Impacts of COVID-19 on the Aquatic Environment: Comparison
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Please note this is a comparison between Version 2 by Conner Chen and Version 1 by F.M. Yusoff.

The COVID-19 pandemic, caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), resulted in ecological changes of aquatic ecosystems, affected the aquatic food supply chain, and disrupted the socio-economy of global populations. Due to reduced human activities during the pandemic, the aquatic environment was reported to improve its water quality, wild fishery stocks, and biodiversity. However, the sudden surge of plastics and biomedical wastes during the COVID-19 pandemic masked the positive impacts and increased the risks of aquatic pollution, especially microplastics, pharmaceuticals, and disinfectants. 

  • COVID-19
  • aquatic environment
  • aquatic foods
  • Fisheries
  • Aquaculture
  • Food security
  • Risk assessment

1. Introduction

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) caused the coronavirus disease 2019 (COVID-19) that brought severe changes to various facets of human lives worldwide. During the pandemic, which has claimed 4,753,573 lives from 232,029,574 cases in 220 countries and territories by 25 September 2021, essentially all countries have implemented various forms of human movement restrictions to curb the spread. COVID-19 pandemic caused chain ecological changes in both aquatic and terrestrial ecosystems, affected aquatic resources and supplies, altered the livelihood of the littoral communities, and changed the socioeconomics of the global population. Dente and Hashimoto [1] noted that the COVID-19 pandemic has resulted in both positive and negative impacts on the environment and human society. The improvement of water quality and the increase in fish stocks were reported in many countries as many industries and other anthropogenic activities decreased across the globe during the restricted movement period [2,3,4][2][3][4]. Aquatic ecosystems including lakes, rivers, and coastal waters rapidly responded to the reduced anthropogenic impacts. Braga [5] noted the water transparency in the lagoon of Venice improved during the lockdown to control the spread of the SARS-CoV-2 infection, mainly due to the reduction of urban water traffic and other related human activities. The improvement of water quality and the increase in some aquatic wild stocks in the aquatic environment were reported in water bodies around the world as the results of reduced agricultural, industrial, and commercial activities [6].
However, negative impacts in the sudden surge of plastics, disinfectants, and pharmaceutical wastes due to the fast spread of COVID-19 quickly masked the positive changes seen at the beginning of the pandemic. COVID-19’s restriction on human movement resulted in disruptions of various aspects of human lives and altered human behavior. The loss of jobs and income increased poverty and disrupted trade and supply chains that could finally cause societal and economic collapses were some of the devastating consequences of the global pandemic. Praveena and Aris [2] reported that the lack of efficient treatment facilities of plastic and medical wastes in Southeast Asian countries resulted in a huge increase of these wastes in water bodies during the lockdown periods. In addition, the COVID-19 pandemic interfered with the supply of basic life necessities, especially water, food, and sanitation. These negative impacts are more apparent in low-income countries with an inadequate supply of basic necessities, where people would be more vulnerable to the impacts of the pandemic [7]. Thus, the aquatic environment-resource-human nexus during the COVID-19 crisis should be carefully studied to understand the complex relationships and formulate effective strategies to minimize the negative impacts.

2. Impacts of COVID-19 on the Aquatic Environment

The aquatic environment consists of a continuum of aquatic ecosystems from the upstream to the estuary and coastal area, punctuated by creeks and tributaries along the way. Numerous lakes and wetlands in the flood plains and/or river basins also contributed immensely to the lotic-lentic water body complex. With the rapid economic development, especially in developing countries, many of these water bodies are subjected to environmental stressors associated with anthropogenic activities and climate change, resulting in water quality deterioration, harmful algal blooms, loss of productivity, and loss of biodiversity. The appearance of COVID-19 showed both its positive and negative impacts on the aquatic environment (Table 1).
Table 1. Impacts of COVID-19 on the aquatic environment.
Components/

Elements		 Impacts/Results Reasons References
Water quality Decrease in total solids, less turbidity Less human activities and decreased discharges

Turbidity levels decreased by 25% due to a reduction in human activities		 [2,4][2][4]
Improvement in suspended particulate matter Decreased of SPM by 15.9% [3]
Increased water transparency Reduction in water-based activities due to lockdown [5]
Decrease in nutrients Less agro-based industries, less nutrient-rich waters from commercial centers and urban areas [8,9][8][9]
Decrease of some heavy metal concentrations in surface and groundwaters Decrease in industrial discharges [9]
Improvement of water quality index (based on DO, BOD, COD, pH, and NH3-N) in rivers and lakes Significant reduction in industrial and agriculture activities and human encroachment.

