Impacts of mining pollution on coastal ecosystems: is fish body condition a reliable indicator?

Identifying reliable biological indicators is fundamental to efficiently assess human impacts on biodiversity and to monitor the outcomes of management actions. This study investigates whether body condition is an appropriate indicator of putative effects from iron ore mining tailings on marine fishes, focusing on the world's largest mining disaster - known as the Mariana disaster, in Brazil. Eight species were used to test the hypothesis that individuals inhabiting an area severely impacted by tailings have reduced body condition in comparison to those in control areas near (<60 km) and distant (>120 km) from the impact site. Contrary to our prediction, no significant difference in condition was detected between the impacted area and both near and distant controls in seven of the eight species. The results indicate that body condition, as measured by the scaled mass index, has limited applicability as indicator of impact from mining pollution on the fishes analysed. Hypotheses that could explain our findings are proposed, including nutrient provisioning from continental drainage that could indirectly influence fish condition and compensate for the deleterious effects of mining pollution.

Habitat use of five sympatric predatory reef fishes at a remote island in the south-western Atlantic.

Density-dependent mechanisms and habitat use are important drivers of marine spatial distribution in complex ecosystems such as coral or rocky reefs. In the last decade, a few studies have assessed habitat use by reef fishes in nearshore and coastal environments along the Brazilian coast. Serranidae (groupers and sea basses) are regarded as excellent models for understanding habitat use patterns due to their diversity, long lifespan, wide distribution, morphological and functional diversity, and behavioural complexity. Their trophic position in the food web, from meso- to top-predators, grants them critical roles as top-down population controllers. Herein, we present the first assessment of habitat use by five sympatric Serranidae in a Brazilian oceanic island, Trindade. The model species selected for this assessment were the coney (Cephalopholis fulva), the rock hind (Epinephelus adscensionis), the greater soapfish (Rypticus saponaceus), the Creole-fish (Paranthias furcifer) and the hybrid between C. fulva and P. furcifer. Our findings revealed that the species showed specific associations with topographic characteristics related to shelter from predation, reproduction and feeding. Habitat use in Trindade was similar to that observed in nearshore coastal environments (where the hybrid is absent). The present work contributes to the knowledge of habitat use and niche partitioning among key species, which is a valuable tool to subsidize effective conservation initiatives such as designing marine protected areas focusing on the behaviour and habitat use of key ecological players.

Niche availability and habitat affinities of the red porgy Pagrus pagrus (Linnaeus, 1758): An important ecological player on the world's largest rhodolith beds.

The red porgy (Pagrus pagrus) is a carnivore bottom dweller sparid, inhabiting flat sandy bottoms, rhodolith and seagrass beds of the Mediterranean Sea, the Western Atlantic (from Florida to Argentina) and the Eastern Atlantic (from Britain to Gabon). Along its native range, the red porgy is highly targeted by commercial and artisanal fisheries. In the past 40 years, the population decline of the species has been widely reported. In many locations, such as the Brazilian coast, stocks have collapsed. The central portion of the Brazilian coast harbours the largest rhodolith beds in the world and the highest levels of nektonic and benthic biodiversity. Along the rhodolith megahabitat, P. pagrus density is disproportionately higher (by 480%) than that of conspicuous benthic fishes inhabiting the same environment. Despite the ecological and economic importance of such an important species along its native range, little is known regarding its habitat use, niche availability and population responses to global warming. Here we present habitat affinities based on data sampled using baited remote stereo-video systems, and modelled niche availability and global warming populational responses. Our findings reveal that the red porgy is a species highly associated with rhodolith beds along the central portion of the Brazilian coast. The presence of a disproportional density and biomass of the red porgy, compared to other marine fish species, indicates that the species plays a key ecological role as a carnivore, mesoconsumer and prey/predator tolerant species, maintaining essential ecological functions in the habitat. In a global warming scenario, the model predicted populational niche shifts poleward and a severe niche erosion at lower latitudes as expected. Conservation initiatives (implementation of Maine Protected Areas, trawling exclusion zones, mining exclusion zones, fisheries management policies) are urgent to secure future stocks of the red porgy and also preserve the fragile rhodolith beds they inhabit.

Limited human access is linked to higher effectiveness in a marine sanctuary.

