the abundant species inhabiting an exposed estuarine beach located in a marine-estuarine transitional zone (Vermelha beach) (Rodrigues-Barreto et al., 2017). For a sheltered estuarine beach (Flamengo beach), richness and abundance were higher during spring (September to November) and lower during winter (June to August), while the relative abundance of fishes varied according to seasonal shifts in day length (Vasconcellos et al., 2010). Harengula clupeola (Clupeidae) peaked in spring, A. brasiliensis in austral summer/autumn, and Trachinotus carolinus (Carangidae), Umbrina coroides (Sciaenidae), and M. liza in winter.

At the entrance of the Bay, fish larvae peaked with highest temperatures and lowest salinities (March) (Castro et al., 2005). Abundance was higher at night, and lower during the day. Larval Cetrengraulis edentulus, Anchoa lyolepis (Engraulidae), and Harengula jaguana (Cupeidae) were dominant during both ebb and flood tides.

The species C. edentulus is the main commercially exploited species in this environment, and spawns from late winter to spring with a peak in November (Franco et al., 2014). Genidens genidens (Ariidae) is a potential sentinel species due to its abundance and non-migratory habits; and southern and southeastern Brazil populations of this species exhibit similar reproductive season and length-weight relationship (Silva et al., 2013).

Sepetiba Bay Estuary: Southeast Brazil

Salinity, depth, and transparency are the main variables influencing fish assemblages along the Sepetiba Bay and sandy beaches in the inner and outer bay areas (Araújo et al., 2002; Pessanha and Araújo, 2003; Figure S9). The species D. rhombeus, C. spixii, and G. genidens dominated the system and preferred shallow, less saline and less transparent waters of the inner bay, where the lowest diversity and highest abundance were also observed. In the outer bay, it was observed the opposite situation (highest diversity and lowest abundance), and Cynoscion leiarchus (Sciaenidae), Diplectrum radiale (Serranidae), and G. aprion were frequent species. The middle bay is inhabited by fishes that prefer average salinities, or with no clear preference [e.g., G. genidens, G. aprion, and Eucinostomus gula (Gerreidae)] (Araújo et al., 2002).‘

In a long-term survey, the salinity gradient influenced spatial changes in fish communities (Araújo et al., 2017). The inner bay was characterized by Chloroscombrus chrysurus (Carangidae), G. genidens, and M. furnieri. In the middle bay, Prionotus punctatus (Triglidae), G. genidens, and M. furnieri were frequent species, while in the outer bay P. punctatus and D. radiale were typical species. Fish richness and abundance decreased over the last three decades (1990–2010s) and sharpest changes were observed in the inner and middle bays since they are the most impacted areas due to high loads of metal and to the enlargement of the Sepetiba Port (Araújo et al., 2017).

Santos Estuary: Southeast Brazil

In the Santos Estuary, D. rhombeus, A. brasiliensis, B. ronchus, G. genidens, and H. clupeola were the most abundant species in the upper estuary during a short-term survey of one rainy (March) and one dry month (August) (Santos J. A. P. et al., 2015; Figure S10). The dry period was dominated by H. clupeola and A. brasiliensis, while the rainy period was dominated by D. rhombeus, G. genidens and B. ronchus. Fish diversity peaked during the rainy month and it was associated to the appearance of a species with affinities for lower salinities (Santos J. A. P. et al., 2015).

Environmental Impacts in Tropical Western Atlantic Estuaries

Habitat Changes

In the Amazon Estuarine Complex, the replacement of culture of sugar cane to permanent agroforests, timber logging (including a shipping terminal), and an industrial estate at Pará River Estuary resulted in habitat loss and critical alterations of fish communities (Barros and Uhl, 1995; Viana and Lucena Frédou, 2014). For the Goiana Estuary, sugarcane plantations, milling, aquaculture, limestone mining, dredging, and urban development are among the landscape modifications (Barletta et al., 2017b).

Alterations in river flow patterns and volume due to damming and dredging, as well as water quality changes due to wastewater disposal, building, and operation of artisanal fishing harbors are severely degrading the São Francisco River Estuary (Barletta et al., 2017b). The decreased river flow reduced dissolved inorganic nitrogen and silicate seawards, and the estuary became oligotrophic (Martins et al., 2011; Medeiros et al., 2011; Genz and Luz, 2012).

Urbanization and pipeline routes for oil and gas industry have caused coastal erosion problems in Guanabara Bay (Araruna et al., 2014), and fish diversity became low in estuarine sandy beaches exposed to wave action with unlimited human access (Franco et al., 2016). In Sepetiba Bay, human modification include the enlargement of Sepetiba Port, dredging activities, construction of a steel factory and a terminal for building submarines (Araújo et al., 2016).

Environmental and Fish Contamination With Plastic Debris

Contamination by microplastics is a concern in the main channel and mangrove creeks of the Goiana Estuary and exibits complex patterns (Lima et al., 2014, 2016). Microplastics are found in every habitat throughout the entire year, sharing the same habitats as fishes and their prey (Lima et al., 2014, 2015, 2016). When precipitation increases, the freshwater flow seawards is a powerful exporter of this contaminant from the upper estuary to the marine environment. Total density of microplastics present the same order of magnitude as total fish larvae and fish eggs in the main channel. Simultaneous comparable amounts of microplastics and fish increase the chances of interactions of these two compartments (Lima et al., 2015). The ingestion of plastic debris by demersal fishes was recorded in ariid catfishes (Possatto et al., 2011), gerreids (Ramos et al., 2012), sciaenids (Dantas et al., 2012; Ferreira et al., 2016), and centropomids (Ferreira et al., 2019).

Sediments in beaches within Guanabara Bay are also polluted with plastic debris, especially microplastics (Carvalho and Baptista Neto, 2016). Microplastics peaked in the warm-rainy season (January-February), but also presented high concentration during the cold-dry season (June–July). Sources are associated to local rivers and streams, fishing and harbor activities, domestic effluents, maritime terminals, and mussel farming (Carvalho and Baptista Neto, 2016; Castro et al., 2016).

Sewage Contamination and Eutrophication

In Santos (Braga et al., 2000; Aguiar and Braga, 2007) and Curuça Estuarine Systems (Venekey and de Melo, 2016), fecal sterols, fecal coliforms, and high loads of nutrients are higher near industrial estates, farms, and cities, revealing a strong sewage contamination. High levels of eutrophication and thermotolerant coliforms are observed in the upper reaches of the Caeté Estuary during the dry season, however, water quality might improve during the rainy season (Monteiro et al., 2016a,b). Water in shallow areas of the inner Guanabara Bay have the poorest quality, being hypertrophic, and sometimes hypoxic (Ribeiro and Kjerfve, 2002; Aguiar et al., 2011). There, fecal sterols in sediments indicate areas of severe and historical sewage contamination (Paranhos et al., 1998; Santos et al., 2008). Poor water quality represents a risk to the biota due to low dissolved oxygen (Braga et al., 2000) and pathogens.

Environmental and Fish Contamination With Petroleum Hidrocarbons and Persistent Organic Pollutants

A pipeline leak following an accident in 2000 was responsible for ~340,000 gallons of oil spilled into Guanabara Bay, severely polluting the upper reaches of the bay with polycyclic aromatic hydrocarbons (PAHs) (Gabardo et al., 2000; Farias et al., 2008; Massone et al., 2013). After two years, sediments in the inner bay were highly contaminated with PAHs, while water samples no longer showed toxicity effects (Silva et al., 2007a). After four years, PAHs decreased by 70%, showing that climatic variations over time can be efficient in hydrocarbons degradation (Farias et al., 2008) and that water circulation was somehow effective in the spill area. Another Diesel oil spill (60,000 L) accident occurred in 2005, and PAHs in tissues of C. parallelus, M. liza, G. genidens, Brevoortia aurea (Clupeidae), and M. furnieri peaked when rainfall inuced the runoff of adjacent streams and left the bay exposed to oil from other sources (Silva et al., 2007b; Soares-Gomes et al., 2010).

In Guanabara Bay, M. furnieri and M. liza presented relatively high levels of polychlorinated biphenyls (PCB) and low levels of polybrominated diphenyl ethers (PBDE) when compared to other ecosystems around the world (Gonçalves da Silva et al., 2013). Croakers presented the highest PCB and PBDE levels, while mullets showed intermediary levels. For C. parallelus, M. liza, T. lepturus, and Sardinella brasiliensis (Clupeidae) the levels of PCBs and organochlorine pesticides (OCs) are below the maximum limit established by the Food and Drug Administration (U.S. Environmental Protection Agency-EPA) and, apparently, pose low risk to human consumption (Silva et al., 2003).

