Anthropogenic pollution of aquatic ecosystems: Emerging problems with global implications

Journal Pre-proof Anthropogenic pollution of aquatic ecosystems: Emerging problems with global implications

Donat-P. Häder, Anastazia T. Banaszak, Virginia E. Villafañe, Maite A. Narvarte, Raúl A. González, E. Walter Helbling PII:

S0048-9697(20)30096-6

DOI:

https://doi.org/10.1016/j.scitotenv.2020.136586

Reference:

STOTEN 136586

To appear in:

Science of the Total Environment

Received date:

19 October 2019

Revised date:

5 January 2020

Accepted date:

6 January 2020

Please cite this article as: D.-P. Häder, A.T. Banaszak, V.E. Villafañe, et al., Anthropogenic pollution of aquatic ecosystems: Emerging problems with global implications, Science of the Total Environment (2018), https://doi.org/10.1016/j.scitotenv.2020.136586

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

© 2018 Published by Elsevier.

Journal Pre-proof Submitted to Stoten

Anthropogenic pollution of aquatic ecosystems: emerging problems with global implications Donat-P. Häder1, Anastazia T. Banaszak2, Virginia E. Villafañe3,5, Maite A. Narvarte,3,4 Raúl A. González3,4 and E. Walter Helbling3,5 1

Friedrich-Alexander Universität, Dept. Biology, Neue Str. 9, D-91096 Möhrendorf, Germany

2

Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología,

Universidad Nacional Autónoma de México, Puerto Morelos, México Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina

4

Centro de Investigación Aplicada y Transferencia Tecnológica en Recursos Marinos

ro

of

3

Almirante Storni, Escuela Superior de Ciencias Marinas, Universidad Nacional del Comahue, 5

-p

San Martín 247, (8520) San Antonio Oeste, Río Negro, Argentina Estación de Fotobiología Playa Unión, Casilla de Correos Nº 15, (9103) Rawson, Chubut,

lP

Abstract

re

Argentina

na

Aquatic ecosystems cover over two thirds of our planet and play a pivotal role in stabilizing

Jo ur

the global climate as well as providing a large array of services for a fast-growing human population. However, anthropogenic activities increasingly provoke deleterious impacts in aquatic ecosystems. In this paper we discuss five sources of anthropogenic pollution that affect marine and freshwater ecosystems: sewage, nutrients and terrigenous materials, crude oil, heavy metals and plastics. Using specific locations as examples, we show that land-based anthropogenic activities have repercussions in freshwater and marine environments, and we detail the direct and indirect effects that these pollutants have on a range of aquatic organisms, even when the pollutant source is distant from the sink. While the issues covered here do focus on specific locations, they exemplify emerging problems that are increasingly common around the world. All these issues are in dire need of stricter environmental policies and legislations particularly for pollution at industrial levels, as well as solutions to mitigate the

Journal Pre-proof effects of anthropogenic pollutants and restore the important services provided by aquatic ecosystems for future generations.

Key words: sewage discharge, nutrients, eutrophication, terrigenous material, oil spill, heavy metal pollution, plastic debris.

Introduction

of

The aquatic environment is composed of marine and freshwater ecosystems. Marine

ro

environments cover approximately 71% of the Earth's surface and are comprised of oceans,

-p

estuaries, coral reefs and coastal ecosystems, whereas freshwater ecosystems cover less than

re

1% of the Earth´s surface and are made of up lentic, lotic and wetland ecosystems. Together these environments generate ca 50% of the world´s net primary production (Alexander, 1999).

lP

Even though the standing crop of aquatic primary producers is only about 1% when compared

na

to that of primary producers from terrestrial ecosystems, the former rival their terrestrial counterparts in producing 50% of the biomass, incorporating 50% of the anthropogenically

Jo ur

released CO2 and being responsible for 50% of the oxygen emission on this planet (Rousseaux and Gregg, 2014; Longhurst, et al., 1995). About 90% of anthropogenically-released CO2 is taken up by the oceans (Reid, 2016) and by funnelling excess CO2 to the deep-sea sediments, via the biological pump, they help to mitigate global change (Hain, et al., 2014). Aquatic ecosystems are exploited to provide food, transportation and recreation. Marine ecosystems also provide ingredients for fertilizers, additives and cosmetics, whereas freshwater ecosystems are utilized to provision water for drinking, sanitation, and agricultural and industrial uses. Anthropogenic activities are severely impacting aquatic ecosystems, which are also increasingly affected by global change, urban and tourism developments and the unsustainable exploitation of aquatic resources. Pollution of water bodies from agricultural, industrial and urban runoffs and waste disposal jeopardize the supply of clean

Journal Pre-proof drinking water and have negative impacts on marine and freshwater organisms (Verhougstraete, et al., 2015; Beiras, 2018). Coastal areas make up approximately 7% of marine environments but due to their high primary productivity they provide over 50% of food for ocean ecosystems (Alexander, 1999), yet they are also highly impacted by pollutants. In this assessment we consider emerging problems that are exemplified at specific locations or hotspots to highlight the effects of pollution in coastal and open ocean habitats and evaluate their effects on marine organisms. Additionally, for each case, we analyzed the

of

factors that contribute to the seriousness of the problem, including the source, dispersal

ro

mechanism, persistence, geographical extension, feasibility of control/mitigation, among

-p

others. The five examples we present here serve as indicators of a more widespread set of

re

problems related to pollution that is directly caused by anthropogenic activities around the globe, both at consumer and at industrial levels. These examples cover most of the

lP

anthropogenic pollutants and can be extrapolated to other systems as in most cases the

na

mechanisms and potential solutions are common. As a first example, we highlight the impact of inadequately treated sewage discharge on coral reefs in the Mexican Caribbean. This has

Jo ur

led to eutrophication of the once pristine waters surrounding coral reefs that in turn has provoked phase shifts to a macroalgal-dominated ecosystem (Bruno, et al., 2009) as well as recent Sargassum blooms (Wang, et al., 2019). Next, we show that wind and terrestrial runoff transport dissolved organic matter (DOM), fertilizers and pesticides, pharmaceuticals and heavy metals into rivers, estuaries and coastal waters (Paches, et al., 2019), thus carrying point source pollutants to other ecosystems. We use two case studies to highlight these issues. In the first example, we focus on riverine and eolic inputs of nutrients and terrigenous material into coastal ecosystems and how they affect phytoplankton communities in the highly productive waters of Patagonia. We then focus on heavy metal pollution from past mining activities in Patagonia that has been detected downstream in marine sediments and salt marshes and that impacts a range of plant and animal species. We continue with crude oil spills that are not

Journal Pre-proof only restricted to accidents such as the Exxon Valdez grounding or the Deepwater Horizon blowup in the Gulf of Mexico (Gill, et al., 2016; Beyer, et al., 2016). Smaller, but more frequent oil spills and inadvertent or intentional dumping of crude oil or its products are released in coastal as well as in open ocean ecosystems. These spills and the dispersants used to dissolve them are harmful to a large variety of aquatic organisms. Finally, we focus on the global problem of plastic pollution. Land-based plastics are transported by rivers, sewers and storm runoff and can be blown from coastal environments into the oceans due to inadequate

of

waste disposal (Derraik, 2002). Another source of plastic pollution is ocean-based via the

ro

fishing, shipping, and aquaculture industries and plastic waste that is dumped by cruise ships

-p

(Derraik, 2002). Large concentrations of plastics have accumulated in the ocean and threaten

re

marine life from plankton to fish and mammals (Avio, et al., 2017). These plastics, on exposure to ultraviolet solar radiation break down into microplastics (<5 mm diameter), which

lP

can be directly ingested by aquatic organisms causing adverse effects on health, whereas the

na

indirect effects of microplastics are due to their ability to absorb hydrophobic pollutants, which then enter the food chain (Chatterjee and Sharma, 2019). Nanoplastics, used widely in

Jo ur

the cosmetic industry are also found in the food chain (Koelmans, et al., 2015). The types of pollution considered here are compared and contrasted in Table 1. In most cases the main source of pollution is industrial rather than being derived from household use. Nevertheless, even though plastic pollution comes from industrial activities (oil, mining, agriculture) or urban waste, the pollution generated by the habits of individual consumers is still relevant. The dispersal of the pollutants is mostly water- or wind-driven. The discharge of these pollutants into the aquatic system ranges from sporadic to continuous, and their persistence ranges from days to centuries. The differences, however, do not imply that one is less harmful than another, because all of them cause negative impacts to aquatic ecosystems. Where strict laws or regulations do not exist, actions must be taken to help to mitigate their impact.

Journal Pre-proof

Sewage discharge on coral reefs in the Mexican Caribbean Tropical coral reef ecosystems are highly biodiverse, providing habitat to more than 30% of marine species, while only occupying approximately 0.1% of the ocean surface (Spalding and Grenfell, 1997). Coral reefs also provide ecosystem services that include coastal protection from storms and hurricanes, fisheries, pharmaceuticals and tourism, with a global value of 36 billion USD per year just from tourism (Spalding, et al., 2017). However, coral reef habitats

of

are degrading at a rate of 1.5% per year, calculated between 1977 and 2001 (Jackson, et al.,

ro

2014). Anthropogenic factors such as rising sea surface temperatures due to climate change,

-p

coastal development, overfishing as well as land-based pollutants such as sewage discharge

re

(Wear and Thurber, 2015) are the most important drivers of coral reef degradation (Burke, et al., 2011). Sewage discharge can be composed of household, municipal and industrial

lP

wastewaters. In the Mexican Caribbean, sewage is derived mostly from households and the

na

tourism industry, and while some is released in a partially treated form, most is untreated (Wear and Thurber, 2015; UNEP, 1994).