Marine Protected Areas (MPAs) are a widely used tool for coral reefs conservation, but massive tourism activities inside MPAs worldwide can challenge their effectiveness. This study investigated the role of different levels of protection strictness (no-entry, low and high tourism-allowed zones) set for a marine sanctuary in shaping benthic cover and reef fish community structure in the richest and largest coral reef system of the Southwestern Atlantic. Reef fish community structure and benthic cover differed between protection levels. No-entry zones showed significant higher coral coverage and biomass of piscivores and herbivores than tourism-allowed zones. Highest differences were found between no-entry and high tourism intensity zones. Despite the fact that protection from fishing by itself can ensure conservation benefits, we show here that the establishment of no-entry zones improve MPAs effectiveness.

Coastal degradation impacts on green turtle's (Chelonia mydas) diet in southeastern Brazil: Nutritional richness and health.

This study evaluated the influence of environmental degradation on the nutritional value of the main marine macrophytes consumed by green sea turtles (Chelonia mydas) in areas with different degrees of urbanization. Macrophyte assemblages in the highly urbanized area (HUa) showed lower richness compared to the lightly urbanized area (LUa) (Mann-Whitney U test: 10.0 ± 3.6 SD genera and 11.9 ± 4.2 taxa per transect vs. 20.1 ± 7.0 genera and 23.5 ± 9.2 taxa per transect) respectively. Also, diet was poorer with 4.0 ± 1.6 genera per turtle (vs. 8.5 ± 4.0 in HUa) and less diverse with Shannon index of diversity = 0.45 ± 0.29 (vs. 0.64 ± 0.46 in LUa). Body condition was similar in both areas. About half of individuals were classified as having normal body condition, 14-15% as underweight and 23-34% as being emaciated. Fibropapillomatosis prevalence (χ2 = 8.720; n = 222; df = 1; p = 0.003) was higher in the HUa but, in affected animals, severity was marginally non-significant (χ2 = 5.721; n = 82; df = 2; p = 0.057). Significant differences in energy content (kcal) were detected between areas in both summer (S) and winter (W). All ANOVAs on total lipids (F = 22.15 [S] and 30.39 [W]), total water-soluble proteins (F = 327.65 [S] and 64.42 [W]) and total carbohydrates (F = 70.90 [S] and 27.62 [W]) showed high significance (p < 0.001). Carotenoids concentration yielded significant results for Halodule in summer and Hypnea in winter (ANOVAs, F = 39.42 and 13.07, respectively). For both, tests revealed that concentration was higher in LUa than HUa. High levels of phycobiliproteins and proteins in this area probably reflect nitrogen accumulation. Frequency and severity of fibropapillomatosis suggest that urbanization-caused alterations in species diversity and in chemical composition of marine plants affect green turtles' health. LIGHT ABSTRACT: The use of coastal areas by humanity is widespread and increasing. The impacts caused to the coastal environment, be it terrestrial, estuarine or marine, are important and affect numerous species. Our study evaluated the influence of environmental degradation on the nutritional value of the main algae eaten by the green turtle, one of the very few marine megaherbivores (those herbivores with body mass above 10 kg). Diet in the highly urbanized area was richer in proteins, lipids and carbohydrates (sugars) and lower in carotenoids (photosynthetic and photoprotectant pigments in algae and plants; precursors of vitamin A involved in oxygen transport in animals-animals do not synthetize such molecules). High levels in phycobiliproteins (photosynthetic pigments present in some algae) and proteins in the highly urbanized area probably result from organic pollution and nitrogen accumulation in coastal waters. Nitrogen compounds dissolved in water are a threat to vertebrates due to its toxicity and negative effects on the immune system. Our results suggest that algae chemical composition and severity of fibropapillomatosis (tumors caused by a herpesvirus in green sea turtles) are directly related through environmental alterations caused by urbanization.

Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil.