Environmental and Fish Contamination With Metals

According to 210Pb dating, increases in heavy metal flux started at the beginning of the last century in Guanabara Bay (Baptista Neto et al., 2013). Sediments are affected by Cr, Pb, and Zn, being the northwestern bay and the Rio de Janeiro harbor the most polluted sectors (Abreu et al., 2016). Sources of metals are related to urban emissions, continental sources, biogeochemical processes, and a chlor-alkali plant at the western portion of the estuary that was responsible for mercury-contaminated effluents entering the bay (Wasserman et al., 2000; Cordeiro et al., 2015; Aguiar et al., 2016). Hg peaks in the western bay, while the northwestern bay is not severely contaminated (Machado et al., 2008). Dredging can pose additional risk of Hg contamination (Silveira et al., 2017), however mangrove forests are biogeochemical barriers accumulating metals and promoting the reduction of metal transport by tidal currents (Kehrig et al., 2003; Borges et al., 2007).

Metal contamination in waters and sediments were also assessed in the Amazon Complex (Lima et al., 2017), Sepetiba Bay (Fonseca et al., 2013), Paraguaçu Estuary (Hatje and Barros, 2012), and Santos Estuarine System (Kim et al., 2016). Sources are associated with mining, industry, natural igneous rock decomposition, reduced freshwater flow, farming, and non-treated sewage (Braga et al., 2000; Paraquetti et al., 2004; Genz et al., 2008).

Bagre spp., M. liza, M. furnieri, C. undecimalis (Kehrig et al., 1998, 2002; Baêta et al., 2006) and T. lepturus (Seixas et al., 2012) are still not severely contaminated with heavy metals in Guanabara Bay. Livers of M. furnieri, Bagre spp. and M. liza accumulates higher loads of Hg and methil-Hg, showing relationship with total length (Kehrig et al., 2002, 2009; Baêta et al., 2006). In Sepetiba Bay, M. liza, C. leiarchus, M. furnieri, and G. genidens had their muscles, gonads, and livers contaminated with heavy metal above maximum permissible levels established by the Brazilian Ministry of Health for human consumption (Lima Junior et al., 2002). Hg in Guanabara and Sepetiba Bays presented positive relationship with trophic levels, suggesting that Hg is being biomagnified through the food webs (Kehrig et al., 2002; Baêta et al., 2006; Bisi et al., 2012).

In the Goiana Estuary, Hg levels in muscles of T. lepturus increased with body size and weight. Hg levels decreased when rainfall increased, through biodilution (Costa M. F. et al., 2009; Barletta et al., 2012). Such seasonal pattern was also observed in Ciénaga Grande de Santa Marta Lagoon for E. plumieri and M. incilis (Alonso et al., 2000). However, Cd, Zn, and Cu in muscle of Ariopsis bonillai (Ariidae) were highest when salinity was lower (Campos, 1992). In the Santos Estuarine System, high levels of Hg in muscle of C. spixii (Azevedo et al., 2009, 2011) and above-limits for Cu and Zn in liver of M. curema (Fernandez et al., 2014) confirmed a high anthropogenic influence.

Subtropical Southwestern Atlantic

Paranaguá Estuarine Complex: South Brazil Tropical-Subtropical Transition

The interaction between seasons and estuarine habitat shifts (ecocline) structured fish movement in the Paranaguá Estuarine Complex (Barletta et al., 2008) (Figure S11). Seasonal variations in temperature and salinity influenced the spatio-temporal use of intertidal habitats for A. brasiliensis (Carvalho and Spach, 2015). Batoids are also distributed according to seasonal variation in the salinity gradient (Possatto et al., 2016). The species C. spixii, S. stellifer, Anchoa parva (Engraulidae), Achirus lineatus (Achiridae), and G. genidens were the most abundant taxa (Barletta et al., 2008). These species preferred the upper and middle estuaries during most of the year, except A. parva, which peaked in the lower estuary during the dry season. During the late-rainy season, when rainfall increases, fishes move seawards to the middle estuary.

Strong influence of the salinity ecocline on fish distribution was also observed in a multiple sampling survey (1993–2011) in the same estuary (Passos et al., 2013). Anchoa januaria, Anchoa tricolor (Engraulidae) A. brasiliensis and H. clupeola were the most abundant species in this system. The upper estuary was inhabited by the estuarine A. januaria, while marine fishes as A. brasiliensis, H. clupeola, and A. tricolor dominated the middle and lower estuaries.

The feeding ecology of Rhinobatos percellens (Rhinobatidae) (Carmo et al., 2015), Ctenogobius shufeldti (Gobidae) (Contente et al., 2012), and A. brasiliensis (Contente et al., 2011); the reproduction and recruitment of Etropus crossotus (Paralichthyidae) (Oliveira and Favaro, 2011); and the importance of the system as nursery for Epinephelus itajara (Serranidae) (Félix-Hackradt and Hackradt, 2008) and Manta birostris (Myliobatidae) (Medeiros et al., 2015) are other information available for this estuarine complex.

Guaratuba Bay Estuary: South Brazil/Tropical-Subtropical Transition

Salinity fluctuations, hydrodynamic variability, and geomorphology of the channel structured fish assemblages in Guaratuba Bay (Vendel et al., 2010; Figure S12). Salinity, transparency, and organic matter were the most important factors distinguishing habitats. A. januaria, A. lepidentostole, O. oglinum, A. brasiliensis, S. greeleyi, and A. lyolepis were all abundant species. The upper-inner estuary was characterized by A. januaria, while the lower-outer estuary was characterized by O. oglinum, A. lyolepis, A. lepidentostole, S. greeleyi, and A. brasiliensis.

In mangrove areas, Haemulopsis corvinaeformis (Haemulidae), and S. rastrifer were the most representative species (Chaves and Vendel, 1997; Chaves and Bouchereau, 1999; Chaves and Corrêa, 2000) and, E. argenteus, E. melanopterus, B. ronchus, and Citharichthys arenaceus (Paralichthydae) were common species (Chaves and Corrêa, 1998). High catches were recorded for winter months, when temperature decreased and salinity increased (Chaves and Bouchereau, 1999). However, mangroves are spawning areas for ~40% of fishes species, especially in summer and spring months, when maturation and spawning become evident (Chaves and Vendel, 1997; Chaves and Bouchereau, 2000). However, for other species as C. parallelus, spawning and hatching are associated to stronger marine influence, while juvenile recruitment associates to salinity declines during the rainy season, when river runoff increases (Chaves and Nogueira, 2013). Mangroves, salt marshes (Chaves and Vendel, 1996, 2008) and adjacent rivers (Costa P. V. et al., 2009) are also feeding grounds for several taxa.

Babitonga Bay Estuary: South Brazil/Subtropical

Depth and salinity structured the spatio-temporal variability of dominant species in Babitonga Bay (Figure S13). Engraulidae, Eucinostomus spp. and Mugil spp. dominated shallow fish assemblages in abundance, followed by A. brasiliensis, A. januaria, A. tricolor, H. clupeola, and Oligoplites saliens (Carangidae) (Vilar et al., 2011). The marine species H. clupeola, O. saliens, A. tricolor, and T. carolinus were characteristic of the outer bay, while estuarine-residents and marine-migrants (A. brasiliensis, A. januaria, S. greeleyi, C. spilopterus and D. rhombeus) were characteristic of the inner bay. Thespecies T. carolinus peaked in the warm rainy season; M. furnieri in the transition season; and O. saliens in the cold dry season.

The first occurrence of larval Microdesmus longipinnis (Microdesmidae) (Souza-Conceição et al., 2013) and the distribution of larvae of the invasive species Omobranchus punctatus (Blennidae) were assessed in Babitonga Bay (Costa et al., 2011). Sciaenidae larvae (B. ronchus, Cynoscion sp., M. furnieri) are abundant and distributed along the entire bay, and peak in abundance in spring and summer months (Costa et al., 2012). Larval Lycengraulis grossidens (Engraulidae) also exhibit spatio-temporal patterns within the Bay (Costa and Souza-Conceição, 2009).

Patos Lagoon Estuary: South Brazil/Subtropical

Salinity and temperature explained most of the variability in a long-term assessment of shallow-water estuarine-dependent fishes in the Patos Lagoon Estuary (Garcia et al., 2012; Figure S14). The westerly wind belt movement, or Southern Annular Mode, influenced variations occurring at a scale of 2 years, while rainfall anomalies due to ENSO events influenced inter-annual variability at scales of 3–7 years. Mugil liza, Brevoortia pectinata (Clupeidae), and M. furnieri occurred year-round. Mugil gaimardianus (Mugilidae), M. curema, and B. pectinata were associated with higher salinities and temperatures. Mugil liza and M. furnieri associated with lower salinities and temperatures.