Jo ur

Sewage effluents, when improperly treated or worse, untreated, that are discharged close to coral reefs are harmful. The degree of effects will depend on the level of treatment the sewage undergoes prior to discharge, the periodicity and volume of the discharge as well as the predominant hydrographic regime governing the site(s) of discharge. The effects are greater when the discharges are chronic, high volume and close to coral reefs located in areas that are not well flushed (Pastorok and Bilyard, 1985). Such is the case in the Mexican Caribbean where coral reefs are located close to the coastline and coastal developments, which are exposed to intense levels of tourism, and associated pollution. As an example, the city of Cancun grew from 150 inhabitants in 1970 (Rioja-Nieto, et al., 2019) to an estimated 750,000

inhabitants

in

2017

(http://worldpopulationreview.com/world-cities/cancun-

population/; data retrieved on 28th September 2019). This 5,000-fold increase in the

Journal Pre-proof population in 47 years, combined with the explosion of tourism to the area (e.g. in 2017, Cancun International airport received 7,612,489 tourists (SECTUR, 2019), has added stress onto the limited capacity of the existing sewage treatment plants in the area (Rioja-Nieto, et al., 2019). A common practice is to inject sewage to depths of 90 m or more below the freshwater lens. However, given that the topography of the Yucatan Peninsula is made up of highly permeable limestone deposits known as karst topography (Rioja-Nieto, et al., 2019), the

of

sewage can travel through the underground aquifer system. Consequently, the sewage is

ro

discharged directly through seeps and blue holes into the ocean close to the coral reefs that are

-p

part of the Mesoamerican Reef System as detected using radium isotopes (Hernández-

re

Terrones, et al., 2015). Metcalfe et al. (2011) discovered contaminants in a series of aquifers that feed into coastal waters, which included caffeine, pharmaceuticals, illicit drugs and

lP

personal care products, derived from domestic sewage.

na

The typical components of sewage discharge are freshwater, endocrine disruptors, sediments, pathogens and nutrients (Pastorok and Bilyard, 1985; Wear and Thurber, 2015)

Jo ur

each of which are potentially toxic to corals (van Dam, et al., 2011) or have negative impacts on physiological processes ranging from coral reproduction, photosynthesis, calcification, and growth (van Dam, et al., 2011). Freshwater inputs can kill corals when exposed to prolonged (>24h) reduced salinity (Jokiel, et al., 1993). Endocrine disruptors affect coral physiology resulting in decreased growth rates and reduced reproductive viability (Pastorok and Bilyard, 1985). Sediments are also known to negatively affect corals through reduced growth and calcification and increased mortality. Effects at the community and ecosystem levels in coral cover and accretion rates, respectively, have also been detected (Fabricius, 2005). Pathogens including enteric bacteria have been detected in seawater close to shore in various sites along the Mexican Caribbean (Munro, et al., 1999). The fecal enterobacterium Serratia marcescens has been identified as the etiological agent of white pox disease that impacts Acropora

Journal Pre-proof palmata, a major Caribbean reef-building coral on the International Union for Conservation of Nature (IUCN) red list (Sutherland, et al., 2010). Nutrient enrichment has also been shown to significantly increase the prevalence of aspergillosis in the Caribbean Sea Fan Gorgonia ventalina and yellow band disease in the Caribbean reef-building corals Orbicella (=Montastraea) annularis and O. franksii (Berg, et al., 2016)). Eutrophication due to the high nutrient content in sewage enhances algal and cyanobacterial growth, which over the shortterm compete with corals by reducing larval recruitment, coral growth and survival (Fabricius,

of

2005; Vega Thurber, et al., 2014; Wagner, et al., 2010) and over the long-term can lead to

ro

phase shifts from coral-dominated to algal-dominated reefs (Bruno, et al., 2009; Suchley, et

-p

al., 2016). This occurs because corals thrive in warm oligotrophic (nutrient-poor) seawater

re

due to the tight nutrient recycling association they have with symbiotic algae and when the surrounding seawater becomes nutrient rich the growth of macroalgae is favored.

lP

In addition, local sources of nutrients exacerbate Sargassum blooms, which have

na

caused major problems recently throughout the wider Caribbean (van Tussenbroek, et al., 2017). These large mats of pelagic Sargassum carry with them a diverse array of associated

Jo ur

biota that use the Sargassum as a habitat and refuge (Butler, et al., 1983). Once the floating mats reach the coast, they strand, accumulate and decompose on the shoreline (Fig. 1A) with the organic breakdown products causing increased turbidity and a brown-tide (van Tussenbroek, et al., 2017, Fig. 1B) for hundreds of meters offshore (Rodriguez-Martinez, et al., 2019). Consequently, the browning provokes mortality of near-shore seagrasses and corals (van Tussenbroek, et al., 2017) as well as demersal neritic fish and crustacea, due to hypoxic conditions and high ammonium and hydrogen sulphide concentrations (Rodriguez-Martinez, et al., 2019). In addition, heavy machinery has been contracted to remove tons of Sargassum from the shoreline and mostly disposed off kilometers inland in abandoned quarries, without a geo-membrane to prevent the degradation products from leaching into the underground aquifer system. Potentially, this is a major source of nutrient pollution that could reach the

Journal Pre-proof coral reef system through the underground network, thus exacerbating the already nutrientenriched coral reef ecosystem. The projected increases in local populations and tourism will intensify the pressures on coral reefs from sewage discharge in the Mexican Caribbean. Stricter management actions are required to prevent and mitigate the damage to the aquatic environment through eutrophication and potentially to human health. The groundwater system is used for human consumption and as the population and tourism increases the groundwater levels reduce.

of

Sewage and wastewater are also injected deep into the underground aquifer system, which

ro

means that if they are not adequately treated prior to release there is an ever-increasing

-p

possibility that the water will be contaminated by faecal bacteria that will affect human health.

re

The continued lack of, or at its best, inadequate treatment of sewage that is discharged into the underground aquifer system could potentially result in the complete collapse of the

lP

coral reef ecosystem in the Mexican Caribbean. To prevent such a catastrophe, the law that

na

establishes the maximal allowable limits in wastewater discharge into water bodies (NOM001-SEMARNAT-2017) must be adopted to ensure tertiary level treatment of sewage before

Jo ur

it is discharged into the underground aquifers close to coral reefs. Municipal governments must also 1) markedly improve the wastewater treatment infrastructure to ensure it can effectively treat sewage considering the projected population and tourism increases, 2) guarantee that the local populations have affordable access to the drainage system and 3) to monitor and manage sewage discharge using best available management practices to reduce the serious threats of sewage pollution near coral reef ecosystems.

Riverine and eolic inputs of terrigenous material and its effects on coastal Patagonia phytoplankton The coastal South West Atlantic Ocean (SWAO) waters are responsible not only for one of the highest production levels of the World’s ocean (Longhurst, et al., 1995; 1998), but they are

Journal Pre-proof also important sites for nursery, recruitment and breeding of fishing resources and flagship species (IWC, 2013). Therefore, there is an increasing interest to evaluate the future of these aquatic systems in the context of global change, including anthropogenic activities. While several variables are already changing (or expected to change in the future), one of the least explored is the input of terrigenous material in the form of both particulate (organic and inorganic) and dissolved organic matter (DOM) into the coastal SWAO system. In the past years, extreme rain events in terms of intensity and frequency as well as

of

changes in wind patterns (Bermejo, et al., 2018; Pessacg, et al., 2015; Bilmes, et al., 2016) in

ro

Patagonia have resulted in more terrigenous materials added to the coastal ecosystems as

-p

measured by dissolved organic carbon (DOC) than has been recorded previously. Such is the

re

case of the Chubut River (Chubut Province, Argentina) (Fig. 2), which also carries sewage and waste water effluents from the growing cities located on the river banks. Altered and more

lP

intense land use contributes nutrients (nitrogen and phosphorus) from agriculture and from

na

new fish-factories located at the mouth of the Chubut River estuary (Bermejo, et al., 2018), all of which eventually reach the coastal ecosystem. Additionally, open caolin (Al2Si2O5(OH)4)

Jo ur

mines are located upstream close to the Chubut River (Galazzo, et al., 1985; Cravero, et al., 1991) releasing high amounts of clay mineral to the coastal areas. All these materials not only affect the aquatic biota, but also have a direct impact on the human population, as the water cannot be treated adequately for consumption. Wind also carries high amounts of terrigenous materials, either as Patagonian dust (Johnson, et al., 2011) or as particles and aerosols originating from volcano eruptions in the Andes (Acker and Leptoukh, 2007). The concentration of particles that reaches aquatic bodies, which depends on the combination of the aerosol index (AI, Fig. 3A) and the numbers of events that occur within a year, has undergone a continuous increase over the past 20 years (Fig. 3B). Increased levels of terrigenous material and DOM have a dual effect. On the one hand they affect the physical properties of the water column, enhancing turbidity and reducing