Closure of industrial and tourism activities		 [10]
Chlorophyll a and Phytoplankton The decline of chlorophyll a Reduction of nitrogen inflow from the land area [11]
Bacterial loads Reduced total coliforms, fecal coliforms, fecal Streptococci, Escherichia coli, Closure of agroindustries: aquaculture, poultry, livestock [9]
Resources and biodiversity Improved; increased deepwater shrimp production Less fishing pressure: reduced anthropogenic activities allowed stock recovery, especially for fast-growing species. [12]
Plastic wastes Increased personal protection equipment (PPE) and face masks Higher use in relation to the COVID-19 pandemic [13,14,15][13][14][15]
Medical wastes—COVID-19 related pharmaceuticals Increased chemical contaminants (endocrine disrupting compounds) are harmful to aquatic ecosystems and human health. Higher wastes from hospitals—10 to 20 times higher, less recycling.

Environmental concerns on antibiotics and antivirals; ivermectin and azithromycin had high effects in aquatic organisms.		 [8,16][8][16]
Impairment of reproductive system in fish Abnormalities in fish ovaries [17]
Disinfectants Strong biocidal properties against bacteria and viruses Formation of dioxin and other carcinogens in surface waters. High ecological risks [18,19][18][19]
Water as a medium to spread viruses SARS-CoV-2 detected in feces Increase of COVID-19 cases and evidence of its presence in wastewaters [20,21,22,23][20][21][22][23]
Transmission of the virus from wastewater to surface water Increased virus to surface waters in less treated or untreated sewage In countries with less efficient waste treatment facilities. [8,24,25][8][24][25]
Use of WBE (wastewater-based epidemiology) An efficient, economical, and powerful tool for assessing, monitoring, and managing the COVID-19 pandemic To prevent contamination of surface and groundwater supply for drinking water [26,27,28][26][27][28]
Use of technologies Contain/removal of viral particles Laser technology [29]
  Coagulation-flocculation and filtration [30]
  Natural microbes—Bioremediation technology (virus elimination via predation, antagonism, and nutrient competition) [31]
  Microalgal technology [32]
The tertiary waste treatment facility Able to completely remove COVID-19 virus Complete deactivation of technologies used [28]
DO is dissolved oxygen, BOD is biological oxygen demand, COD is chemical oxygen demand, NH3-N is ammoniacal nitrogen.