Shallow-water marine fishes peaked in the 1995/1996 La Niña due to low precipitation rates and freshwater runoff; decreasing in the 1997/1998 El Niño when precipitation and river discharge increased (Garcia et al., 2001, 2004). Anchoa marinii (Engraulidae), A. brasiliensis, M. liza, M. platanus, M. curema, and Jenynsia multidentata (Anablepidae) were frequent species. Estuarine-resident fishes increased upstream in La Ninã situation, and showed opposite patterns in El Niño. Estuarine-dependent fishes also showed contrasting patterns (Garcia et al., 2001). The species A. brasiliensis and M. platanus peaked in shallow waters. Mugil liza peaked in La Niña and lowered in El Niño. During El Niño, sub-adults and adults of A. brasiliensis were absent from upstream shallow waters due to the high freshwater discharge (Garcia et al., 2001), while the freshwater fishes Astyanax eigenmaniorum, Oligosarcus jenynsii (Characidae), and Parapimelodus nigribarbis (Pimelodidae) dominated the upstream reaches (Garcia et al., 2001, 2003).

Age, growth, and reproductive aspects of Mycteroperca marginata (Epinephelidae) (Seyboth et al., 2011), Odontesthes argentinensis (Atherinopsidae) (Moresco and Bemvenuti, 2006), M. liza (Garbin et al., 2014), and Jenynsia multidentata (Anablepidae) (Garcia et al., 2004) were also studied for this system. New species belonging to the families Loricariidae (Carvalho et al., 2008; Rodriguez and Reis, 2008) and Gobiidae (Burns et al., 2010; Cheffe et al., 2010), and reports on the occurrence range and competition of the invasive Acestrorhynchus pantaneiro (Acetrorhynchidae) (Neuhaus et al., 2016) are also available for the lagoon. Long-term assessments of ichthyoplankton are also available and must be incorporated into conservation planning (Martins et al., 2007; Costa et al., 2016; Costa and Muelbert, 2017).

Population genetics revealed that many species in the lagoon and adjacent systems are in process of speciation, suggesting that managerial actions must consider different sub-populations (Beheregaray and Levy, 2000; Da Silva Cortinhas et al., 2016).

The ariid white sea catfish Genidens barbus was once an important fishery resource in the estuary, where the species had the most abundant population known in the past (Velasco et al., 2007). Therefore, studies on this species became important for the region. Description of growth parameters using length and age data (Velasco et al., 2007) and the use of estuarine carbon sources revealed by isotope analyses (Pereyra et al., 2016) report biological aspects for the species. Ecological aspects were revealed by otolith microchemistry and patterns of estuarine uses (Avigliano et al., 2015), inter-annual variability (Avigliano et al., 2017a), freshwater residence times (Avigliano et al., 2017b), nursery grounds and connectivity (Avigliano et al., 2016) are available for the species.

Micropogonis furnieri is a common species in the Patos Lagoon and represents an economically important fish for the artisanal fishery (Costa et al., 2015). Several aspects of the biology and ecology of this species is also available regarding the system. Feeding ecology studies using different aspects, as daily consumption (Figueiredo and Vieira, 2005), feeding strategies (Mendoza-Carranza and Vieira, 2008), and stable isotope inferences are available (Mont'Alverne et al., 2016). Otolith microchemistry was used to reveal aspects of growth and age of young individuals (Cavole and Haimovici, 2015). In addition, studies have emphasized the importance of ontogenetic approaches while studying fish movement, since early life stages of M. furnieri have multiple and complex habitat preferences, suggesting that essential fish habitats must be explored for species with complex life cycles to improve management and conservation planning (Costa et al., 2014, 2015).

Environmental Impacts in Subtropical West Atlantic Estuaries

Habitat Changes

The largest Latin America maritime terminal for agro-industrial products (e.g., soy beans) is located in the Paranaguá Estuarine Complex and Pontal do Felix port is a recent additional structure built in the upper estuary. Dredging operations for maintenance of the shipping channel have altered its geomorphology resulting in upstream intrusion of coastal waters and changes in fish communities (Barletta et al., 2016). During the dredging process, total mean density and biomass of C. spixii, Aspistor luniscutis (Ariidae) and G. genidens increased, while Menticirrhus americanus (Sciaenidae), S. rastrifer and C. leiarchus decreased significantly in the dredged channel. Ariid catfishes were favored by the damage of the benthic fauna, while other species as sciaenids disappeared. Future dredging operations must be avoided during reproductive (October to December) and recruitment (April to June) seasons of fishes, which occurs in the late-rainy season. Therefore, dredging in the Paranaguá Estuary should be performed during the dry season (July to September) to promote sustainable fishery practices (Barletta et al., 2016).

The expansion of the Rio Grande Port and jetties at the entrance of the Patos Lagoon Estuary has changed sediment deposition patterns (texture and distribution) in the estuarine and coastal regions (Cunha and Calliari, 2009; Silva et al., 2015). Moreover, the construction of a dam between the estuary and the Patos-Mirim lagoon to prevent the entrance of salt water resulted in the absence of estuarine and marine species upstream (Burns et al., 2006).

Sewage Contamination and Eutrophication

In Paranaguá Bay (Martins et al., 2010; Cunha et al., 2011; Brauko et al., 2016), Babitonga Bay (Martins et al., 2014) and Patos Lagoon (Martins et al., 2007), fecal steroids are higher close to ports and urban areas pointing to a significant sewage contamination of waters and sediments. In Guaratuba Bay, signs of eutrophication due to organic and inorganic matter inputs are still partially controlled by precipitation and tidal currents (Mizerkowski et al., 2012; Rodrigues et al., 2013). Phosphorus is higher in sediments from the upper estuary and in the transition between the upper and middle estuary (Cotovicz Junior et al., 2014). Increases in nutrient inputs, water temperature and salinity induce blooms of harmful diatoms in the bay, poisoning the biota and causing human intoxication (Tibiriçá et al., 2015).

Plastic Contamination

Contamination with plastic debris was assessed only in the Paranaguá Estuarine Complex, being more significant near urbanized areas in the upper and middle reaches. It is affected by local hydrological processes, with no seasonal or spatial trends along the salinity gradient (Possatto et al., 2015).

Environmental and Fish Contamination With Persistent Organic Pollutants

In November 2004, an oil tanker spilled methanol and bunker oil in front of Paranaguá harbor and the osmoregulation of A. brasiliensis was affected until seven months after the accident (Souza-Bastos and Freire, 2011). Tributyltin (TBT) and organic contaminants of antifouling paints in liver were reported for C. spixii, with higher levels closer to Paranaguá harbor (Santos et al., 2014). Furthermore, a model revealed that PAHs adsorbed in sediments and solubilized in water can be possibly transferred to fishes and biomagnified along the trophic chain of the estuarine complex (Froehner et al., 2011).

In Guanabara Bay, aliphatic hydrocarbons and linear alkylbenzenes inputs are related with geochemical processes. Higher loads were observed during summer months due to increased summer holidays (Dauner and Martins, 2015). OCs and PCBs had low concentrations due to low inputs from the Germany rivers discharging in the bay (Combi et al., 2013). In Babitonga Bay, PCBs and diclorodifeniltricloroetano (DDT) also presented high concentration at specific sites close to anthropogenic impacted areas of São Francisco harbor (Rizzi et al., 2017).

For the Patos Lagoon Estuary, hydrocarbon pollution is related to combustion of fossil fuels, release of oil, industrial and domestic effluents. Higher concentrations in sediments are observed near refineries and oil terminals, shipping lanes and sewage discharges (Medeiros et al., 2005; Garcia et al., 2010).

Environmental and Fish Contamination With Metals

Sediments in Paranaguá (Anjos et al., 2012) and Guaratuba Bays (Sanders et al., 2008) are contaminated with metals, sometimes above World Health Organization (WHO) critical limits. Metal contamination in water is widely reported for the Patos Lagoon Estuary (Windom et al., 1999; Mirlean et al., 2001; Costa and Wallner-Kersanach, 2013). Metals presented higher concentrations close to urban and industrial areas, being human inputs and geochemical anomalies the main identified sources of these pollutants (Niencheski et al., 1994; Sá et al., 2006; Anjos et al., 2012; Costa et al., 2013).

In the Paranaguá Estuarine Complex, muscles of C. spixii and G. genidens are contaminated by metals, with levels of Cr and As exceeding the permissible limits for seafood consumption (U.S. EPA) (Angeli et al., 2013). In Babitonga Bay, levels of Zn and Cr in muscles of E. brasilianus, C. paralellus, and M. platanus are still acceptable for human consumption (Bonatti et al., 2004). However, in the Patos Lagoon Estuary, Hg levels in M. furnieri, N. barba, G. genidens, and Odontesthes bonariensis (Atherinopsidae) were above background levels, but below critical levels for human consumption (U.S. EPA) (Niencheski et al., 2001; Kutter et al., 2009).