Journal Pre-proof penetration of solar radiation available for photosynthesis. On the other hand, they also alter the chemical properties of the water body, as DOM especially (and Patagonian dust, to a lesser extent) carry nutrients which tend to favor growth of phytoplankton (Paparazzo, et al., 2018; UNEP, 2012; Rabalais, et al., 2009), especially if they are limiting in the system. This dual role of DOM under simulated conditions of global change was investigated on a post-bloom natural phytoplankton community from the Chubut River estuary (Villafañe, et al., 2018). It was found that future concentrations of higher DOM and nutrients, and of lower pH,

of

stimulated phytoplankton growth, when compared to present day conditions. However, when

ro

comparing these dual roles of DOM under future conditions, the photosynthetic efficiency of

-p

phytoplankton cells was lower when DOM acted as a source of nutrients as compared to that

re

in a more turbid environment (i.e., DOM as attenuator). This mismatch among the two roles of DOM could be due to the formation of more free radicals in the presence of increased

lP

nutrients such that the cells have to cope with increased concentrations of reactive oxygen

na

species in detriment to other metabolic processes. On the other hand, increased terrigenous material and DOM would favor smaller cells mainly due to a reduction of solar radiation

Jo ur

levels. Other studies have shown that the addition of nutrients from both eolic and riverine origin decrease the CO2 sink capacity of the SWAO by as much as 27% (Cabrerizo, et al., 2018) due to higher UVR-induced inhibition together with a shift in the community towards small nanoflagellates. Similar results were found when comparing the responses of two communities occurring along the seasonal succession in which growth was stimulated by the addition of DOM and nutrients, but cells were photosynthetically less efficient (Vizzo, et al., 2019). Overall, these changes in the structure and physiology (mainly photosynthesis) of natural phytoplankton communities due to the input of higher amounts of terrigenous materials will have a great impact on the trophodynamics in coastal Patagonian ecosystems. The lack of thorough waste management and the fact that sewage is dumped directly into the ground via poorly designed septic tanks results in contaminated terrigenous material

Journal Pre-proof reaching the river and coastal ecosystems. A strict control of these issues would decrease the harmful impact of this terrigenous material. In addition, all sewage should have adequate pretreatments before being dumped into the river/ground, and a continuous monitoring of several variables in the river and discharges should be enforced.

Heavy metal pollution in salt marshes of Patagonia Although the term Patagonia evokes images of a pristine, huge, wild regions, marine pollution

of

has been evident in the last decades. Compared to most coastal areas, the human population

ro

density along the Patagonian coast is extremely low (less than 4 people km-2), although the

-p

populations are concentrated in nine cities ranging from 50,000 to 100,000 persons each

re

(INDEC, 2010). Unplanned urban development coupled with scarcely controlled industrial activities (e.g., sewage enriched with carbonates or the effluent of fishing companies), have

lP

led to severe impacts on the coastal zone. The sources of the impacts include urban waste,

na

extraction and transport by the petroleum and gas industry, port and maritime traffic, mining, fishing and tourism. Some strategic initiatives to mitigate environmental pollution and

Jo ur

improve the management of marine and coastal resources have been implemented since the mid-1990s (http://www.patagonianatural.org/proyectos/pmzcp-2). However, these efforts have been undermined by the inability of governments of the coastal states to sustain long-term policies and effective actions, and pollutants of great concern, such as heavy metals, are still problematic. The concentration of five heavy metals (mercury, cadmium, copper, lead and zinc) in marine sediments were studied at 19 sampling points (including 11 cities) along 4,400 km of the Patagonian coast, with Comodoro Rivadavia and San Antonio Oeste having the highest levels, reflecting anthropogenic pollution (Commendatore, et al., 1996; Gil, et al., 2006) (Fig. 4A). Mine tailings are the most important sources of heavy metal pollution, especially lead and zinc, from abandoned mining activities initiated before 1970. Mine tailings are wastes left

Journal Pre-proof over after extraction of the mineral product from ore-bearing rock, and apart from crushed rocks, they contain potentially harmful substances, such as heavy metals and remnants of chemicals. Since tailings have been stored inland near the San Antonio Bay (North Patagonia, Argentina, Fig. 4B), the pollution is not only local, but has also affected areas within 10 km from the deposits. The release of metals has resulted in significant levels of lead and zinc in sediments and the marine biota along the San Antonio Bay channel, particularly in the intertidal zone (Idaszkin, et al., 2017; Marinho, 2017). Although metal mining has ceased in

of

the coastal zone and there are no new mine tailings, lead and zinc pollution still affects the sea

ro

bottom in the vicinity of the polluted sites.

-p

San Antonio Bay (SAB) is a salt marsh with high biodiversity that sustains ecosystem

re

services such as fisheries and tourism. Like other salt marshes and mudflats, this site is low, wet and muddy lying at the interface between land and sea (Fig. 4C). The tidal regime is

lP

semidiurnal and macrotidal, with an amplitude of nearly 9 m; hence more than 90% of its

na

surface is uncovered at each tide. Its shores are relatively complex due to the variety of habitats formed across the vast intertidal zone. Except for sporadic and heavy precipitation, no

Jo ur

freshwater is discharged into the bay, creating an extreme habitat in spring and summer for the inhabitants due to the lack of water. The bay and surrounding sites, which were proclaimed a Marine Protected Area in 1993, contain different structural zones and habitats at the land-sea interface for terrestrial and aquatic organisms (algae, mollusks, crabs and fish) that interact in complex ways. Besides its continuous supply of dead organic matter that is degraded by bacteria to detritus, marsh vegetation also provides protection and food for different species that use the ecosystem as a nursery ground (Perier, 1994). Several species of fish and crabs move through the flats at high tide. Resident and migratory birds (penguins, puffins) and marine mammals (southern sea lion, southern right whale, bottlenose dolphin) frequently visit the tidal flats for feeding, resting or as part of their migratory routes (Svendsen, 2013). The SAB´s heavy metal pollution has been of great concern, not only because of the

Journal Pre-proof inherent toxicity, widespread sources, persistence, and non-degradability, but also because it may be an important source of human exposure via respiration of polluted atmospheric dust (Caramuto, et al., 2009). The sediments have been used as indicators of metal pollution and several biomonitors have been employed to evaluate the levels of trace elements in the ecosystem. For example, local areas that sustain mollusk production has been monitored for lead, mercury, zinc, cadmium, and arsenic since 2003 (SENASA, 2019) and the presence of these heavy metals is controlled in fish and crustacean products. In 2008, a remediation

of

process of the Patagonian metal hotspot began and while the polluted areas near the bay have

ro

been reduced dramatically (https://multisectorialplomo.org), the chronic effects on the coastal

-p

zone will remain for many years.

re

Metal bioaccumulation, both in salt-marsh plants and common marine invertebrates of the region (bivalves, snails and crabs), has been demonstrated (Marinho, 2017).

lP

Environmental conditions in the affected zone, such as temperature, redox potential, organic

na

complexation, concentrations of metal and ligand species, pH, general physiological behavior and life histories (Li, et al., 2019) may also play a role in the metal concentrations of the

Jo ur

biological systems in this hotspot. Metals affect animal health as carcinogens through oxidative mechanisms by generating free radicals and reactive oxygen species, which attack and damage DNA and enzymes (Bal and Kasprzak, 2002). Since metal ions can penetrate into the cell, they can interrupt cellular metabolism and, in some cases, enter the nucleus, producing direct DNA damage and also affecting nuclear chromatin (Le Croizier, et al., 2018). Although some research on the metal bioaccumulation has been performed in invertebrates, ecotoxicological effects have not been specifically studied for the local fauna. In the context of global warming and related environmental change, contaminant pathways and biological systems are affected. Mining wastes deposited on land from previous human activities are being remediated but, in the meanwhile, high concentrations will continue to affect some marine organisms and coastal sediments, due to increased

Journal Pre-proof precipitation rates in the scenario predicted for this area (Marcovecchio, et al., 2019; Barros and Camilloni, 2016). New heavy metal discharges into the environment from human activities related to climate change can also be expected from growing shipping traffic and oil and gas activities in the coastal Patagonian zones (Conti, et al., 2011; Duarte, et al., 2012). Further, climate change could influence the food web structure and affect contaminant cycles through new contaminant interactions, which may alter bioaccumulation (Alava, et al., 2017). Unfortunately, there are no integrated studies or models showing the change in precipitation

of

rate and its effects on metal contaminant levels in phytoplankton, zooplankton, the trophic

ro

structure and the overall system, with the exception of the Bahía Blanca estuary (to the north

-p

of the SAB region) (Fernández-Severini, et al., 2013). National and international efforts to

re

control or reduce global effluents, as well as initiatives to make a more adequate use of the ocean realm (e.g. Marine Spatial Planning) are therefore increasingly essential. In the

lP

meantime, considering the predicted climate change scenarios (IPCC, 2019), we recommend

na

to conduct an international initiative of a global survey to identify, map and remediate other

Jo ur

coastal heavy metal hotspots.