2.1. Positive Impacts of COVID-19

With the reduction of industrial, commercial, and other anthropogenic activities associated with COVID-19-restricted movements, lakes, rivers, estuaries, and seas showed improvements in their water quality and biotic life, indicating that humans are actually responsible for their pollution and deterioration. The improvement of water quality and the reduction in fishing pressure provided the opportunity for aquatic animals to multiple at a faster rate compared to the earlier period before the COVID-19 pandemic [33]. Edward et al. [34] reported that water quality parameters such as turbidity, nutrient concentrations, microbial levels, microplastics, dissolved oxygen, phytoplankton concentrations, and fish densities in the southeast Indian coastal ecosystem have improved after the lockdown period associated with the COVID-19 pandemic. A decrease in anthropogenic activities including tourism, business, and commercial pursuits, agriculture, and industries has decreased discharges into waterways. Selvam et al. [9] reported that the decrease in heavy metals and bacterial loads were due to decreased industrial and agricultural activities, respectively. After the lockdown, Edward et al. [34] reported that microplastic concentrations from eight locations along the coastal area of the Gulf of Mannar, India have decreased from the range of 138–616 items/100 m2 to 63–347 items/100 m2. In rivers, Goi [35], and Wang and Xue [36] reported that water turbidity and other water quality parameters improved as the COVID-19 pandemic lockdown provided opportunities for natural self-purification. Similarly, Pinder et al. [37] reported that heavily polluted rivers in India have improved substantially with clean clear waters for the first time in decades. Using remote sensing techniques in their study of an Indian lake, Wagh et al. [38] noted a significant reduction in chlorophyll a, colored dissolved organic matter, and total suspended solids due to low pollution discharges during the COVID-19 lockdown period when anthropogenic activities were restricted, and many large and small-scaled industries were closed. In addition, Sun et al. [4] also noted that turbidity levels in Wuhan lakes significantly decreased due to the sharp reduction in human activities after the lockdown.
In addition to the improvement seen in streams and rivers, estuaries and seas also showed some recovery signs. Cherif et al. [39] used satellite imagery to illustrate that the reduction in industrial activities due to the COVID-19 pandemic resulted in the improvement of the estuarine and coastal waters of Morocco. In the coastal waters, Mishra et al. [11] reported a decline of chlorophyll a and phytoplankton abundance due to the decrease of nitrogen supply from the land area. Shafeeque et al. [40] reported that the strict lockdown resulted in decreases in turbidity and chlorophyll-a along the coastal areas of India, as decreased human activities reduced the reduction of atmospheric NO2. Thus, with fewer pollutants and destruction associated with human activities, the waters in many places became clearer, cleaner, and facilitated self-rehabilitation.
Positive impacts of COVID-19, although transient, allow for insights into the causes and consequences of anthropogenic activities that can be managed through effective regulation and management of eco-resources for the revival of biodiversity and ecosystem health [34,41][34][41]. With suitable strategies and commitments adopted by authorities and stakeholders, COVID-19 illustrated that an impaired environment can be efficiently restored.