Warm Temperate Southwestern Atlantic

Río de La Plata Estuary: Subtropical/Temperate Transition

A comprehensive overview of fish diversity and the environmental influence on fish distribution and composition is available for the Río de La Plata Estuary (Jaureguizar et al., 2016; Figure S15). Salinity structured spatial patterns of larval fishes during austral late spring (December 1999) and summer (February 2000) (Berasategui et al., 2004). The horizontal salinity gradient, bottom salinity and water temperature are the main factors structuring species composition across seasons (Jaureguizar et al., 2003b, 2004; Lorenzo et al., 2011). Micropogonias furnieri, C. guatucupa, B. aurea, M. schmitti, and M. ancylodon are abundant species. The freshwater and shallow upper estuary was typified by P. valenciennesi and N. barbus (Jaureguizar et al., 2004). The middle estuary contained the highest densities of M. furnieri, B. aurea, M. ancylodon, where depths and salinities had intermediate values (Jaureguizar et al., 2004). Density of M. furnieri and M. ancylodon were higher in summer, while density of B. aurea increased during winter and autumn. The saltier and deeper lower estuary was dominated by C. guatucupa, M. schmitti. Larger catches of C. guatucupa were observed in autumn, while M. schmitti during winter and spring (Jaureguizar et al., 2004).

Studies regarding ontogenetic diet shifts in Urophycis brasiliensis (Phycidae) (Acuña-Plavan et al., 2007), first records of larval Elops smithi (Elopidae) (Machado et al., 2012) and adult E. melanopterus (Gerreidae) (Solari et al., 2010), phylogenetic approaches for the endemic Pimelodus albicans (Pimelodidae) (Vergara et al., 2008) and aspects of reproduction in B. aurea (Macchi and Acha, 2000) are available. However, most studies have focused on Sciaenidae species, especially the most abundant and commercially interesting ones (M. furnieri, C. guatucupa, Pogonias cromis, and Macrodon ancylodon).

The species P. cromis spawn between October and January (Macchi et al., 2002), M. ancylodon between October and March (Militelli and Macchi, 2006), C. guatucupa in March and December (Militelli and Macchi, 2006), and M. furnieri between November and March (Macchi et al., 2003). Young age-classes of C. guatucupa decreases seawards, with a reverse pattern in spring, while older age-classes inhabit marine coastal areas (Jaureguizar et al., 2006). Short-term changes in oceanographic conditions have greater influence structuring C. guatucupa populations than long-term variability (Jaureguizar and Raúl, 2009). During 1998 El Niño and 1999 La Niña, adults were associated with high salinities, when the area was dominated by wind driven inflow of seawater. During typical years (1994 and 2003), juveniles correlated with low salinities, when winds forced freshwater to flow seawards (Jaureguizar and Raúl, 2009).

Selective processes differentiate populations of M. furnieri between the estuary and adjacent coastal locations, and the influence of salinity and temperature in phenotypic cohesion can structure these populations (D'Anatro et al., 2011; D'Anatro, 2017). Larvae of M. furnieri are abundant during the warmest months, showing high predominance in the river-estuarine transition and positive correlation with bottom salinity horizontal gradient (Braverman et al., 2009). Ontogenetic approaches revealed a complex use of the estuary by M. furnieri, based on the bottom salinity gradient (Jaureguizar et al., 2003a, 2008). Spawning occurs in the innermost areas, near the upstream edge of the salinity wedge (Acha et al., 1999).

Pando Estuary: A Sub-estuary of Río de La Plata

For the Pando Sub-Estuary (Figure S16), M. furnieri, M. liza, P. orbignyanus, B. aurea, and Parapimelodus valenciennis (Pimelodidae) are the most abundant species (Acuña-Plavan et al., 2010; Gurdek and Acuña-Plavan, 2016). Marine migrants were correlated with higher salinity, while freshwater species peaked at lower salinity and estuarine species correlated with higher temperature. Significant correlations between abundance and temperature are related to synchronized events during species life cycles.

Length-weight relationship of 12 species, including the abundant ones, are available for this sub-estuary (Gurdek and Acuña-Plavan, 2014). For the most abundant species M. furnieri, the length-weight relationship was assessed along its ontogeny over an intra-annual cycle (Gurdek and Acuña-Plavan, 2016). This species produces the seasonal courtship/spawning sounds from November to March (spawning season), with a strong seasonal variability, appearing in October, peaking in January-March, and disappearing in April (Tellechea et al., 2011).

Mar Chiquita Coastal Lagoon: Temperate Southwest Atlantic, Argentina

In Mar Chiquita Lagoon (Figure S17)., B. aurea, O. argentinensis, M. liza, and M. furnieri are abundant species, especially in summer months (Bruno et al., 2013). Juveniles of Platanichthys platina and Ramnogaster arcuata (Clupeidae) are also frequent (González Castro et al., 2009). Marine fishes peaked in the lower estuary when temperature increased in summer and autumn. Brevoortia aurea was the most abundant species in the southern-lower portion, and O. argentinensis in the middle and northern-upper portion of this estuary (Bruno et al., 2013). Juvenile recruitment is ruled by seasonal onshore winds (Bruno et al., 2015). However, salinity and temperature structured fish assemblages (González Castro et al., 2009). Brevortia aurea peaks in higher salinity and temperatures. The species M. liza and O. argentinensis correlated with low salinities. Peaks of O. argentinensis occurr at lower temperatures, while M. furnieri peaks at higher temperatures. The occurrence of M. curema (González Castro et al., 2006) and T. carolinus (Díaz de Astarloa et al., 2000), both with tropical-subtropical affinities, in the temperate lagoon is related to the presence of warm neritic waters from the continental shelf originated in subantarctic waters of the Malvinas Current.

Anchoa marinii (Engraulidae) reproduces between December and April when temperature increases and mature females aggregates in adjacent coastal areas (López et al., 2015). The species M. liza migrates seawards in April-May and November-December to spawn (González Castro et al., 2011). Aggregations of mature females of B. aurea can be observed in October-November in the lower estuary (Lajud et al., 2016).

Bahía Blanca Estuary: Temperate Southwest Atlantic, Argentina

For the Bahía Blanca Estuary (Figure S18), the reproductive aspects of Sympterygia acuta (Rajidae) (Díaz-Andrade et al., 2009) and the feeding ecology of R. arcuata (Lopez Cazorla et al., 2011) are described. In addition, the influence of biotic and environmental factors on seasonal patterns of juvenile fishes in Spartina alterniflora saltmarsh and a contiguous tidal flat in the Bahía Blanca Estuary was also evaluated (Valiñas et al., 2012). However, fish research is focused on three economically important species: M. furnieri, C. guatucupa and P. orbignyanus (Blaber and Barletta, 2016).

The age structure of the population of C. guatucupa was revealed by otolith analyses (Lopez Cazorla, 2000), while for P. orbignyanus, age structure was revealed by scales reading and growth parameters (Lopez Cazorla, 2005). Seasonal diet shifts and ontogenetic changes in the feeding ecology of the three species (Lopez Cazorla and Forte, 2005; Sardiña and Lopez Cazorla, 2005a,b), as well as dietary overlaps between the two co-occurring sciaenid species (Sardiña and Lopez Cazorla, 2005c) were assessed within the system. Foraging activities of M. furnieri have direct and indirect effects on the granulometric composition and stability of bottom sediment of salt marshes (Molina et al., 2017).

Environmental Impacts in Warm Temperate Western Atlantic Estuaries

Habitat Changes

Habitat modifications in Río de La Plata Estuary include shoreline retreats due to deforestation, tourism activities, and land development (Cellone et al., 2016). Urban beach erosion and accretion have strong relationships with climate changes, sea level rise, and increased storminess (Gutiérrez et al., 2016).

Various ports, cities, livestock, agriculture and oil, chemical, and plastic industries are located in Bahía Blanca Estuary (Spetter et al., 2015). The estuary has one of the largest deep water ports in the country (Ingeniero White port), which is regularly dredged (Zilio et al., 2013). A project to deepening a navigation channel in the inner estuary to a depth of 13.5 m related to a natural gas provision have been pointed to cause physical and social consequences to the system. The loss of nursery services and of the jobs associated with fishing activities, cease of recreational activities during the dredging process, the loss of the coastal landscape, water pollution derived from sediment removing and the effects on groundwater are imminent possibilities (Zilio et al., 2013). Increased erosion of coastal terraces in response to rising sea level, increased land use in the harbor area and aggradation due to dredged spoils deposition are also observed in Bahía Blanca (Pratolongo et al., 2013).