The rupture of the Fundão mining dam (Doce river basin, Brazil) caused a wide range of negative impacts. Yet, assemblage-level implications to estuarine and coastal fishes remain unclear, partly due to the lack of pre-disaster information. Based on monthly otter trawl surveys, we analyzed spatial and seasonal variability in univariate (total biomass, biomass of species vulnerable to exploitation, rarefied richness and evenness) and multivariate (species composition and trophic composition) indicators of fish biodiversity in the Doce river delta, eastern Brazil. We determined the independent and interactive effects of environmental, seasonal and spatial variables on species composition to test whether environmental alterations provoked by mine tailings could affect assemblage's organization. Most indicators present idiosyncratic spatiotemporal patterns, suggesting they have complementary roles in revealing changes in fish biodiversity. Environmental variables, including those affected by the Fundão dam collapse such as turbidity, dissolved oxygen and pH, were much more important than seasonal and spatial predictors in explaining the variation in fish species composition. These findings highlight the potential from mine tailings to disrupt local ichthyofauna and indicate a preponderant role of environmental conditions in assemblage structuring. Given the lack of data prior to rupture, our results may be used as a baseline against which to assess temporal trends in fish biodiversity relative to changes detected in less disturbed estuarine and coastal assemblages.

Marine fish assemblages of Eastern Brazil: An update after the world's largest mining disaster and suggestions of functional groups for biomonitoring long-lasting effects.

When the Fundão dam collapsed in Brazil, 50 million m3 of iron ore tailings were released into the Doce river, resulting in the world's largest mining disaster. The contaminated mud was transported 668 km downstream of the Doce river and reached the Atlantic Ocean 17 days after the collapse. Seven months later, there was evidence that the tailings had reached the largest and richest coral reef formation in the South Atlantic Ocean. This study provides the first description of species composition, abundance, and diversity patterns of fish assemblages in estuaries, coastal areas, and coral reefs affected by the rupture of the mining dam in the Doce river. A linear mixed model (GLMM) was used to evaluate the influence of salinity on fish abundance across estuarine and coastal ecosystems. In addition, based on functional traits related to habitat use and feeding habits, this study identified fish species suitable as bioindicators of the long-lasting effects of this major mining disaster. Bottom trawls were used to sample five estuaries and their respective coastal areas, and a visual census was employed to sample five reef areas, representing an impact gradient. A total of 269 species were recorded in all three habitats, but only seven were shared among them. The results showed lower similarity in assemblages among estuarine areas compared to the coastal and reef areas. Species composition among estuaries and reef ecosystems was more heterogeneous. In contrast, coastal habitats exhibited high homogeneity. Salinity had no statistically significant effect on fish abundance either in estuaries (p = 0.22) and along the coast (p = 0.14). Twelve fish species were identified as suitable bioindicators for evaluating the long-lasting effects of resuspension of contaminated sediments. These species are commonly found in the ecosystems under the influence of the disaster inhabiting potentially contaminated substrates and substrate-associated benthic preys.

Effects of seasonal contaminant remobilization on the community trophic dynamics in a Brazilian tropical estuary.

In tropical estuaries, wet seasons are responsible for the downstream transport of allochthonous material from the upper basin and flooded plains. Although allochthonous matter is commonly associated to nutrient and detritus input, pollutants are also transported throughout the basin or suspended from the river bottom via strong streamflow remobilization and rainfall dynamics. We assessed community and population trophic niche-based patterns using organisms' stable isotopes signatures in the wet and the dry seasons to test if estuarine trophic diversity is affected by remobilization of metal-contaminated material from a mining dam collapse that occurred in the Doce river basin, Brazil. Trophic depletion was detected community-wide and in a key consumer group (bottom-dwelling fishes) at the end of the wet season in the impacted Doce river estuary (DRE). Conversely, higher trophic diversity values were recorded in a well-preserved estuary used as control site. Stable isotopes mixing models indicated in the DRE that G. genidens, a predator fish species, presented poor-quality diet based on pollutant-tolerant tiny organisms, a finding that strongly contrasts from diet described in other, little-impacted Brazilian estuaries. Although wet seasons are expected to increase trophic, functional and taxonomic diversity in tropical estuaries, in the DRE the rainfall-driven dynamics poses a threat to the community due to the presence of ore tailings.

Using drones and ROV to assess the vulnerability of marine megafauna to the Fundão tailings dam collapse.