2.2. Negative Impacts of COVID-19

2.2.1. COVID-19 in Wastewaters

Wastewaters have been reported to contain SARS-CoV-2 RNA that could be transmitted and contaminate the aquatic environment [42]. Kumar et al. [43] suggested that the presence of viral loads in wastewater could indicate that the transmission of SARS-CoV-2 through wastewater is possible, especially in countries where sewer systems are not effective enough in removing the virus. Wastewaters from hospitals and quarantine centers for COVID-19 may contain high concentrations of the viral particles, and, thus, effective treatments of hospital wastewater should be strictly enforced to inactivate the virus and prevent transmission [44,45][44][45]. Zhang et al. [19] reported high concentrations of SARS-CoA-2 RNA (0.5 to 18.7 × 103 copies/L) in hospital septic tanks, even after disinfection with sodium hypochlorite (800 g/m3). Langone et al. [28] reported that SARS-CoV-2 RNA particles were still present in wastewater from secondary treatment plants, but they could be completely removed in wastewater treatment plants (WWTPs) equipped with tertiary waste treatments. Balboa et al. [46] reported that no SARS-CoV-2 RNA was found in well-treated effluent or sludge.
Wastewater contains high concentrations of micro-organisms, organic and inorganic substances that could contribute to the natural degradation of viral RNA [47]. However, Yang et al. [31] reported that sewage sludge in WWTPs could harbor a high abundance of SARS-CoV-2 that could survive for months, as the complex organic matter of the sludge could protect the virus from inactivation. Balboa et al. [46] noted that untreated sewage sludge has high concentrations of viral particles and suggested that thickened sewage sludge was a suitable sampling area for COVID-19 monitoring. Thickened sludge with a high abundance of viral RNA formed a suitable spot for COVID-19 incidence monitoring.
SARS-CoV-2 in human guts, stools, and wastewater forms an important fecal-oral route transmission, especially in countries where wastewater treatment facilities are not adequate to remove the viral particles [25,30,48][25][30][48]. Municipal wastewaters in many countries have been used for cleaning, flushing toilets, watering agricultural land, or even for drinking in certain big cities with limited freshwater supply. Thus, the transmission of SARS-CoV-2 RNA via wastewater discharges is a possible route for infection in humans [25]. Zhang et al. [19] reported that viruses in fecal materials in septic tanks can contribute to the spread of SARS-CoV-2 through drainage pipelines. Cervantes-Avil’es et al. [21] reported that SARS-CoV-2 has been detected in wastewater treatment plants, manholes, sewer networks, and various sludge treatment facilities in Europe, North America, South America, and Asia. In fact, the increase of SARS-CoV-2 genetic materials in the wastewater is positively correlated with the number of active COVID-19 patients and can be used as an indicator for the environmental surveillance of the COVID-19 pandemic [43]. Albastaki et al. [20] showed a direct and significant correlation between SARS-CoV-2 viral load in wastewaters and the number of cases in the United Arab Emirates. Gwenzi [25] suggested three main pathways as to how SARS-CoV-2 can be transmitted via the fecal-oral route, all of which are related to the environment (contaminated drinking water), fishery resources (raw or semi-cooked foods from SARS-CoV-2 contaminated waters), or aquaculture products (wastewater-based aquaculture).
The transmission of SARS-CoV-2 via wastewater could eventually contaminate surface waters, as the virus could not be eliminated by conventional secondary treatment of sewage [24]. These viral particles could eventually get to the human through the aquatic food chain and aquatic-based resources such as fish and shellfish [21]. The survival time of SARS-CoV-2 in waters strongly depends on temperature, oxidative chemicals, the concentration of suspended solids and organic matters, and predation along the food chain where SARS-CoV-2 could survive for months in waters with high suspended particles [28,31][28][31]. Balboa et al. [46] reported that SARS-CoV-2 has a strong affinity for biosolids. Thus, turbid rivers and lakes with high suspended solids contents are more susceptible to carrying viral particles and form an important route for the viral spread in a community. Wang et al. [49] reported that river hydrology plays an important role in the long transmission route of SARS-CoV-2.
Grossly inefficient wastewater treatment in developing countries could make the waterborne transmission of SARS-CoV-2 a serious threat to the environment and people [45]. Make-shift quarantine centers that do not have adequate facilities for treating SARS-CoV-2 contaminated wastes were commonly used to house thousands of COVID-19 patients, as hospitals were full to the brim. These poor developing countries are at risk, as the absence of proper management of COVID-19 related wastes including wastewater and medical wastes might further spread the virus [1,50][1][50]. Adelodun et al. [44] offerred useful suggestions for low-income countries such as use of chlorination, ozonation, and UV radiations to deactivate SARS-CoV-2 in their wastewater and prevent/minimize the COVID-19 outbreaks. In low-income countries, where waste treatment facilities are inadequate to remove the virus, it is very important to ensure that wastes should be disinfected by cheap but effective disinfectants and to prevent the discharge of the wastewater to natural water bodies.

2.2.2. Medical Wastes

With the advent of COVID-19 around the globe, there is a massive surge of medical wastes including plastics, antiviral medicines and drugs, and disinfectants that potentially affect the aquatic environment. With the emergence of COVID-19, there has been an increased use of disinfectants to inactivate the virus on surfaces. DeLeo et al. [18] reported that disinfectant Quat (quaternary ammonium compounds) was commonly used during the COVID-19 pandemic in many countries since it has strong biocidal properties and is effective against bacteria and viruses. Fortunately, the ecotoxicity of this disinfectant is minimized due to its high biodegradation rate and readily absorbed to particles in water and sediment. In addition, chlorine (ClO2), sodium hypochlorite (NaOCl), or ultraviolet (UV) water treatment can be used, as they are relatively cheap and easily available [24]. However, high doses of chlorine and sodium hypochlorite (~6700 g/m3) required to completely remove SARS-CoV-2 RNA had high disinfection by-product residual with significant ecological risks [19]. Thus, the ecological risk of disinfection by-product residuals needs to be evaluated.
Currently, COVID-19 vaccination is compulsory to acquire immunity against SARS-CoV-2 by minimizing spread, severity, and death. COVID-19 vaccine vials and ancillary supplies are considered infectious materials. Therefore, the disposal of these materials also requires standard operation waste treatment procedures. Treatment by disinfecting solutions such as chlorine prior to final disposal is necessary to avoid contamination to both humans and the environment. Biomedical waste generated daily is a serious concern, as many would end up in the water and act as sources of chemical pollutants or as substrates for viral particles [51]. The increased use of antiviral and antibiotics also results in increased waste of these medicines in water bodies. Nibamureke and Wagenaar [17] reported that medicinal waste could result in impaired fish reproduction. Tarazona et al. [16] developed models to predict the impacts of antibiotics and antiviral drugs on the ecology of aquatic ecosystems and showed sub-lethal effects on fish.