Sewage Contamination and Eutrophication

The Río de La Plata Estuary is moderately eutrophic. Increases in freshwater runoff and nutrient loads, associated to a low potential to dilute and flush nutrients, suggest that the system is prone to worsening eutrophication conditions generating further dissolved oxygen stress and harmful algal blooms (Nagy et al., 2002). Sewage effluents pose a potential ecotoxicological risk to aquatic biota due to inputs of estrogens (Valdés et al., 2015). In the Bahía Blanca Estuary, sewage and industrial discharges receive poor or no treatment before reaching the system (Pierini et al., 2012). Microbiological contamination was revealed by the presence of Escherichia coli and Samonella spp. in water and sediments close to sewage discharges in the Rosales Harbor and tributaries discharging into the estuary (Spetter et al., 2015; Streitenberger and Baldini, 2016).

Environmental Contamination With Plastic

Plastic contamination has been assessed since 1999 by the National Direction of Aquatic Resources in the Río de La Plata Estuary and by the Ocean Conservancy's International Coastal Cleanup Day in Uruguayan aquatic systems. Most plastic debris comes from urban wastes, waterways, and marine traffic in Uruguayan waters (Lozoya et al., 2015). The bottom salinity front of the salt-wedge is the main barrier accumulating plastic debris upstream (Acha et al., 2003). In the southern coast of the system, 100% of freshwater fishes belonging to eleven species were contaminated with microplastics in their gut contents, especially fibers, with higher numbers near sewage discharges, where they varied from 30 to 89 fibers per stomach (Pazos et al., 2017).

Environmental and Fish Contamination With Petroleum Hidrocarbons Persistent Organic Pollutants

High levels of aliphatic and aromatic hydrocarbons in waters, sediments, soils and biota were observed after ~1,000 tons of oil spilled in coastal waters of Río de La Plata (Colombo et al., 2005a,b). Petroleum direct inputs and combustion, harbor activities, and vehicular emissions are the main sources of hydrocarbons to this system (Venturini et al., 2015). PCBs have highest concentrations near industrialized areas close to Buenos Aires, and transformers oil containing Aroclor 1,254–1,260 are the probable sources (Colombo et al., 2005c).

PAHs, PCBs, and PBDEs in sediments of the Bahía Blanca Estuary had higher concentrations near urban and industrial areas (Arias et al., 2010; Oliva et al., 2015; Tombesi et al., 2017). TBT and dibutyltin (DBT) concentrations were higher in sediments near Puerto Belgrano harbor (Argentina's Army), where there are intense shipyard activities (Delucchi et al., 2007). Levels of OCs were moderate, when compared to worldwide ranges, and showed a high correlation with precipitation in sites near agricultural fields (Arias et al., 2011).

In Río de La Plata, Cyprinus carpio (Cyprinidae), Mugil cephalus (Mugilidae), O. bonariensis, and Prochilodus lineatus (Prochilodontidae) showed moderate to high levels of aliphatic hydrocarbons and PCBs in their muscles with signs of bioaccumulation (Colombo et al., 2000, 2007a,b; Menone et al., 2000; Cappelletti et al., 2015). The highest concentrations were recorded in P. lineatus, especially near the urban center, exceeding guidelines for human consumption (U.S. EPA) (Colombo et al., 2000; Speranza et al., 2016). In the Bahía Blanca Estuary OCs contaminated C. guatucupa with a size-related bioaccumulation pattern (Lanfranchi et al., 2006). PAHs were reported to contaminate Odontesthes sp. in the system; and the global average for this pollutant indicated that Bahía Blanca is chronicaly polluted (Arias et al., 2009, 2010).

Environmental and Fish Contamination With Metals

Metal contamination in sediments and water were assessed in Río de La Plata Estuary (Tatone et al., 2013, 2015), Mar Chiquita Lagoon (Marcovecchio et al., 2001; Beltrame et al., 2009), and Bahía Blanca Estuary (Botté et al., 2007; Grecco et al., 2011). Sources and highs levels of metals are related to polluted discharges from agricultural, urban and industrial sources (Camilión et al., 2003; Marcovecchio et al., 2016; Santucci et al., 2017).

In Río de La Plata, Pterodoras granulosus (Doradidae), P. lineatus (Villar et al., 2001), M. platanus, and M. furnieri are contaminated with metals with signs of bioaccumulation. Hg is the most important contaminant for M. furnieri, however values are still below the international standards (U.S. EPA) recommended for suspending human consumption (Corrales et al., 2016). Hg levels in edible muscle of fishes from Mar Chiquita Lagoon are also safely below recommendation standards (Marcovecchio et al., 2001; Marco et al., 2006). In the Bahía Blanca Estuary, low levels of Cd and Zn were observed in top predators M. schmitti and Halaelurus bivius (elasmobranchii), however Hg levels exceeded the international standards (Marcovecchio et al., 1986, 1988a,b, 1991) and also showed signs of bioaccumulation. Livers of Brevortia aurea, O. argentinensis, M. furnieri, C. guatucupa, M. schmitti, and P. orbignyanus are also contaminated with metals. At least one sample of each species presented concentrations of Mn and Cr hazardous to humans (La Colla et al., 2017).

Eastern Pacific Estuaries

Tropical Eastern Pacific

Bahía málaga estuary: Colombia/Panamá Bight Ecoregion

At least 237 species inhabit the Bahía Málaga Estuary (Figure S19) (Artunduaga, 1978; Rubio, 1984a,b; Castillo, 1986; Castellanos-Galindo et al., 2006). The combination of tidal and dial cycles explained shifts in fish communities, but a biomass decrease was notable when rainfall increased at the end of the annual cycle (Castellanos-Galindo and Krumme, 2013). Spatial and temporal patterns of larval fish community along the main channel of the estuary was also assessed during an annual cycle (Medina-Contreras et al., 2014). Seriola sp. (Carangidae) and Cetengraulis mysticetus (Engraulidae) were the most abundant larvae. Salinity or temperature were not correlated with larval density, but larvae varied greatly among months, suggesting a strong influence of seasonality in the bay (Medina-Contreras et al., 2014).

The composition and diversity of intertidal fishes were assessed in Isla Palma, in the lower estuary (Castellanos-Galindo et al., 2005). Freshwater fishes are known to reach Isla Palma due to high rainfall rates influenced by the Intertropical Convergence Zone (Cordoba and Giraldo, 2014). Clupeidae were the most abundant family, in terms of numbers, inhabiting intertidal mangrove habitats in the innermost portion of the estuary, however Lutjanidae, Tetraodontidae and Ariidae dominated in weight (Castellanos-Galindo and Krumme, 2013).

Studies on the feeding ecology of Centropomus unionensis (Centropomidae) (Mancilla and Rubio, 1992), and diet, growth and reproduction of Lutjanus guttatus (Lutjanidae) (Suárez and Rubio, 1992a,b) are also available. According to a trophic flow model performed in the inner portion of the bay, the very low salinity throughout the year is responsible for the low number of primary and secondary consumers (e.g., zooplankton, crustaceans and some fishes) in the mangrove system. Therefore, zoobenthivorous (snappers, catfishes) and detritivorous (mullets) fishes dominate in biomass, when compared to piscivorous and zooplanktivorous fishes (Castellanos-Galindo et al., 2017).

Rio palmar and rio javita estuaries: Ecuador/Guayaquil Ecoregion

Fish communities were compared between the dry and the wet season in mangrove creeks and main channel of Palmar and Javita rivers (Shervette et al., 2007; Figure S20). The diversity of species belonging to the families Gobiidae, Gerreidae and Engraulidae is high in the mangrove system of Palmar Estuary, while species of Carangidae, Engrauliae, and Gerreidae are diverse in the Javita main channel. Significant differences were detected among areas and seasons for both systems, and the percent of mangroves and mean depth influenced fish communities. Although these estuaries present low species diversity compared with other tropical estuarine systems (Blaber, 2000), they still provide important nursery habitats for many fishes of commercial and ecological importance (Shervette et al., 2007).

Environmental Impacts in Tropical Eastern Pacific Estuaries

Habitat Changes

Not more than 4,000 people, distributed in small villages, live in Bahía Málaga (Castellanos-Galindo and Krumme, 2013). However, over the last 25 years, Bahía Málaga has faced anthropogenic changes relative to the construction of a naval base in the mid 1980's and an increased tourism activity nearby (Castellanos-Galindo et al., 2011). This resulted in mangrove loss, but no specific estimates are available. Governmental agencies plan to construct a deep-water commercial harbor, what might be an important threat to marine and estuarine fish diversity. Nevertheless, La Plata (~6,791 ha) and La Sierpe (~25,178 ha) areas have recently been declared protected areas by local environmental agencies.

Sewage Contamination and Eutrophication

Water quality assessments asserted that Bahía Málaga is still in good conditions with no signs of eutrophication or changes in physic-chemical parameters (Betancourt Portela et al., 2011). However, further chemical pollution assessments are necessary for the region, including their fate for the local biota.