Crude oil spills in the Gulf of Mexico Catastrophic disasters such as the Exxon Valdez grounding in Prince William Sound, Alaska in 1989, alerted the public about the ecological impacts of crude oil spills (Camilli, et al., 2010). About 20% (37,000 metric tonnes) of its cargo was released. However, very large crude carriers can hold up to 150,000 tonnes and ultra-large carriers up to 306,000 tonnes (Fingas, 2016). Accidental spills due to storms, earthquakes, mechanical failure or human error accumulate to much larger total losses. In addition, it is estimated that about 47% of oil released into the oceans stems from natural seepage and amounts to about 600,000 metric tonnes per year (Kvenvolden and Cooper, 2003). The Deepwater Horizon blowout in 2010, in the Gulf of Mexico, released millions of

Journal Pre-proof barrels of crude oil (Forth, et al., 2017) that included components toxic to marine organisms. In addition to immediate mortality, sublethal damage can lead to impaired recovery and population reductions in many animal taxa (Peterson, et al., 2003). Water samples taken after the Deepwater Horizon accident showed that 3 of 14 stations sampled (21%) were toxic to bacteria (Microtox assay), 4 of 14 stations sampled (34%) were toxic to phytoplankton (QwikLite assay) and 6 of 14 stations samples (43%) induced DNA damage (λ-Microscreen Prophage induction assay) (Paul, et al., 2013). Toxicity of the contaminated water could be

of

found at least 1.5 years after the accident and effects were still being registered in salt marsh

ro

and polychaete recovery up to 6.5 years after the spill (Fleeger, et al., 2018).

-p

Crude oil affects heart development (Incardona, et al., 2014) and interferes with the

re

cardiac activity in fish (Brette, et al., 2014). Components of crude oil such as polycyclic aromatic substances are agonists of the aryl hydrocarbon receptor as are dioxins (Incardona,

lP

2017). In seabirds, crude oil pollutes the plumage, which results in impaired flying and

na

thermal insulation. Birds try to remove it from their feathers resulting in ingestion of the oil, which affects hepatic antioxidant enzymes, decreases the hemoglobin concentration and

Jo ur

results in increased liver weight (Harr, et al., 2017; Bursian, et al., 2017). Exposure to oilcontaminated seawater was shown to affect coral larval settlement of two species (Agaricia humilis and Orbicella faveolata) with likely repercussions on coral recruitment, such that the deleterious effects of the oil spill continue long after exposure is over (Hartmann, et al., 2015). One remedy to remove oil spills is to apply dispersants to break down the droplet size and dissolve it into the water. After the Deepwater Horizon accident almost 7 million liters of the dispersant Corexit 9500A were distributed in the Gulf of Mexico (Jasperse, et al., 2018). However, the dispersant is highly cytotoxic and genotoxic, as are the crude oil compounds, to zooplankton such as the oligotrich ciliate Strombidium, tintinnic ciliates such as Eutintinnus and dinoflagellates (Almeda, et al., 2014) as well as oysters (Jasperse, et al., 2018). The toxins enter higher trophic levels by predation and spread throughout the entire food web. Coral reef

Journal Pre-proof larvae are also affected by crude oil components and natural gas (Negri, et al., 2016); a concentration of about 100 µg/L fully blocked the metamorphosis of the larvae of Acropora tenuis. Exposure to solar UV augmented the sensitivity of these corals. The dispersant used after the Deepwater Horizon blowup was even found to be cytotoxic and genotoxic to sperm whale skin cells (Wise, et al., 2014). Eventually microbial degradation breaks down crude oil components such as alkanes and aromatic hydrocarbons (Kleindienst, et al., 2015b). These hydrocarbonoclastic bacteria

of

are ubiquitous in the oceans, but in order to enhance the breakdown of the chemicals it was

ro

suggested to spread cultures at the polluted site (Ron and Rosenberg, 2014). Since these

-p

bacteria need nitrogen and phosphorous, it was recommended to seed the water with fertilizers

re

such as uric acid (Hong, et al., 2016). Unfortunately, the chemical dispersants impair the crude oil-degrading prokaryotes and alter the bacterial community structure (Kleindienst, et al.,

lP

2015a). For example, the marine Marinobacter grew well in the presence of crude oil, but

na

growth was impaired by the addition of the dispersant.

Jo ur

Plastic pollution in the marine environment Over 8 million tons of mostly single-use plastics enter the ocean each year (https://plasticoceans.org/the-facts/), despite the existence of recycling and awareness campaigns all around the world. While the sources of the plastics are difficult to pinpoint, it has been estimated that every year between 1.15 and 2.41 million tons of plastic is carried by rivers to the sea (Réu, et al., 2019). Most of the top polluting rivers are located in Asia, such as the Yangtze and the Pearl River, which are responsible for 67% of the total plastic that ends up in the oceans (Lebreton, et al., 2017). Other sources of plastics in the marine environment include aquaculture, shipping and fishing activities, sewer and storm runoff, as well as transport of beach litter and debris by wind (Kershaw and Rochman, 2015). Nanoplastics (size range from 1 to 1000 nm) used in the cosmetics industry, particles from tire wear and

Journal Pre-proof shedding of microfibers from synthetic clothing also end up in the ocean (Barboza, et al., 2018b). Most of the plastic is durable and is fragmented by the action of waves and sand into microplastics (Hermsen, et al., 2018). Plastic debris that floats or is found on beaches becomes brittle due to autocatalytic oxidation in the presence of solar ultraviolet radiation, into microplastics (Müller, et al., 2018). Due to their small size, microplastics are highly bioavailable and easily ingested by aquatic organisms such as mollusks, echinoderms, corals,

of

larval stages of vertebrates, green sea turtle, cetaceans and seabirds causing adverse effects on

ro

health (Botterell, et al., 2019; Caron, et al., 2018). An assessment of 34 commercial fish

-p

species in the South Pacific subtropical gyre revealed that plastic was ingested by all but one

re

species and then transferred from prey to predators (Markic, et al., 2018). Another study (Setälä, et al., 2018) showed that 33% of the gooseneck barnacles (Lepas spp.) ingested

lP

between 1 and 30 microplastic particles. Microplastics in the marine environment inevitably

na

end up in seafood such as fish, bivalves and crustaceans (Gallo, et al., 2018). For example, Barboza (2018b) reported that in the fingerprint oyster Alectryonella plicatula ~11

Jo ur

microplastic particles were found per organism with a size range of 5–5000 µm. In North Sea herrings (Clupea harengus) 566 particles were counted in the gastrointestinal tract with sizes >1 mm, and in the cod Gadus morhua 80 particles of similar size were found in the gastrointestinal tract. While the gastrointestinal tract of commercial fish is usually not consumed and therefore humans may not directly be affected, mollusks and some crustaceans as well as small or juvenile fish are eaten whole so that the plastic debris is transferred. However, microplastics have recently been detected in the muscle of commercially important fish species including Platycephalus indicus, Saurida tumbil, Sillago sihama, Cynoglossus abbreviatus as well as in the exoskeleton and muscle of the tiger prawn Penaeus semisulcatus (Abbasi, et al., 2018), resulting in potential consumption by humans. Plastic debris may transport toxic pollutants either intentionally added during

Journal Pre-proof production or absorbed to the surface during their use and persistence in the environment. These substances include toxic metals such as mercury, styrene, phthalates, bisphenol A, polychlorinated biphenyls and polycyclic aromatic hydrocarbons (Barboza, et al., 2018a; Barboza, et al., 2018c). Some of these chemicals are regarded as very toxic to animals and humans and act as carcinogens, endocrine disruptors and neurotoxins (Hahladakis, et al., 2018). Therefore, microplastics pose a serious threat to the biota and human health because of its mechanical effects e.g. on membranes as well as the toxic effects of chemicals adsorbed to

of

the particles. In addition to chemicals, bacteria and other microorganisms have been found to

ro

be attached to plastic particles which may be carried to distant locations as introduced

-p

pathogens (Keswani, et al., 2016). Exposure to microplastics in laboratory experiments

re

involving marine organisms can result in mortality (Luis, et al., 2015, Gray and Weinstein, 2017) or reduced feeding, body mass and metabolic rate (Welden and Cowie, 2016). It may

lP

affect predatory performance (de Sá, et al., 2015), behavioral responses and reduced

na

swimming rate (Barboza, et al., 2018a). In addition, decreased fertilization and larval abnormalities have been observed (Martínez-Gómez, et al., 2017). Exposure can also result in

Jo ur

neurotoxicity due to acetylcholinesterase inhibition and oxidative damage (Oliveira, et al., 2013; Avio, et al., 2015; Ribeiro, et al., 2017) and other deleterious effects (Barboza, et al., 2018c).