The ecology and life history of marine megafauna can answer the ecological importance of a region. This study assesses and monitors the abundance and home range of sea turtles, seabirds, marine mammals and the association with coastal microhabitats in potentially impacted areas at the Rio Doce river mouth, Comboios, and Piraquê-açu river mouth after the collapse of the Fundão dam. Remotely Operated Vehicles (ROV) and UAVs (Unmanned Aerial Vehicles, or drones) were used for megafauna species identification, behavior, population data, habitat characterization, and monitoring of environmental protection areas. The species Sotalia guianensis and Pontoporia blainvillei were the most recorded cetaceans, and the main observed behavior was feeding. Guiana dolphin (S. guianensis) occurs in greater density in the Rio Doce river mouth region, resulting in more than 10 sightings/km2, while franciscana (P. blainvillei) were the most concentrated Comboios area. The seabirds (all species) had up to 15 sightings/km2 at the Rio Doce river mouth, the highest density among sampled areas. The green turtle (Chelonia mydas) was the most frequently recorded, followed by the leatherback turtle (Dermochelys coriacea). The green turtle occurred at a higher concentration at the Piraquê-Açu river mouth (above 6 sightings/km2). The sites closest to Rio Doce river mouth and Comboios predominantly showed mud bottoms, while those at Piraquê-Açu mouth were mostly reef structures. The estuarine areas showed greater importance for megafauna than marine areas.

Spatiotemporal variations in density and biomass of rocky reef fish in a biogeographic climatic transition zone: trends over 9 years, inside and outside the only nearshore no-take marine-protected area on the southern Brazilian coast.

Biogeographical transition zones are important areas to investigate evolutionary ecological questions, but long-term population monitoring is needed to better understand ecological processes that govern population variations in such edge environments. The southernmost Brazilian rocky reefs are the southern limit of distribution for 96% of the tropical ichthyofauna of the western Atlantic. The Arvoredo Marine Biological Reserve is the only nearshore no-take marine-protected area (MPA) located in this transition zone. The main aim was to investigate how the populations of rocky reef fish species vary in density and biomass in space and over time, inside and outside the Arvoredo MPA. This study presents results based on a 9 year (2008-2017) underwater visual census monitoring study to evaluate the density and biomass of key fish species. Variations in density and biomass were detected for most species. Factors and mechanisms that may have influenced spatial variation are habitat structural complexity and protection from fisheries. Temporal variations, otherwise, may have been influenced by species proximity to their distributional limit, in synergy with density-dependent mechanisms and stochastic winter temperature oscillations. The MPAs harbour higher density and biomass for most species. Nonetheless, a prominent temporal decline in the recruitment of Epinephelus marginatus calls into question the continuous effectiveness of the MPA.

Early evidences of niche shifts in estuarine fishes following one of the world's largest mining dam disasters.

The Fundão dam collapse occurred on November 2015 in Mariana city (Brazil), provoking a series of ecological impacts over the Doce river basin and its nearshore environment. However many impacts over fishery target fauna (fish and shrimp) are still unknown or underestimated due to the lack of baseline data in the region. In the present study we assessed the isotopic niches modeled from δ13C and δ15N signatures of six estuarine fish species before and after the impact to assign potential shifts at the population- and community-level. We showed isotopic niche has altered in all studied species irrespective of its trophic group and habitat use. Niche community metrics indicated a depletion of trophic diversity and basal resources of the whole community after the impact. Food web changes as we reported here can impair the energy transfer through the food chain and put at risk the sustainability of small fisheries that rely upon local resources.

BRUVS reveal locally extinct shark and the way for shark monitoring in Brazilian oceanic islands.

Here we present records of sharks obtained using baited remote underwater stereo-video systems (stereo-BRUVS) at two Brazilian oceanic islands. Fourteen of the 60 deployments recorded 19 sharks in Trindade Island. In Saint Peter and Saint Paul Archipelago (SPSPA), two pelagic and two demersal deployments recorded two and one shark, respectively, including the locally extinct Galapagos shark Carcharhinus galapagensis. Stereo-BRUVS should be considered as adjuncts to other non-invasive methods to monitor shark populations.