Temperate Eastern Pacific

Valdivia River Estuarine System: Chile/Araucanian/Chiloense Ecoregion

A study on the migratory patterns of Galaxias maculatus (Galaxiidae) from larval to adult stage revealed a strong association with seasonal changes in salinity along the Valdivia estuary (Hugo, 1973; Figure S21). Another study in Corral Bay detected that higher densities of larvae were observed near the tidal front, and differences were related to tidal intrusion of salt water (Vargas et al., 2003). According to patterns of circulation, Corral bay is a source of young fish larvae. Strangomera bentincki (Clupeidae), Odontesthes regia laticlavia (Atherinopsidae), Gobiesox marmoratus (Gobiesocidae), and Hypsoblennius sordidus (Blenniidae) were the most abundant larval species.

The seasonal influence on diatery ontogenetic shifts of the Chilean silverside O. regia was assessed in the Valdivia Estuarine System and this species is acknowledged as a selective omnivorous predator (Fierro et al., 2014). In the Corral bay, the feeding ecology of Myxodes viridis (Clinidae) was also assessed in different depths and tidal cycles (Ochoa-Muñoz et al., 2013).

Environmental Impacts in Temperate Eastern Pacific Estuaries

Environmental Contamination With Persistent Organic Pollutants

PAHs in sediments of Corral Bay showed a medium pollution rate with a temporal variation, with a substantial increase observed from March to September during 2000 (Palma-Fleming et al., 2004). Aliphatic hydrocarbons were at low to medium contamination rate with no temporal variation, and inputs are relative to the petroleum hydrocarbon-diesel fraction and biogenic hydrocarbons (Palma-Fleming et al., 2012). Such impacts are related to control of prague, fluvial wood transportation, wood and paper industries, shipyards, fishing industries, and salmon conditioning jails.

Environmental Contamination With Metals

Dramatic changes in the Valdivia River Estuarine System are related to wastewater and solid emissions from industrial or domestic activities, aerial emissions, farming/agriculture, and oil spills (Palma-Fleming et al., 2012). Cd level within the Corral Bay was lower than in other Pacific coastal areas, but increased upstream rivers as salinity decreased (Pinochet et al., 1995). Cu and As in sediments were above standards of the Sediment Quality Guidelines (U.S. EPA) in all sampling points of Corral Bay, being an indicative of toxicological effects for the biota (Palma-Fleming et al., 2012).

Discussion

The Importance of the Ecocline and Seasonality Concepts to Study Fish Movement and Environmental Quality Assessments

Estuaries were long poorly understood because of their complex natural processes and only recently, over the past four decades, fully recognized as a key coastal ecosystem (Elliot and Whitefield, 2011). Therefore, studies regarding the estuarine ecocline concept and the influence of environmental variability on fish movement and environmental changes are still missing even in large and important systems of the Western Atlantic and along all eastern Pacific coast of SA (Blaber and Barletta, 2016). The influence of the estuarine ecocline on fish movement were discussed in the Amazon, Caeté, Guanabara, Santos, Guaratuba, Babitonga, Pando and Mar Chiquita systems. In Ciénaga Grande, Goiana, Paraguaçu, Sepetiba, Paranaguá and Patos Lagoon systems, not only fishes, but also environmental quality (water and sediments) were assessed regarding the influence of the ecocline. However, the main concern is that in most surveys, fishes and environmental quality were short-term assessed, and/or across limited spatial scales, regardless the annual variability of the salinity gradient, as in Cienaga Grande Lagoon (Rueda and Defeo, 2003), Paraguaçu Estuary (Hatje and Barros, 2012), Guaratuba Bay (Vendel et al., 2010), and Río de La Plata (Jaureguizar et al., 2003b). Therefore, ecological patterns, biological behavior and physico-chemical processes might still be obfuscated by the lack of annual cycles, long-term, and full lenght approaches. Thus, efforts for conservation, recovery and sustainable use of estuarine resources were lead by poorly informed managerial actions (Barletta et al., 2010).

Systems in the tropical Northwestern Atlantic have recently gained attention. Lists of species are available for the Atrato River Delta (Correa-Herrera et al., 2016, 2017) and Orinoco River Delta, on the Caribbean coast (Cervigón, 1985; Blaber, 2000; Blaber and Barletta, 2016) (Figure 1, Table 1). In the Atrato Delta, spatio-temporal patterns of fish larvae and their densities, comparable to microplastics available in the water, were also assessed (Correa-Herrera et al., 2017). In Northeast Brazil, few fish and human impacts studies are available for the Parnaíba River Delta (Oliveira, 1974; Watanabe L. A. et al., 2014; Ribeiro et al., 2017), Potengi River Estuary (Oliveira et al., 2011; Buruaem et al., 2013; Souza et al., 2016) and Itamaracá Estuarine System (Ekau et al., 2001; Vasconcelos Filho et al., 2003, 2010). In Southern Brazil, the Laguna Estuarine Complex has intense artisanal fisheries activities and an industrial fleet focused on mullets for most of the year (Barletta et al., 2017b). However, fish research and human impacts along the ecocline were never evaluated.

“An ecocline represents a boundary of progressive change between two systems, representing the response to the gradual difference in one major environmental factor acting at a different scales and influencing the total differences within the gradient” (Attrill and Rundle, 2002). Within any estuarine system, the salinity is the major environmental factor referred in the ecocline concept (Barletta and Dantas, 2016). Hence, researchers have proposed that the proper management of estuaries are dependent upon reliable biological and abiotic data encompassing multiple aspects of space and seasonality along the estuarine gradient (Machado et al., 2016; Barletta et al., 2017a; Underwood et al., 2017).

Regarding fish research, accurate sampling design using monthly surveys replicated along different reaches and encompassing several aspects of seasonality are available for the Caeté Estuary (Barletta et al., 2005), Goiana Estuary (Dantas et al., 2013) and Paranaguá Estuarine Complex (Barletta et al., 2008, 2016). These provided reliable data on fish movement over annual cycles on which managerial reccomendations must be build. In European Atlantic estuaries (Vetemaa et al., 2006; Martinho et al., 2007), as well as in North-American Atlantic estuaries (Love and May, 2007; Granados-Dieseldorff and Baltz, 2008), accurate sampling designs for fish research are also available as reference to be replicated in any estuarine system.

In addition, the spatio-temporal variability of the estuarine ecocline influences patterns of use of essential habitats by the different ontogenetic phases of a fish species. Therefore, the ontogenetic approach is another important point of view while studying fish movement (Acuña-Plavan et al., 2007; Ferreira et al., 2019). Very few studies worldwide address ontogeny, such as in estuaries from Australia (Taylor et al., 2006), North America (Stehlik and Meise, 2000), South Africa (Harris et al., 1999), and Asia (Lin et al., 2007). In SA, fish ontogeny was assessed in Río de La Plata (Acuña-Plavan et al., 2007), Pando (Gurdek and Acuña-Plavan, 2016), Bahía Blanca (Lopez Cazorla and Forte, 2005; Sardiña and Lopez Cazorla, 2005a,b), and Goiana (Dantas et al., 2010, 2015; Ramos et al., 2016) estuaries. These studies asserted that the ecological unit is not the species in their own, but their different ontogenetic phases. Costa et al. (2014) and Ferreira et al. (2016, 2019) emphasized that the different phases of a species can have multiple and complex habitat preferences over spatio-temporal scales, and essential habitats must be explored to improve management and conservation planning.

Regarding environmental and fish contamination, accurate samplings are available for microplastics in the Goiana Estuary (Lima et al., 2014; Ferreira et al., 2016, 2019; Silva et al., 2018), for metals in Guanabara Bay (Baêta et al., 2006; Cordeiro et al., 2015) and for POPs in Río de La Plata (Colombo et al., 2000; Venturini et al., 2015). However, for most SA systems, the bioavailability and contamination of fishes with POPs, metals and microplastics were never assessed along the ecocline. Rainfall variability is a strong controller of metal and POP levels in fish tissues, since drought periods can enhance contamination and high precipitation rates diminishes the contaminants through biodilution (Costa M. F. et al., 2009; Barletta et al., 2012; Bisi et al., 2012). Fish contamination is higher near urban, industrial or rural areas and, sometimes, values exceeded the permissible limits for human consumption (U.S. EPA) (Marcovecchio et al., 2001; Delucchi et al., 2007; Fernandez et al., 2014). Moreover, the bioaccumulation and biomagnification of metals and POPs are occurring in the trophic web of most estuaries (Marcovecchio et al., 1986; Cappelletti et al., 2015). In the Negombo Estuary (Sri Lanka), for example, metal contamination of M. cephalus was year-round categorized along spatial locations and seasons providing a reliable design that can be replicated worldwide using different pollutants (Mendis et al., 2015).