While there is much information on the effects of plastics on marine organisms, the knowledge of potential effects on human health is still in its infancy and controversial (Barboza, et al., 2018b); however, we do know that particles larger than 150 µm will probably not be absorbed by the human body but smaller ones (≤ 20 µm) may penetrate into inner organs and even smaller fragments (0.1–10 µm) may cross cell membranes, the blood-brain barrier and the placenta and thus trigger immunosuppression and inflammations (Lusher, 2015). Because of growing amounts of plastic debris and its serious effects on many marine

Journal Pre-proof organisms, urgent measures are needed to prevent further littering of the oceans and the removal of this material which has a long lifetime. Actually some countries are taking measures to reduce plastic pollution by recycling the material, outlawing plastic bags or banning the use of nanoplastics in cosmetics (Schwartz, et al., 2019; Guerranti, et al., 2019). Another promising approach is to collect plastic debris in the oceanic gyres by ships and convert it to fuel to drive vessels (https://resource-recycling.com/plastics/2019/10/16/plastics-

of

to-fuel-powered-ships-will-collect-marine-debris/).

ro

Final remarks

-p

In this review, we give specific examples of how some pollutants from anthropogenic origin

re

can affect marine organisms and ecosystems. All marine ecosystems are potentially vulnerable, even in rather remote and pristine sites that do not produce large amounts of

lP

pollutants and are located away from large cities. This is because the sea and the atmosphere

na

are effective transportation systems (Table 1), carrying a huge number of substances in the form of diverse chemicals, sewage, etc. even to remote areas.

Jo ur

While the five examples of marine pollution discussed in this review differ from each other basically by the kind of pollutant, the environment and the regional context in which they occur (Table 1), all affect coastal freshwater and marine ecosystems. Globally, the marine coastal domain contributes 30% (Longhurst, et al., 1995) of the primary sea production and supports the two most important material and non-material areas (fishing and tourism, respectively) (Nature Contribution to People (NCP, sensu Díaz 2018)). The human population is projected to increase by 50% to 122% in the period 20302060 (Neumann, et al., 2015) along coastal ecosystems worldwide, which will exacerbate pollution problems. In the future scenario, coastal societies should not only address the problem of pollution but also the issues arising from a greater demand for marine resources for food, more developments to accommodate higher tourism activities and the sea level rise

Journal Pre-proof expected by climate change effects. An urgent need is for adequate regulation and legislation, as well as the adoption of best practices and proper mechanisms to minimize the disposal of pollutants into the marine system, such as better waste treatment and efficient remediation projects. Although there are international legal agreements and instruments to address some of the marine pollution sources, the magnitude and complexity that this problem has taken in recent years and its expected aggravation, determine the need to review and adapt the multiple existing

of

international instruments at the highest level to deal with the aquatic pollution problem in a

-p

ro

more effective way.

Acknowledgments

re

This work was supported by Agencia Nacional de Promoción Científica y Tecnológica -

lP

ANPCyT (PICT 2015-0462 and PICT 2017-0411), Consejo Nacional de Investigaciones

na

Científicas y Técnicas - CONICET and Fundación Playa Unión, Contribution N° xx of Estación de Fotobiología Playa Unión. ATB thanks M. en C. Laura Celis for help with

Jo ur

literature searches, to the Servicio Académico de Monitoreo Meteorológico y Oceanográfico for supplying photos for Figure 1. Funding was provided to ATB by UNAM-ICML project No. 608. We thank the comments of two anonymous reviewers that helped us to greatly improve our manuscript.

References Abbasi, S., Soltani, N., Keshavarzi, B., Moore, F., Turner, A., Hassanaghaei, M., 2018. Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian Gulf. Chemosphere 205, 80-87. Acker, J.G., Leptoukh, G., 2007. Online analysis enhance NASA Earth science data. EOS, Transactions American Geophysical Union 88, 14-17. Alava, J.J., Cheung, W.W., Ross, P.S., Sumaila, U.R., 2017. Climate change–contaminant interactions in marine food webs: Toward a conceptual framework. Global Change Biology 23(10), 3984-4001. Alexander, D.E., 1999. Encyclopedia of Environmental ScienceSpringer. Almeda, R., Hyatt, C., Buskey, E.J., 2014. Toxicity of dispersant Corexit 9500A and crude oil

Journal Pre-proof

Jo ur

na

lP

re

-p

ro

of

to marine microzooplankton. Ecotoxicology and Environmental Safety 106, 76-85. Avio, C.G., Gorbi, S., Regoli, F., 2017. Plastics and microplastics in the oceans: From emerging pollutants to emerged threat. Marine Environmental Research 128, 2-11. Avio, C.G., Gorbi, S., Milan, M., Benedetti, M., Fattorini, D., d'Errico, G., Pauletto, M., Bargelloni, L., Regoli, F., 2015. Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environmental Pollution 198, 211-222. Bal, W., Kasprzak, K.S., 2002. Induction of oxidative DNA damage by carcinogenic metals. Toxicology Letters 127(1-3), 55-62. Barboza, L.G.A., Vieira, L.R., Guilhermino, L., 2018a. Single and combined effects of microplastics and mercury on juveniles of the European seabass (Dicentrarchus labrax): Changes in behavioural responses and reduction of swimming velocity and resistance time. Environmental Pollution 236, 1014-1019. Barboza, L.G.A., Vethaak, A.D., Lavorante, B.R., Lundebye, A.-K., Guilhermino, L., 2018b. Marine microplastic debris: An emerging issue for food security, food safety and human health. Marine Pollution Bulletin 133, 336-348. Barboza, L.G.A., Vieira, L.R., Branco, V., Figueiredo, N., Carvalho, F., Carvalho, C., Guilhermino, L., 2018c. Microplastics cause neurotoxicity, oxidative damage and energy-related changes and interact with the bioaccumulation of mercury in the European seabass, Dicentrarchus labrax (Linnaeus, 1758). Aquatic Toxicology 195, 49-57. Barros, V.R., Camilloni, I., 2016. La Argentina y el cambio climático: De la física a la política. Eudeba. Beiras, R., 2018. Marine Pollution, sources, fate and effects of pollutants in coastal ecosystems. Elsevier. Berg, M., Winkel, L., Amini, M., Rodriguez-Lado, L., Hug, S., Podgorski, J., Bretzler, A., de Meyer, C., Trang, P., Lan, V., 2016. Regional to sub-continental prediction modeling of groundwater arsenic contamination, Arsenic Research and Global Sustainability: Proceedings of the Sixth International Congress on Arsenic in the Environment (As2016), June 19-23, 2016, Stockholm, Sweden. CRC Press, pp. 21. Bermejo, P., Helbling, E.W., Durán-Romero, C., Cabrerizo, M.J., Villafañe, V.E., 2018. Abiotic control of phytoplankton blooms in temperate coastal marine ecosystems: A case study in the South Atlantic Ocean. Science of the Total Environment 612, 894 – 902. Beyer, J., Trannum, H.C., Bakke, T., Hodson, P.V., Collier, T.K., 2016. Environmental effects of the Deepwater Horizon oil spill: A review. Marine Pollution Bulletin 110(1), 28-51. Bilmes, A., Pessacg, N., Alvarez, M.P., Brandizi, L., Cuitiño, J.I., Kaminker, S., Bouza, P.J., Rostagno, C.M., Núñez de la Rosa, D., Canizzaro, A., 2016. Inundaciones en Puerto Madryn: Relevamiento y diagnóstico del evento del 21 de Enero de 2016. Informe Técnico CCT CONICET-CENPAT, 1-20. Botterell, Z.L., Beaumont, N., Dorrington, T., Steinke, M., Thompson, R.C., Lindeque, P.K., 2019. Bioavailability and effects of microplastics on marine zooplankton: A review. Environmental Pollution, 98-110. Brette, F., Machado, B., Cros, C., Incardona, J.P., Scholz, N.L., Block, B.A., 2014. Crude oil impairs cardiac excitation-contraction coupling in fish. Science 343(6172), 772-776. Bruno, J.F., Sweatman, H., Precht, W.F., Selig, E.R., Schutte, V.G.W., 2009. Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90, 1478-1484. Burke, L., Reytar, K., Spalding, M., Perry, A., 2011. Reefs at risk revisited. Bursian, S.J., Dean, K.M., Harr, K.E., Kennedy, L., Link, J.E., Maggini, I., Pritsos, C., Pritsos, K.L., Schmidt, R., Guglielmo, C.G., 2017. Effect of oral exposure to artificially weathered Deepwater Horizon crude oil on blood chemistries, hepatic antioxidant