Mesophotic ecosystems at Fernando de Noronha Archipelago, Brazil (South-western Atlantic), reveal unique ichthyofauna and need for conservation

Abstract Although several studies on the ichthyofauna of the Fernando de Noronha Archipelago have been carried out, its mesophotic fish diversity has never been surveyed before. Here we used SCUBA and technical rebreather diving, baited remote underwater videos and remotely operated vehicle to record shallow (≤ 30 m depth) and mesophotic (31 to 150 m depth) fishes. Nineteen fish species belonging to 14 families are reported here as new records, representing an increase of 8.2% in marine fish richness for the region, which now has a total of 250 species and 77 families. These new records include four potential new species and highlight the importance of surveying mesophotic ecosystems, even in well studied sites. Our results also emphasize the need for protection and attention to the unique ichthyofauna found at mesophotic depths.(AU)

Resumo Apesar de muitos estudos sobre a ictiofauna do Arquipélago de Fernando de Noronha terem sido realizados, sua diversidade de peixes mesofóticos nunca foi estudada antes. Neste estudo utilizamos mergulho autônomo e mergulho técnico, vídeos subaquáticos remotos com isca e veículo operado remotamente para registrar peixes de ecossistemas rasos (≤ 30 m de profundidade) e mesofóticos (31 a 150 m de profundidade). Dezenove espécies de peixes pertencentes a 14 famílias são apresentadas aqui como novos registros, representando um aumento de 8,2% na riqueza de peixes marinhos da região, que agora possui um total de 250 espécies e 77 famílias. Esses novos registros incluem quatro prováveis novas espécies e reforçam a importância de estudos em ecossistemas mesofóticos. Nossos resultados também enfatizam a necessidade de proteção e atenção à essa ictiofauna única encontrada nesses ecossistemas profundos.(AU)

New records of the snow bass Serranus chionaraia (Perciformes: Serranidae) confirm an established population in the Brazilian Province.

The snow bass Serranus chionaraia is a small-bodied reef fish presumed to be restricted to the Caribbean Province, with a single specimen captured south of the Amazon River mouth. Recent surveys with baited remote underwater stereo-video systems detected the species c. 1900 km southward. Meristic and morphometric characters of two specimens examined in this study confirmed the species identity, which greatly extends the species' range southward on the eastern coast of Brazil and indicates the presence of an established population of S. chionaraia in the Brazilian Province.

Lower diversity of recruits in coastal reef assemblages are associated with higher sea temperatures in the tropical South Atlantic.

Climate change will lead to community shifts and increase the vulnerability of coastal marine ecosystems, but there is yet insufficient detail of how early life stages of marine populations are linked to oceanic-climate dynamics. This study aimed to investigate how ocean-climate variability is associated with spatial and temporal changes in benthic larval recruitment of tropical reef assemblages. Recruitment (abundance, richness, and diversity) of benthic invertebrates was monitored for one year on macroalgal beds in four rocky reefs in a marine protected region in the Eastern coast of Brazil, and compared to fluctuations in meteo-oceanographic conditions at multiple temporal scales (days, weeks, and months). Our results revealed that recruitment of benthic invertebrates varies widely (up to 15 orders of magnitude) among sampled reefs and in time, with wave height, wind speed, and sea temperature being significantly related to recruitment variability. We detected strong taxonomic variability in recruitment success and ocean-climate variables, which highlights the complexity of estimating community vulnerability to climate change in benthic communities. Given that macroalgal beds are key to recruitment of some species regionally (4-30 km), the protection of coastal nursery habitats may be critical for marine conservation and species adaptation in a climate change scenario. Considering the projected ocean-climate change in IPCC scenarios, our study suggests that recruitment of marine populations in coastal reefs could be highly sensitive to climate change in the tropical South Atlantic Ocean.

Remote sensing, isotopic composition and metagenomics analyses revealed Doce River ore plume reached the southern Abrolhos Bank Reefs.