2.2.3. Plastic Pollution

Persistent wastes such as plastic materials become a global pollution problem because they do not biodegrade easily and could be transported to aquatic ecosystems by winds, storm drains, and rivers. These plastic materials undergo fragmentation and break down into smaller plastic particles of difference sizes categorized as mesoplastics (5 mm to 25 mm), microplastics (<5 mm), and nanoplastics (1 nm to 1 µm) through various mechanical, chemical, and weathering processes [13]. Plastic materials submerged in water leached out heavy metals including lead, cadmium, antimony, and copper, in addition to toxic leachable organic substances related to plastic additives and contaminants [52]. Fadare and Okoffo [53] reported an unprecedented rise in the global production of polymer-based face masks (single use), resulting in an increase in microplastics pollution. Many of these toxic pollutants can enter the aquatic food chain, which could accumulate in aquatic foods and transfer to humans. Pan et al. [54] also reported an average of 246 items m−3 of microplastics in a Chinese river consisting of PP (polypropene) and PE (polythene) as the major polymers.
With 206.2 million COVID-19 cases and 4.4 million deaths in 220 countries as of the 13 August 2021, billions of pieces of personal protective equipment (facemasks, gloves, aprons, etc.) ended up as waste that could pose as health hazard to the environment and human lives if they are not properly treated and managed. Benson et al. [14] estimated more than 12 billion (equivalent to 105,000 tonnes) medical and fabric masks were discarded monthly in African countries, mainly due to the increased consumption of single-use plastics for surgical masks, medical gowns, face shields, safety glasses, protective aprons, sanitizer containers, plastic shoes, and plastic gloves for the protection from SARS-CoV-2. Ardusso et al. [13] also reported that textile fibers for PPE are impregnated with silver (Ag) and copper (Cu) nanoparticles to reduce the infection and spread of SARS-CoV-2. These antiviral textile wastes are a form of an emerging contaminant with long-term negative repercussions on aquatic environments and biota. Most plastics used in medical applications are made from polypropylene, and the plastic residues are classified as biohazardous materials. Studies by Nzediegwu and Chang [50] and Gwenzi [25] have shown that coronavirus can survive on material surfaces between six to nine days. Aragaw [55] noted that face masks are easily ingested by big animals high in the aquatic food chain such as fishes, turtles, and water birds, with enormous effects on their populations and survival. Humans at the end of the aquatic food chain would have a high risk of eating contaminated aquatic foods. Based on past studies, Latchere et al. [56] illustrated the toxicity of microplastics (MPs) and nano plastics (NPs) at the species, community, and ecosystem levels, demonstrating the contamination of plastics through the aquatic food chain. Despite the plethora of problems associated with different experiments and analyses, many studies clearly demonstrated the toxicity of plastics in the freshwater-marine continuum, as well as along the trophic transfer. The improper disposal and disinfection of bottles and containers used in healthcare and treatment facilities could be another potential source of viral transmission. Thus, developing countries with poor waste management facilities are at risk.