Moreover, metals and POPs are somewhat controlled by other abiotic factors and their proper assessment are indeed also needed. The biogeochemistry and bioavailability of metals and POPs in estuaries are controlled by suspended particulate matter loads and dissolved oxygen levels, which in turn are strongly controlled by the salinity gradient (Janeiro et al., 2008; Bayen, 2012; Costa et al., 2012). Freshwater inputs from rivers and streams; effluents from the agriculture fields; untreated domestic and industrial sewages; oil spill and release; and combustion of fossil fuel are probable sources of metals and POPs contamination for fishes, but are hardly ever assessed (Costa M. F. et al., 2009; Barletta et al., 2012; Venturini et al., 2015). For this reason, all these sources still need further attention in SA coastal systems.

On the other hand, the inadequate disposal practices and fishery activities along river basins and coastal areas are the most obvious source of plastic pollution (Lima et al., 2014). This problem become worse when large plastics fragment into smaller particles (<5 mm), increasing the chances of interactions even during the earliest phases of a fish life cycle (Lima et al., 2015, 2016). Microplastics present higher concentrations within semi-enclosed environments and the river basin is recognized as one of the main source of microplastic inputs into estuaries, where they become ubiquitous over the year (Lima et al., 2014; Cheung et al., 2016; Lebreton et al., 2017); Vendel et al., 2017.

The problems regarding the interaction of microplastics and fishes are available for the Goiana (Ferreira et al., 2016, 2019; Silva et al., 2018) and Río de La Plata (Pazos et al., 2017) estuaries. The most complete scenario is reported for the Goiana Estuary, where the distribution patterns of microplastics were first reported (Lima et al., 2014). The estuarine ecocline acts as a control of microplastics in drier months and exporter of microplastics to the marine environment in rainy months, when runoff increases seawards (Lima et al., 2014; Lebreton et al., 2017). Microplastics have comparable densities with ichthyoplankton, emphasizing a high concentration in the main channel (Lima et al., 2015). Ingestion of plastic filaments is widespread and affect different ontogenetic phases of demersal fishes (Possatto et al., 2011; Dantas et al., 2012; Ramos et al., 2012; Ferreira et al., 2016, 2019; Silva et al., 2018). Every estuarine system in SA is experiencing this same problem of contamination due to generalized poor disposal practices (Costa and Barletta, 2015). However, “there have been very few papers describing multivariate tests of spatial or temporal patterns of microplastics” (Underwood et al., 2017).

Disruption of Estuarine Ecoclines Caused by Human Modifications in Estuarine Morphology

Human interventions in estuarine geomorphology lead to alterations in the natural inflow of salt water, and disrupt the ecocline along the whole system. Such problem is worse under the influence of industrial activities due to several months of dredging to the maintenance of waterways and artificial channels or the damming of major rivers, which increase saline intrusion, changing fish communities (Barletta et al., 2016, 2017b; Prestrelo and Monteiro-Neto, 2016). Impacts of dredging has been widely discussed worldwide (Wilber and Clarke, 2001; Nayar et al., 2003; Güt and Curran, 2017). The loss of nursery services and of the jobs associated with fishing activities are the main consequences of dredging or damming. Wasserman et al. (2016) asserted that the main concern for the interpretation of such impacts is the absence of studies using local hydrodynamics.

In SA, dredging activities were discussed in Sepetiba Bay (Araújo et al., 2016), Guanabara Bay (Silveira et al., 2017), Bahía Blanca Estuary (Zilio et al., 2013), and Paranaguá Estuarine Complex (Barletta et al., 2016). The damming of the São Francisco Estuary, for example, decreased the magnitude of its flow from 2,846 m3 s−1 to 800 m3 s−1, leading to increased saline intrusion (Barletta et al., 2017b). Water transposition from the river basin to the adjacent semi-arid region to serve rural populations, industrial, and tourism activities during severe droughts has been widely criticized for its potential impacts (Barletta et al., 2017b). In the Rhine-Meuse estuary, for example, it is suggested that the restoration of tidal and river dynamics in polders are the best options for the ecological rehabilitation of one of the most important wetlands in the Netherlands (Storm et al., 2005; Slater, 2016). However, possibilities for a natural recovery of the São Francisco Estuary are far from any perspective, since background and novel information on human-driven changes are absent. Further investigations are needed since the saline intrusion in the current stagnant estuary has increased, changing ecological functions for fishes. Fortunately, larger systems have shown the capacity to withstand human modifications. However, “the full recovery of coastal marine and estuarine ecosystems from over a century of degradation can take a minimum of 15–20 years for attainment of the original biotic composition and diversity may lag far beyond that period” (Borja et al., 2010).

Estuarine Conservation and Recommendations

The avoidance of governmental institutions in using the basic estuarine concepts has been debated for decades (Dauvin and Ruellet, 2009). Researches using ecocline concepts are increasing in quantity and quality (Blaber, 2000; Barletta et al., 2016; Reis et al., 2016). However, the time elapsed to compile scientific information and the establishment of plans is the main challenge. Despite the variety of coastal ecosystems in SA, the number of effective Marine Protected Areas is still insufficient, and conservation measures are not implemented outside these areas to guarantee the conservation of connected habitats.

The lack of basic sanitation is the worst concern in SA (Costa and Barletta, 2016). In riverside settlements, uncontrolled sewage discharges along the whole course of rivers only increases at estuaries. Several nano- and biotechnologies are alternatives to reduce contaminants in effluents and offer a potential treatment of surface water, groundwater and wastewater contaminated by toxic metal ions, organic and inorganic solutes, and microorganisms (Wang et al., 2010; Qu et al., 2013; Martínez-Huitle and Ferro, 2016).

Plans aiming at estuarine conservation must consider year-rounded cycles of retention and flush of environmental contaminants along ecoclines, as well as their interactions with fishes (Barletta et al., 2016). However, the majority of studies consider only limited spatial patterns based on the distance to point-sources of impacts. The lack of temporal assessments also leads to misinterpretation of whether estuaries are able to withstand human modifications and when (and if) estuaries will recover from unpredictable climatic events. Withal, environmental quality assessment have evolved when biological measures in fishes were integrated to ecological relevance, providing a new support for management, and monitoring schemes (Duarte et al., 2017).

An example of successful monitoring of is through the use of the Integrated Biomarker Response index (IBR), which can indicate different sources of anthropogenic contamination in aquatic environments using fish as bioindicator. Larger biomarker responses are often found in the most contaminated sites (Duarte et al., 2017). In the Estuarine-Lagoon Complex of Iguape-Cananéia (Southeast Brazil), the spatio-temporal changes in parameters such as oxidative stress, biotransformation, genotoxicity, and histopathological alterations in Atherinella brasiliensis correlated to sediment pollution with metals, PAHs and pharmaceuticals and personal hygiene products (PPCPs) in areas of greater human presence (Salgado et al., 2018). The IBR corroborated with these results, indicating that the Cananéia City has the worst environmental quality (Salgado et al., 2018). The metabolic enzyme activities, protein content and lipid peroxidation were analyzed in muscle and liver of Ramnogaster arcuata (Clupeidae) to assess the correlation with PAHs levels in tissues. IBR was significant to assess PAH toxicity and highlighted R. arcuata as a good bioindicator in the Bahía Blanca Estuary (Ronda et al., 2018). These multi-biomarker approaches help in the comprehension of ecosystem health aiming at a more comprehensive assessment of environmental quality (Duarte et al., 2017). Moreover, comparative measures of IBR before and after any type of managerial or conservative action can help to assure the success or failure of such actions. Therefore, further studies regarding fish indices should be performed as a tool to assess environmental quality in SA estuaries.

Another problem faced in SA is the overexploitation of estuarine fishery resoruces. Along the Amazon River basin, multispecies fishery follows a clear seasonal pattern of river hydrological cycles (Isaac et al., 2016). However, hydrological alterations due to the construction of dams, in addition to deforestation and climate change affect the seasonal and annual dynamics of these fisheries (Isaac et al., 2016; Pinaya et al., 2016). Overexploitation of fishery resources is known since the early 80's, when traditional communities shift from labor in multiple resources (agriculture, fishing, and small-scale stock raising) to concentrate in commercial fishing (McGrath et al., 1993). Although captures per unit effort remained stable over time, body lengths of most-caught species were below length at first maturation (Castello et al., 2011). Fishery was characterized as moderately exploited, with few profitable species being overexploited. For the region, management of fisheries can lead to increased yields through the enforcement of minimum size of capture and closed seasons of catches (Castello et al., 2011).