On November 5th, 2015, the Fundão dam rupture released >50 million m3 of ore tailings into the Doce River, Minas Gerais State, Brazil. The huge volume of mud spread along the river and reached the sea, 17 days after the disaster, in Regência, Espírito Santo State (ES). In 2018, after three years of the disaster, the impacts of the ore tailings in the marine environment are still unclear. This study aims to investigate possible short-term impacts in marine biodiversity caused by the ore tailings' mud over the reef ecosystems that are closest to the disaster area: i.e. recently discovered reefs in the southern Abrolhos Bank. A remote sensing surveillance including winds, sea surface temperature, total suspended material and watercolor (MODIS Aqua data) indicated that the iron tailings plume reached the southern portion of Abrolhos Bank on June 16th, 2016. Subsequently, to obtain further evidence of the presence of the tailings in the coral reefs, water samples were collected in a gradient spanning from the river estuary to the reefs in southern Abrolhos Bank, we also analyzed the isotopic and microbial composition of the samples, as well as the reef benthic composition. Despite no clues of negative impact on benthic (coral) communities, isotopic analysis confirmed the presence of the plume over the reefs area. This study serves as a baseline for future long-term impact assessments of the health of coral reefs in the Abrolhos Bank.

Marine debris in Trindade Island, a remote island of the South Atlantic.

Marine debris is widespread in oceans worldwide, including the most remote locations. Here, for the first time, we report macro-debris accumulation on beaches of Trindade Island, a remote island 1160 km from mainland Brazil. High debris density was recorded on windward, east-coast beaches, which are exposed to wind-driven currents. Small-sized plastic fragments were the most abundant debris. Polyethylene (67%), polypropylene (30%) and polyamide (3%) were the most prevalent polymeric materials identified by ATR-FTIR. Identified debris show that interaction with Trindade fauna, mainly with seabirds and endangered terrestrial crabs, exists and already has some impact. This study provides baseline information on Trindade macro-debris demonstrating that the island, located on the edge of the South Atlantic Gyre, acts as a sink for gyre debris, exposing the island fauna to the threats related to plastic contamination.

Endemic fish species structuring oceanic intertidal reef assemblages.

Intertidal reef environments are facing a global crisis as climate changes are causing sea-level rise. Synergistically, other human-induced impacts (e.g., sewage, habitat loss) caused by concentration of human populations near the coast increase the natural vulnerability of intertidal ecosystems. However, the effect of these threats have long been neglected due, in part, to a limited knowledge of some aspects of intertidal fish ecology. We tested what are the main differences and drivers in fish assemblages structure between tidepools in three oceanic and three continental shelf (coastal) sites of the tropical southwestern Atlantic (Brazilian Province) using standardized sampling methods. Oceanic and coastal fish assemblages were distinctly structured at the trophic and composition levels. The noteworthy endemism species rate (38-44%) and high densities in oceanic sites are supported by resident species restricted to mid and high-shore tidepools where herbivores were the major trophic group. The coastal sites, on the other hand, were dominated by widely distributed and carnivore species. Physical (substrate type, pool height, subtidal distance and rock coverage), biological (sessile animal coverage) and chemical (salinity) parameters act as the driving forces influencing fish spatial occupancy. Here, clear evidences of high fish endemism and importance of endemics structuring oceanic communities may act as the last straw in favor of the conservation of oceanic intertidal reefs.

Island biogeography of marine organisms.

Studies on the distribution and evolution of organisms on oceanic islands have advanced towards a dynamic perspective, where terrestrial endemicity results from island geographical aspects and geological history intertwined with sea-level fluctuations. Diversification on these islands may follow neutral models, decreasing over time as niches are filled, or disequilibrium states and progression rules, where richness and endemism rise with the age of the archipelago owing to the splitting of ancestral lineages (cladogenesis). However, marine organisms have received comparatively little scientific attention. Therefore, island and seamount evolutionary processes in the aquatic environment remain unclear. Here we analyse the evolutionary history of reef fishes that are endemic to a volcanic ridge of seamounts and islands to understand their relations to island evolution and sea-level fluctuations. We also test how this evolutionary history fits island biogeography theory. We found that most endemic species have evolved recently (Pleistocene epoch), during a period of recurrent sea-level changes and intermittent connectivity caused by repeated aerial exposure of seamounts, a finding that is consistent with an ephemeral ecological speciation process. Similar to findings for terrestrial biodiversity, our data suggest that the marine speciation rate on islands is negatively correlated with immigration rate. However, because marine species disperse better than terrestrial species, most niches are filled by immigration: speciation increases with the random accumulation of species with low dispersal ability, with few opportunities for in situ cladogenesis and adaptive radiation. Moreover, we confirm that sea-level fluctuations and seamount location play a critical role in marine evolution, mainly by intermittently providing stepping stones for island colonization.