Journal Pre-proof

Jo ur

na

lP

re

-p

ro

of

enzyme activities, organ weights and histopathology in western sandpipers (Calidris mauri). Ecotoxicology and Environmental Safety 146, 91-97. Butler, J.N., Morris, F., Cadwallader, J., Stoner, A.W., 1983. Studies of Sargassum and the Sargassum community. Bermuda Biological Station. Cabrerizo, M.J., Carrillo, P., Villafañe, V.E., Medina-Sánchez, J.M., Helbling, E.W., 2018. Increased nutrients from aeolian-dust and riverine origin decrease the CO2-sink capacity of coastal South Atlantic waters under UVR exposure. Limnology and Oceanography 63, 1191-1203. Camilli, R., Reddy, C.M., Yoerger, D.R., Van Mooy, B.A., Jakuba, M.V., Kinsey, J.C., McIntyre, C.P., Sylva, S.P., Maloney, J.V., 2010. Tracking hydrocarbon plume transport and biodegradation at Deepwater Horizon. Science 330(6001), 201-204. Caramuto, M.E., Narvarte, M.A., Carbajal, M., Esteves, J.L., Harris, G., 2009. Contaminación ambiental por metales pesados y salud humana en San Antonio Oeste. In: Belmonte, A. (Ed.), Construyendo confianza: Hacia un nuevo vínculo entre estado y sociedad civil. Fundación CIPPEC: Fund. CIPPEC. Subsecretaría para la Reforma Institucional y Fortalecimiento de la Democracia, Jefatura de Gabinete de Ministros, Presidencia de la Nación, Buenos Aires. Caron, A.G., Thomas, C.R., Berry, K.L., Motti, C.A., Ariel, E., Brodie, J.E., 2018. Ingestion of microplastic debris by green sea turtles (Chelonia mydas) in the Great Barrier Reef: Validation of a sequential extraction protocol. Marine Pollution Bulletin 127, 743-751. Chatterjee, S., Sharma, S., 2019. Microplastics in our oceans and marine health. Reinventing Plastics 19, 54-61. Commendatore, M., Gil, M., Harvey, M., Colombo, J., Esteves, J., 1996. Evaluación de la contaminación por hidrocarburos y metales en la zona costera patagónica. Fundación Patagomia Natural, Chubut (Argentina). Conti, M.E., Stripeikis, J., Finoia, M.G., Tudino, M.B., 2011. Baseline trace metals in bivalve molluscs from the Beagle Channel, Patagonia (Argentina). Ecotoxicology 20(6), 13411353. Cravero, M.F., Domínguez, E., Murray, H.H., 1991. Valores δO18 y δD en caolinitas, indicadores de un clima templado moderado durante el Jurásico Superior-Cretácico Inferior de la Patagonia, Argentina. Revista de la Asociación Geológica Argentina 46, 20-25. de Sá, L.C., Luís, L.G., Guilhermino, L., 2015. Effects of microplastics on juveniles of the common goby (Pomatoschistus microps): Confusion with prey, reduction of the predatory performance and efficiency, and possible influence of developmental conditions. Environmental Pollution 196, 359-362. Derraik, J.G.B., 2002. The pollution of the marine environment by plastic debris: A review. Marine Pollution Bulletin 44, 842-852. Díaz, S., Pascual, U., Stenseke, M., Martín-López, B., Watson, R., Molnár, Z., Hill, R., Chan, K., Baste, I., Brauman, K., Polasky, S., Church, A., Lonsdale, M., Larigauderie, A., Leadley, P., van Oudenhoven, A., van der Plaat, F., Schröter, M., Lavorel, S., Aumeeruddy-Thomas, Y., Bukvareva, E., Davies, K., Demissew, S., Erpul, G., Failler, P., Guerra, C., Hewitt, C., Keune, H., Lindley, S., Shirayama, Y., 2018. Assessing nature's contributions to people. Science 359, 270-272. Duarte, C.A., Giarratano, E., Gil, M.N., 2012. Trace metal content in sediments and autochthonous intertidal organisms from two adjacent bays near Ushuaia, Beagle Channel (Argentina). Marine Environmental Research 79, 55-62. Fabricius, K.E., 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Marine Pollution Bulletin 50(2), 125-146. Fernández-Severini, M.D., Hoffmeyer, M.S., Marcovecchio, J.E., 2013. Heavy metals concentrations in zooplankton and suspended particulate matter in a southwestern

Journal Pre-proof

Jo ur

na

lP

re

-p

ro

of

Atlantic temperate estuary (Argentina). Environmental Monitoring and Assessment 185(2), 1495-1513. Fingas, M., 2016. Oil spill science and technology. Gulf Professional Publishing. Fleeger, J., Riggio, M., Mendelssohn, I., Lin, Q., Hou, A., Deis, D., 2018. Recovery of saltmarsh meiofauna six years after the Deepwater Horizon oil spill. Journal of Experimental Marine Biology and Ecology 502, 182-190. Forth, H.P., Mitchelmore, C.L., Morris, J.M., Lipton, J., 2017. Characterization of oil and water accommodated fractions used to conduct aquatic toxicity testing in support of the Deepwater Horizon oil spill natural resource damage assessment. Environmental Toxicology and Chemistry 36(6), 1450-1459. Galazzo, J.L., Cerro, R.L., Depetris, P.J., 1985. Los caolines de Chubut y Santa Cruz. Sus características importantes para el uso papelero. Asociación Geológica Argentina, Revista XL 3-4, 278-283. Gallo, F., Fossi, C., Weber, R., Santillo, D., Sousa, J., Ingram, I., Nadal, A., Romano, D., 2018. Marine litter plastics and microplastics and their toxic chemicals components: The need for urgent preventive measures. Environmental Sciences Europe 30(1), 13. Gil, M., Harvey, M., Esteves, J., 1999. Heavy metals in intertidal surface sediments from the Patagonian Coast, Argentina. Bulletin of Environmental Contamination and Toxicology 63(1), 52-58. Gil, M.N., Torres, A., Harvey, M., Esteves, J.L., 2006. Metales pesados en organismos marinos de la zona costera de la Patagonia argentina continental. Revista de Biología Marina y Oceanografía 41(2), 167-176. Gill, D.A., Ritchie, L.A., Picou, J.S., 2016. Sociocultural and psychosocial impacts of the Exxon Valdez oil spill: Twenty-four years of research in Cordova, Alaska. The Extractive Industries and Society 3(4), 1105-1116. Gray, A.D., Weinstein, J.E., 2017. Size- and shape-dependent effects of microplastic particles on adult daggerblade grass shrimp (Palaemonetes pugio). Environmental Toxicology and Chemistry 36, 3074-3080. Guerranti, C., Martellini, T., Perra, G., Scopetani, C., Cincinelli, A., 2019. Microplastics in cosmetics: Environmental issues and needs for global bans. Environmental Toxicology and Pharmacology 68, 75-79. Hahladakis, J.N., Velis, C.A., Weber, R., Iacovidou, E., Purnell, P., 2018. An overview of chemical additives present in plastics: migration, release, fate and environmental impact during their use, disposal and recycling. Journal of Hazardous Materials 344, 179-199. Hain, M.P., Sigmal, D., Haug, G.H., 2014. The biological pump in the past, Reference Module in Earth Systems and Environmental Sciences, Treatise on Geochemistry (Second Edition), The Oceans and Marine Geochemistry. Elsevier, The Netherlands, pp. 485517. Harr, K.E., Cunningham, F.L., Pritsos, C.A., Pritsos, K.L., Muthumalage, T., Dorr, B.S., Horak, K.E., Hanson-Dorr, K.C., Dean, K.M., Cacela, D., 2017. Weathered MC252 crude oil-induced anemia and abnormal erythroid morphology in double-crested cormorants (Phalacrocorax auritus) with light microscopic and ultrastructural description of Heinz bodies. Ecotoxicology and Environmental Safety 146, 29-39. Hartmann, A.C., Sandin, S.A., Chamberland, V.F., Marhaver, K.L., de Goeij, J.M., Vermeij, M.J., 2015. Crude oil contamination interrupts settlement of coral larvae after direct exposure ends. Marine Ecology Progress Series 536, 163-173. Hermsen, E., Mintenig, S.M., Besseling, E., Koelmans, A.A., 2018. Quality criteria for the analysis of microplastic in biota samples: A critical review. Environmental Science & Technology 52(18), 10230-10240. Hernández-Terrones, L.M., Null, K.A., Ortega-Camacho, D., Paytan, A., 2015. Water quality