Landings at Guanabara Bay, accounted to ~19,000 tons (US$ 4.8 million) between 2001 and 2002 (Jablonski et al., 2006). Small pelagic fishes (Atlantic anchoveta and Brazilian sardinella) and demersal fishes (croakers, mullets and catfishes) comprised the main catches, with densities compatible with commercial fisheries (Jablonski et al., 2006). However, fishermen associations have complained that fish abundance and fishery income has decreased since the oil spill in January 2000 (Jablonski et al., 2006). Unless regional industries implement regulations to avoid environmental degradation and measures to treat effluents, pollution will continue to threaten the development of artisanal fishing (Bessa et al., 2004).

State of poverty and lack of power of the artisanal fishermen are pointed as the main factor making this group invisible in the formulation of public policies, which favors industrial fishing (Galli et al., 2007). In the Rio de LA Plata Estuary, for example, the overexploitation of M. furnieri was attributed to improvements of the industrial fleet (Horta and Defeo, 2012). In Bahia Blanca Estuary, Cynoscion guatucupa is the most important resource captured by the artisanal fishery fleet. However, overexploitation and collapses in stocks are also related to increasing industrial operations in open waters adjacent to the estuary (Lopez Cazorla et al., 2014). Thus, the recognition of the socio-economic importance of artisanal fishing through the participation in decisions to the sustainability of their activities, improvement of the fishermen income through fish processing and selling at the landing points are frames needed to change this situation (Jablonski et al., 2006; Galli et al., 2007).

The conservation of coastal ecosystems and traditional livelihoods are ruled by different policies to preserve natural resources through the co-management perspective (ICMbio, 2012; Barletta et al., 2017b). Limited mesh sizes, closed periods, establishment of fishing seasons; no-take-zones, quotas for common resources; efforts to reduce/eliminate wastewater disposal, control uptake of freshwater by damming and control salinity intrusion by dredging can be highlighted as priorities for SA estuaries.

Re-establish operation licenses and accurately analyse risk assessments of activities next to river basins and sourround estuaries are important steps to prevent habitat loss (Lotze et al., 2006; Huang et al., 2014). Mangrove deforestation, for example, is of major concern in most estuarine systems along the Ecuadorian coast, especially due to aquaculture, and construction of shrimp ponds (Shervette et al., 2007; Hamilton and Stankwitz, 2012). It is asserted that shrimp aquaculture is responsible for 80% of carbon lost due to mangrove deforestation (Hamilton and Lovette, 2015). From an estimated 362,000 ha of mangrove forest, almost 50% had been lost, being the Muisne region the most impacted area (Zhengyun et al., 2003). In the Chone Estuary, for example, the establishment of shrimp farms, covering 51,919,128 m2 was responsible to reduce mangrove area from 42,377,182 m2 in 1968 to 14,654,255 m2 in 2006 (Hamilton and Stankwitz, 2012). In the Grande Estuary, most estuarine area is dedicated to shrimp farms, accounting for a mangrove loss of 47%. On the other hand, in Rio Hondo and Cayapas-Mataje, only 16 and 10% of mangrove loss due to shrimp farming was recorded by 2008 (Hamilton and Stankwitz, 2012). The maintenance of shrimp ponds needs to be managed and integrated to mangrove functioning, as an example of using mangroves as nutrient filter of pond effluents prior to the return of water back to the estuary (Twilley et al., 1998). Moreover, successful actions aiming at the recovery of deforested and degraded mangrove has been presented for some systems in SA. Replanting of mangroves in the Acaraú River (Paula et al., 2016) and Paraiba do Sul River estuaries (Rezende et al., 2015); and salt marshes in the Patos Lagoon (Tagliani et al., 2007) are acknowledged as a good approach to recover degraded wetlands and restablish biodiversity (Rezende et al., 2015).

Biodiversity is also threatened due to invasive species, which in turn are introduced by water ballast and aquaculture escaping. Estuaries and coasts are susceptible to introductions of non-native species since they are centers for the vessel activities. The introduction of these species may cause niche overlaps, when the invasive species uses the same resources as native species (Neuhaus et al., 2016). Although this sharing of resources may not affect the survival of the species, introductions and invasions of piscivorous predators, for example, can impact not only the species richness of native fish community but may also cause changes over all trophic levels, altering the equilibrium of the system (Neuhaus et al., 2016). This might also lead to impacts on native fishery resources, diseases, and parasites occurrences (Tomás et al., 2012). In Brazil, several case studies relate the introduction of non-native carnivorous fish to a decrease in local diversity. Examples are the introduction of O. beta in the Santos Estuary (Tomás et al., 2012), A. pantaneiro in the Patos Lagoon Estuary (Neuhaus et al., 2016) and O. punctatus in Babitonga Bay (Costa et al., 2011). Thus, studies assessing the overlapping food niches and, consequently, the degree of competition in the presence of invasive species, are important for the conservation of native species.

The estuarine ecocline has a great influence in the connectivity among river basins and coastal waters, and estuaries are recognized as important ecosystems for providing biological and geochemical demands to both these systems (Able, 2005; Barletta et al., 2010; Watanabe K. et al., 2014). Conservation issues aiming to improve resilience must onset before the ecosystem modifications overpass their capacity to maintain its natural resources and services (Williams and Crutzen, 2013). This is the case of the environmental tragedy at Doce River basin (southeast Brazil), on November 2015, where the disruption of a containment dam of mining tailings (Fundão/Samarco) contaminated the river with 50 million.m−3 of mud flood (Barletta et al., 2017b). It caused an immeasurable impact along hundreds of km of river bed toward the coasts of more than one Brazilian state. Lives and livelihood losses, kill of tons of fishes (Barletta et al., 2017b), contamination of sediments, potable and surface waters with metals (Segura et al., 2016; Gomes et al., 2017) are among the many accounted impacts. This is just one case of environmental accident affecting a SA coastal system, where co-management, practices of emergency and risk assessment protocols have traditionally less and less attention. Therefore, potentially, every system can share the fate of Doce River.

All these issues are of major concern for the South Eastern Pacific estuaries, since the lack of estuarine research lead to a poor understand of what is the real status of the systems. This might be attributed to socio-economic problems. Most countries have a lower development indicator and the percentage of gross domestic product destined to research and development is lowest in countries such as Peru, Colombia, Ecuador and Chile, when compared to Brazil and Argentine, for example (Cociocca and Delgado, 2017). In addition, problems such as guerrillas, narco-traffickers, decaying economy due to populism, inequality, and educational options has been of major concern for these contries. Therefore, financial support is hardly ever destined to research and development (Cociocca and Delgado, 2017). Moreover, the commoditization of shrimp farmings in Ecuador has destroyed thousands of hectares of mangroves (Zhengyun et al., 2003), but concomitantly has generated $ 1 billion annually, leading to government negligencies (Hamilton, 2012). In Peru, a research Agenda of priorities for coastal systems has only recently gained attention due to the workshop “Advancing Green Growth in Peru” in 2016 (McKinley et al., 2018). Nevertheless, Brazil and Argentina has been also suffering due to economic instability, corruption, crime and narco-traffickers and the future of research is an imminent concern (Cociocca and Delgado, 2017).

According to all recorded damages, SA estuaries have almost never recovered to background situations, despite time and efforts. The constant habitat modifications that were relatively slow for nearly 400 years, have increased since after Second World War and industrialization (and urbanization) in the continent, worsening environmental quality and reducing fish yields for coastal zones. If anthropogenic interferences keep with their course and speed, regardless all reported environmental concerns, natural resources and services provided by estuaries will face the most severe degradation in the near future. Further research to support managerial planning and action should, therefore, not only be scientific-based on the continent-wide natural diversity, but also need to consider the social importance of estuaries for traditional fishers and other populations, whose dependence upon these systems goes beyond livelihoods.

Author Contributions

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.

Conflict of Interest Statement

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

Acknowledgments

The authors acknowledge financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico through grant (CNPq-Proc.404931/2016-2); Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) through scholarship (FACEPE/BFP-0130-1.08/15). MB is CNPq Fellow.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2019.00237/full#supplementary-material

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Keywords: estuarine ecocline, estuarine conservation, human modification, contamination of aquatic habitats, fish ecology, environmental quality

Citation: Barletta M and Lima ARA (2019) Systematic Review of Fish Ecology and Anthropogenic Impacts in South American Estuaries: Setting Priorities for Ecosystem Conservation. Front. Mar. Sci. 6:237. doi: 10.3389/fmars.2019.00237

Received: 14 January 2019; Accepted: 16 April 2019;
Published: 09 May 2019.

Edited by:

Christos Dimitrios Arvanitidis, Hellenic Centre for Marine Research (HCMR), Greece

Reviewed by:

Alan Whitfield, South African Institute for Aquatic Biodiversity, South Africa
José Lino Vieira De Oliveira Costa, Universidade de Lisbon, Portugal

Copyright © 2019 Barletta and Lima. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Mário Barletta, barletta@ufpe.br