Microplastic Pollution

The sudden COVID-19 pandemic could exacerbate the microplastic (MP, plastic polymers with <5 mm) pollution, causing more stress to the aquatic environment. The amount of hazardous microplastics in the environment is aggravated by the unprecedented use of face masks and personal protective equipment (PPE) associated with the COVID-19 pandemic [15]. Severini et al. [57] reported that MPs form approximately 95% of the marine litter.
Microplastics enter aquatic ecosystems through industrial discharges, wastewaters, fisheries activities, marine traffic, and other non-point sources from the land and form a major portion of the marine litter. About 97% of plastic residues associated with COVID-19 medical services are incinerated and, in the process, toxic chemicals are released into the environment [15]. Microplastics are a serious threat to aquatic environments, biota, and human health since they are carriers of hazardous contaminants such as heavy metals, polycyclic hydrocarbons (PAHs), and persistent organic pollutants.
The increase of microplastics in aquatic ecosystems due to COVID-19 also has implications for the wild fish stocks and potential health risks from harvested products. The ingestion of microplastics with hazardous contaminants by commercial shrimps posed a serious threat to food security and food safety for humans. In addition, the aquaculture sector is also at risk, especially those in estuaries and coastal areas where a very large input of plastic wastes could accumulate in cultured organisms through the marine food chain. The increase of microplastics in the environment due to COVID-19 could pollute coastal waters, increase ingestion by top predators including commercial species, increase the body microplastic concentration, and increase mortality in shrimps, and, thus, has the potential to affect aquaculture farming [58,59][58][59]. Severini et al. [57] illustrated that fibers (identified as polyethylene (PE), polyproplylene (PP), and cellulose) containing several elements (C, O, Si, Al, K, S, Br, Ba, Zn, Ti, and Fe) were ingested by a commercial shrimp, Pleotocus muelleri, in a coastal area in the Southwestern Atlantic.
Overall, pathways of plastics to aquatic ecosystems in developed countries are relatively minimal due to well-managed and efficient waste management systems. However, poor waste management systems in underdeveloped and developing countries increase the risk of plastics entering water bodies including lakes, rivers, and coastal waters, as they are ill-equipped to curb the plastic losses to the environment [60,61][60][61]. In addition, leachate from landfills, winds, storms, runoffs, and floods further increase the transfer of plastics from the land source to the aquatic food chains [60].

3. Transmission of COVID-19 to Natural Waters

In countries where raw sewage is directly discharged into natural water bodies, the likelihood of the transmission of SARS-CoV-2 from wastewaters is very likely. This possible transmission route raises serious concerns, especially in low-income countries where raw wastewater is discharged directly into natural water bodies or through inefficient wastewater treatment plants (Figure 1). The presence of SARS-CoV-2 in natural water has been reported by many studies [9,49][9][49]. Guerrero-Loterra et al. [23] reported the presence of SARS-CoV-2 in urban rivers with low sanitation facilities, indicating the transmission of the viral particles from untreated wastewaters and increasing the threat of COVID-19 to the environment and human health. Rimoldi et al. [62] reported the presence of SARS-CoV-2 RNA in treatment plants and in the receiving rivers in northern Italy, demonstrating the danger of inefficient sewerage systems.
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Figure 1. Transmission routes of COVID-19 virus to natural water bodies. WWTP = Wastewater treatment plant.
The presence of SARS-CoV-2 in feces and municipal wastewater raised the possibility of it spreading to wider water bodies from insufficiently treated effluent [31]. According to Wartecki and Rzymski [63], the survival of coronaviruses in natural waters depends on water temperature, light, organic matter concentrations, and predation. High water temperature decreased the viral loads due to the denaturation of viral enzymes and proteins [51]. Similarly, intense light and high predation would also decrease the viral concentrations in natural waters. However, high organic matter content would enhance the viral particles in natural waters [46,63][46][63]. The fate of SARS-CoV-2 RNA in surface waters is dependent on the efficiency of wastewater treatment plants and on potentially inactivating stressors such as sunlight, oxidative chemicals, and predation along the food chain [28]. In addition, Yang et al. [31] also reported that a high abundance of natural microbes could contribute to virus elimination via predation, antagonism, and nutrient competition. Thus, the role of environmentally friendly microbes to eliminate the virus should be further studied and elucidated. In fact, algae have been used to eliminate the virus by inducing the virus to attach to the algal biomass, which could be sedimented and removed [32].
The contamination of surface waters is more common than the groundwater, as the latter is deep down in the aquifer and is protected by soil filtration and sediment adsorption mechanism that could remove the virus. However, Selvam et al. [9] reported that there are active interactions between surface waters and the groundwater, indicating that the latter can be seriously infected by SARS-CoV-2 in areas with infected surface waters.

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