Journal Pre-proof

Jo ur

na

lP

re

-p

ro

of

assessment in the Mexican Caribbean: Impacts on the coastal ecosystem. Continental Shelf Research 102, 62-72. Hong, S., Yim, U.H., Ha, S.Y., Shim, W.J., Jeon, S., Lee, S., Kim, C., Choi, K., Jung, J., Giesy, J.P., 2016. Bioaccessibility of AhR-active PAHs in sediments contaminated by the Hebei Spirit oil spill: Application of Tenax extraction in effect-directed analysis. Chemosphere 144, 706-712. Idaszkin, Y.L., Carol, E., del Pilar, A.M., 2017. Mechanism of removal and retention of heavy metals from the acid mine drainage to coastal wetland in the Patagonian marsh. Chemosphere 183, 361-370. Incardona, J.P., 2017. Molecular mechanisms of crude oil developmental toxicity in fish. Archives of Environmental Contamination and Toxicology 73(1), 19-32. Incardona, J.P., Gardner, L.D., Linbo, T.L., Brown, T.L., Esbaugh, A.J., Mager, E.M., Stieglitz, J.D., French, B.L., Labenia, J.S., Laetz, C.A., 2014. Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish. Proceedings of the National Academy of Sciences 111(15), E1510-E1518. INDEC, 2010. Censo nacional de poblaciones, hogares y viviendas. https://www.indec.gob.ar/ftp/cuadros/poblacion/censo2010_tomo1.pdf IWC, I.W.C.-. 2013. Report of the IWC - Workshop on the Assessment of Southern Right Whales. Journal of Cetacean Research and Management 14, 439-462. Jackson, J.B.C., Donovan, M.K., Cramer, K.L., Lam, V.V., 2014. Status and Trends of Caribbean Coral Reefs. 1970-2012. Global Coral Reef Monitoring Network, IUCN, Gland, Switzerland. Jasperse, L., Levin, M., Tsantiris, K., Smolowitz, R., Perkins, C., Ward, J.E., De Guiseae, S., 2018. Comparative toxicity of Corexit® 9500, oil, and a Corexit®/oil mixture on the eastern oyster, Crassostrea virginica (Gmelin). Aquatic Toxicology 230, 10-18. Johnson, M.S., Meskhidze, N., Kiliyanpilakkil, V.P., Gassó, S., 2011. Understanding the transport of Patagonian dust and its influence on marine biological activity in the South Atlantic Ocean. Atmospheric Chemistry and Physics 11, 2487–2502. Jokiel, P., Hunter, C., Taguchi, S., Watarai, L., 1993. Ecological impact of a fresh-water “reef kill” in Kaneohe Bay, Oahu, Hawaii. Coral Reefs 12(3-4), 177-184. Kershaw, P., Rochman, C., 2015. Sources, fate and effects of microplastics in the marine environment: Part 2 of a global assessment. Reports and studies-IMO/FAO/UnescoIOC/WMO/IAEA/UN/UNEP Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection (GESAMP) eng no. 93. Keswani, A., Oliver, D.M., Gutierrez, T., Quilliam, R.S., 2016. Microbial hitchhikers on marine plastic debris: Human exposure risks at bathing waters and beach environments. Marine Environmental Research 118, 10-19. Kleindienst, S., Paul, J.H., Joye, S.B., 2015a. Using dispersants after oil spills: Impacts on the composition and activity of microbial communities. Nature Reviews Microbiology 13(6), 388-396. Kleindienst, S., Seidel, M., Ziervogel, K., Grim, S., Loftis, K., Harrison, S., Malkin, S.Y., Perkins, M.J., Field, J., Sogin, M.L., 2015b. Chemical dispersants can suppress the activity of natural oil-degrading microorganisms. Proceedings of the National Academy of Sciences 112(48), 14900-14905. Koelmans, A.A., Besseling, E., Shim, W.J., 2015. Nanoplastics in the aquatic environment. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine anthropogenic litter. Springer, Berlin, pp. 329-344. Kvenvolden, K., Cooper, C., 2003. Natural seepage of crude oil into the marine environment. Geo-Marine Letters 23(3-4), 140-146. Le Croizier, G., Lacroix, C., Artigaud, S., Le Floch, S., Raffray, J., Penicaud, V., Coquillé, V., Autier, J., Rouget, M.-L., Le Bayon, N., 2018. Significance of metallothioneins in

Journal Pre-proof

Jo ur

na

lP

re

-p

ro

of

differential cadmium accumulation kinetics between two marine fish species. Environmental Pollution 236, 462-476. Lebreton, L.C., Van der Zwet, J., Damsteeg, J.-W., Slat, B., Andrady, A., Reisser, J., 2017. River plastic emissions to the world’s oceans. Nature Communications 8, 15611. Li, X., Chi, W., Tian, H., Zhang, Y., Zhu, Z., 2019. Probabilistic ecological risk assessment of heavy metals in western Laizhou Bay, Shandong Province, China. PloS one 14(3), e0213011. Longhurst, A., 1998. Ecological geography of the sea. Academic Press, San Diego. Longhurst, A., Sathyendranath, S., Platt, T., Caverhill, C., 1995. An estimate of global primary production in the ocean from satellite radiometer data. Journal of Plankton Research 17, 1245-1271. Luis, L.G., Ferreira, P., Fonte, E., Oliveira, M., Guilhermino, L., 2015. Does the presence of microplastics influence the acute toxicity of chromium(VI) to early juveniles of the common goby (Pomatoschistus microps)? A study with juveniles from two wild estuarine populations. Aquatic Toxicology 164, 163-174. Lusher, A., 2015. Microplastics in the marine environment: Distribution, interactions and effects, Marine anthropogenic litter. Springer, Cham, pp. 245-307. Marcovecchio, J.E., De Marco, S.G., Gavio, M.A., Narvarte, M., Fiori, S., Gerpe, M.S., Rodríguez, D.H., Abbate, M.C.L., La Colla, N., Oliva, A.L., 2019. The Northern Argentine Sea, World Seas: an Environmental Evaluation. Elsevier, pp. 759-781. Marinho, C.H., 2017. Procesos de absorción-desorción asociados a metales pesados en un sistema macromareal Patagónico. Universidad Nacional del Comahue. Markic, A., Niemand, C., Bridson, J.H., Mazouni-Gaertner, N., Gaertner, J.-C., Eriksen, M., Bowen, M., 2018. Double trouble in the South Pacific subtropical gyre: Increased plastic ingestion by fish in the oceanic accumulation zone. Marine Pollution Bulletin 136, 547-564. Martínez-Gómez, C., León, V.M., Marina, S.C., Gomáriz-Olcina, M., Vethaak, A.D., 2017. The adverse effects of virgin microplastics on the fertilization and larval development of sea urchins. Marine Environmental Research 130, 69-76. Metcalfe, C.D., Beddows, P.A., Bouchot, G.G., Metcalfe, T.L., Li, H., Van Lavieren, H., 2011. Contaminants in the coastal karst aquifer system along the Caribbean coast of the Yucatan Peninsula, Mexico. Environmental Pollution 159(4), 991-997. Müller, A., Becker, R., Dorgerloh, U., Simon, F.-G., Braun, U., 2018. The effect of polymer aging on the uptake of fuel aromatics and ethers by microplastics. Environmental pollution 240, 639-646. Munro, M.H., Blunt, J.W., Dumdei, E.J., Hickford, S.J., Lill, R.E., Li, S., Battershill, C.N., Duckworth, A.R., 1999. The discovery and development of marine compounds with pharmaceutical potential. Journal of Biotechnology 70(1-3), 15-25. Negri, A.P., Brinkman, D.L., Flores, F., Botté, E.S., Jones, R.J., Webster, N.S., 2016. Acute ecotoxicology of natural oil and gas condensate to coral reef larvae. Scientific Reports 6, 21153. Neumann, B., Vafeidis, A.T., Zimmermann, J., Nicholls, R.J., 2015. Future coastal population growth and exposure to sea-level rise and coastal flooding-a global assessment. PloS one 10(3), e0118571. Oliveira, M., Ribeiro, A., Hylland, K., Guilhermino, L., 2013. Single and combined effects of microplastics and pyrene on juveniles (0+ group) of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Ecological Indicators 34, 641-647. Paches, M., Aguado, D., Martínez-Guijarro, R., Romero, I., 2019. Long-term study of seasonal changes in phytoplankton community structure in the western Mediterranean (Valencian Community). Environmental Science and Pollution Research, 1-11. Paparazzo, F.E., Crespi-Abril, A.C., Gonçalves, R.J., Barbieri, E.S., Villalobos, L.L.G., Solís,

Journal Pre-proof

Jo ur

na

lP

re

-p

ro

of

M.E., Soria, G., 2018. Patagonian dust as a source of macronutrients in the Southwest Atlantic Ocean. Oceanography 31(4), 33-39. Pastorok, R.A., Bilyard, G.R., 1985. Effects of sewage pollution on coral-reef communities. Marine Ecology Progress Series 21(1), 175-189. Paul, J.H., Hollander, D., Coble, P., Daly, K.L., Murasko, S., English, D., Basso, J., Delaney, J., McDaniel, L., Kovach, C.W., 2013. Toxicity and mutagenicity of Gulf of Mexico waters during and after the Deepwater Horizon oil spill. Environmental Science & Technology 47(17), 9651-9659. Perier, M.R., 1994. La fauna íctica en el litoral de la Bahía de San Antonio (Golfo San Matías, Pcia. de Río Negro). Universidad Nacional de La Plata. Pessacg, N., Flaherty, S., Brandizi, L., Solman, S., Pascual, M., 2015. Getting water right: A case study in water yield modelling based on precipitation data. Science of the Total Environment 537, 225-234. Peterson, C.H., Rice, S.D., Short, J.W., Esler, D., Bodkin, J.L., Ballachey, B.E., Irons, D.B., 2003. Long-term ecosystem response to the Exxon Valdez oil spill. Science 302(5653), 2082-2086. Rabalais, N.n., Turner, R.E., Díaz, R.J., Justic, D., 2009. Global change and eutrophication of coastal waters. ICES Journal of Marine Science 66, 1528-1537. Reid, P.C., 2016. Ocean warming: Setting the scene. In: Laffoley, D., Baxter, J.M. (Eds.), Explaining Ocean Warming: Causes, scale, effects and consequences. International Union for Conservation of Nature (IUCN), Gland, Switzerland, pp. 17-45. Réu, P., Svedberg, G., Hässler, L., Möller, B., Svahn, H.A., Gantelius, J., 2019. A 61% lighter cell culture dish to reduce plastic waste. PloS one 14(4), e0216251. Ribeiro, F., Garcia, A.R., Pereira, B.P., Fonseca, M., Mestre, N.C., Fonseca, T.G., Ilharco, L.M., Bebianno, M.J., 2017. Microplastics effects in Scrobicularia plana. Marine Pollution Bulletin 122, 379-391. Rioja-Nieto, R., Garza-Pérez, R., Álvarez-Filip, L., Ismael, M.-T., Cecilia, E., 2019. The Mexican caribbean: From Xcalak to holbox, World Seas: An environmental evaluation. Elsevier, pp. 637-653. Rodriguez-Martinez, R., Medina-Valmaseda, A.E., Blanchon, P., Monroy-Velázquez, L.V., Almazán-Becerril, A., Delgado-Pech, B., Vásquez-Yeomans, L., Francisco, V., GarcíaRivas, M.C., 2019. Faunal mortality associated with massive bleaching and decomposition of pelagic Sargassum. Marine Pollution Bulletin 146, 201-205. Ron, E.Z., Rosenberg, E., 2014. Enhanced bioremediation of oil spills in the sea. Current Opinion in Biotechnology 27, 191-194. Rousseaux, C.S., Gregg, W.W., 2014. Interannual variation in phytoplankton primary production at a global scale. Remote Sensing 6, 1-19. Schwartz, D., Milfont, T.L., Hilton, D., 2019. The interplay between intrinsic motivation, financial incentives and nudges in sustainable consumption. A Research Agenda for Economic Psychology, 87. SECTUR, 2019 Results of tourism activity 2018. Undersecretariat of Planning and Tourism Policy. SENASA, 2019. https://www.argentina.gob.ar/senasa Setälä, O., Lehtiniemi, M., Coppock, R., Cole, M., 2018. Microplastics in marine food webs, Microplastic contamination in aquatic environments. Elsevier, pp. 339-363. Spalding, M., Grenfell, A., 1997. New estimates of global and regional coral reef areas. Coral Reefs 16(4), 225-230. Spalding, M., Burke, L., Wood, S.A., Ashpole, J., Hutchison, J., Zu Ermgassen, P., 2017. Mapping the global value and distribution of coral reef tourism. Marine Policy 82, 104-113. Suchley, A., McField, M.D., Alvarez-Filip, L., 2016. Rapidly increasing macroalgal cover not

Journal Pre-proof

Jo ur

na

lP

re

-p

ro

of

related to herbivorous fishes on Mesoamerican reefs. PeerJ 4, e2084. Sutherland, K.P., Porter, J.W., Turner, J.W., Thomas, B.J., Looney, E.E., Luna, T.P., Meyers, M.K., Futch, J.C., Lipp, E.K., 2010. Human sewage identified as likely source of white pox disease of the threatened Caribbean elkhorn coral, Acropora palmata. Environmental Microbiology 12(5), 1122-1131. Svendsen, G., 2013. Distribución y uso de hábitat de mamíferos marinos en el Golfo San Matías. Universidad Nacional del Comahue. UNEP, 1994. Regional overview of land-based sources of pollution in the wider Caribbean Region. CEP Technical Report. UNEP. UNEP, 2012. Environmental effects of ozone depletion and its interactions with climate change: Progress report, 2011., Photochemical & Photobiological Sciences, pp. 15. van Dam, J.W., Negri, A.P., Uthicke, S., Mueller, J.F., 2011. Chemical pollution on coral reefs: exposure and ecological effects, Ecological Impacts of Toxic Chemicals, pp. 187-211. van Tussenbroek, B.I., Arana, H.A.H., Rodríguez-Martínez, R.E., Espinoza-Avalos, J., Canizales-Flores, H.M., González-Godoy, C.E., Barba-Santos, M.G., Vega-Zepeda, A., Collado-Vides, L., 2017. Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities. Marine Pollution Bulletin 122(1-2), 272281. Vega Thurber, R.L., Burkepile, D.E., Fuchs, C., Shantz, A.A., McMinds, R., Zaneveld, J.R., 2014. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Global Change Biology 20(2), 544-554. Verhougstraete, M.P., Martin, S.L., Kendall, A.D., Hyndman, D.W., Rose, J.B., 2015. Linking fecal bacteria in rivers to landscape, geochemical, and hydrologic factors and sources at the basin scale. Proceeding of the National Academy of Sciences 112, 10419-10424. Villafañe, V.E., Paczkowska, J., Andersson, A., Durán Romero, C., Valiñas, M.S., Helbling, E.W., 2018. Dual role of DOM in a scenario of global change on photosynthesis and structure of coastal phytoplankton from the South Atlantic Ocean. Science of the Total Environment 634, 1352-1361. Vizzo, J.I., Helbling, E.W., Masuda, T., Villafañe, V.E., 2019. Efectos del cambio global en la fisiología y estructura del fitoplancton del estuario del Río Chubut en dos estadíos de la sucesión anual. Novena Jornada de Becarios y Primer Encuentro Patagónico de Becarios, Puerto Madryn. Wagner, D.E., Kramer, P., Van Woesik, R., 2010. Species composition, habitat, and water quality influence coral bleaching in southern Florida. Marine Ecology Progress Series 408, 65-78. Wang, M., Hu, C., Barnes, B.B., Mitchum, G., Lapointe, B., Montoya, J.P., 2019. The great Atlantic Sargassum belt. Science 365, 83-87. Wear, S.L., Thurber, R.V., 2015. Sewage pollution: Mitigation is key for coral reef stewardship. Annals of the New York Academy of Sciences 1355(1), 15-30. Welden, N.A.C., Cowie, P.R., 2016. Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environmental Pollution 218, 895900. Wise, C.F., Wise, J.T., Wise, S.S., Thompson, W.D., Wise, J.P., 2014. Chemical dispersants used in the Gulf of Mexico oil crisis are cytotoxic and genotoxic to sperm whale skin cells. Aquatic Toxicology 152, 335-340.

Journal Pre-proof Table 1: Brief comparison of the emerging problems assessed in this manuscript to highlight similarities and contrast the dynamics of these pollutants. Pollutant

Source

Periodicity

Dispersal mechanism

Geographic extension

Sewage

Household, Domestic animals, Hotels, Industrial wastewater

Daily and seasonal pulses over an increasing baseline

Stormwater runoff, drains and channels

Local regional

/

Nutrients and terrigenous material

Natural processes, Cities, Agriculture

Pulsed over an increasing baseline

Wind, Riverine discharge

Local regional

/

Heavy metals

Industry

Sporadic

Runoff, Winds, Leaching

Local regional

o J

Industry

Sporadic

Spills, currents

Plastic

Consumers, Industry

Constant

Winds, water discharges (rivers, sewages), human wastes

Local regional

Global

Treatment type

Environmental concern

Days months

to

Wastewater treatment

Days months

to

Fecal contamination of drinking water, Eutrophication of aquatic ecosystems Eutrophication and reduced penetration of solar radiation in aquatic ecosystems Carcinogens, DNA and enzyme damage, Neurological damage in humans Immediate mortality, Sublethal damage in marine wildlife Severe to lethal in fish, birds and marine mammals, Unknown in humans

l a

n r u

Crude oil

Persistence*

e

r P

/

Decades centuries

/

Weeks

Decades centuries

o r p

to

None

Ad hoc remediation techniques

Ad hoc remediation techniques

to

f o

Clean up techniques under research

Existence of regulations and controls Partial / depending on local laws and control capacities

Feasibility of control / mitigation Medium

Partial / depending on local laws and control capacities

Medium

Severe / depending on regional and local laws and control capacities

High

Severe / depending on international agreements

High

None or scarce

Low

*Persistence: Refers to the time elapsed to return to the initial condition naturally or through corrective measures.

Journal Pre-proof

Figure Legends Figure 1. Aerial view of a Sargassum bloom reaching the coastline along the Mexican Caribbean: (A) beaching of Sargassum in August 24, 2018, (B) degradation of Sargassum causing a brown tide August 23, 2018 and (C) persistence of brown tide, September 27, 2018. Photos by Edgar Escalante Mancera and Miguel Angel Gomez Reali.

of

Figure 2. Aerial view of the Chubut River estuary: (A) normal conditions; (B) after an

ro

extreme rain event (Photo source: Diario Jornada); (C) Dissolved organic carbon

re

-p

concentration (DOC in g C m-3) during the normal (A) and extreme (B) conditions.

Figure 3. (A) Mean (and SD) of annual aerosol index (AI, relative units), (B) Total number of

lP

AI above 0.6 from 1995 to 2018 over the Chubut River estuary (modified from Cabrerizo et

na

al. 2018).

Jo ur

Figure 4. Map of Patagonia, Argentina and photos of the San Antonio Bay area. (A) Points surveyed for heavy metals (yellow circles) along the Patagonian coast. Red circles indicate values of most concern. The larger red circle indicates the San Antonio Bay hotspot (adapted from Gil, et al., 1999); (B) Aerial view of channels and intertidal areas of San Antonio Bay showing the proximity of the mine tailing (black open circle) to the city of San Antonio and to the sea; (C) Close up view of the mine tailing next to the route leading to San Antonio. Photos by Martin Brunella.

Journal Pre-proof Declaration of interests x The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Jo ur

na

lP

re

-p

ro

of

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

Journal Pre-proof

Highlights Corals reefs are impacted by sewage reaching the ocean through underground aquifers Riverine and eolic inputs of terrigenous material affect marine phytoplankton Crude oil spills result in mortality or sublethal damage in many marine organisms Patagonian coastal zones show high concentrations of heavy metals

Jo ur

na

lP

re

-p

ro

of

About 8 million tonnes of plastic enter the oceans every year affecting marine life

Figure 1

Figure 2

Figure 3

Figure 4