REVIEWS IN FISHERIES SCIENCE & AQUACULTURE
2022, VOL. 30, NO. 1, 122–134
https://doi.org/10.1080/23308249.2021.1876633
NOTE
The Synergistic Impacts of Anthropogenic Stressors and COVID-19 on
Aquaculture: A Current Global Perspective
G. Sar
aa , M. C. Manganob , M. Berlinoa , L. Corbaria , M. Lucchesea , G. Milisendab , S. Terzoa
, M. S. Azazac , J. M. F. Babarrod , R. Bakiue , B. R. Broitmanf , A. H. Buschmanng ,
R. Christofolettih , A. Deiduni , Y. Dongj , J. Galdiesi , B. Glamuzinak , O. Luthmanl ,
P. Makridism , A. J. A. Nogueiran , M. G. Palomoo , R. Dineshramp , G. Rilovq , P. Sanchez-Jerezr
, H. Sevgilis , M. Troellt,u , K. Y. AbouelFadlv , M. N. Azraw , P. Britzx , C. Brugerey ,
E. Carringtonz , I. Celicaa , F. Choiab , C. Qinac , T. Dobroslavick , P. Galliad ,
D. Giannettoae , J. Grabowskiab, M. J. H. Lebata-Ramosaf , P. T. Limag , Y. Liuah , S. M. Llorensai ,
G. Maricchioloaj , S. Mirtoak , M. Pecarevick , N. Raggal , E. Ravagnanam , D. Saidian ,
K. Schultzab, M. Shaltoutao , C. Solidoroaa , S. H. Tanap , V. Thiyagarajanaq , and B. Helmuthab
aLaboratory of Ecology, Earth and Marine Sciences Department, University of Palermo, Palermo, Italy; bStazione Zoologica Anton
Dohrn, Department of Integrative Marine Ecology (EMI), Sicily Marine Centre, Palermo, Italy; cAquaculture Laboratory, National
Institute of Marine Science and Technology, Tunis, Tunisi; dInstituto de Investigaciones Marinas IIM-CSIC, Vigo, Spain; eDepartment of
Aquaculture and Fisheries, Agricultural University of Tirana, Tirane, Albania; fDepartamento de Ciencias, Facultad Artes Liberales,
Universidad Adolfo Iba~nez, Vin~a del Mar, Chile & Millennium Institute “Coastal Social-Ecological Millenium Institute” (SECOS); gCentro
i-Mar and CeBiB, Universidad de Los Lagos, Puerto Montt, Chile; hInstitute of Marine Sciences, Federal University of S~ao Paulo
(UNIFESP/IMar), S~ao Paulo, Brazil; iDepartment of Geosciences, University of Malta, Msida, Malta; jThe Key Laboratory of Mariculture,
Ministry of Education, Fisheries College, Ocean University of China, Qingdao, China; kDepartment of Applied Ecology, University of
Dubrovnik, Dubrovnik, Croatia; lSchool of Natural Science, Technology and Environmental Studies, S€odert€orn University, Huddinge,
Sweden; mDepartment of Biology, University of Patras, Rio Achaias, Greece; nDepartamento de Biologia and CESAM, Universidade de
Aveiro, Campus de Santiago, Aveiro, Portugal; oLaboratory of Marine Ecology, Natural History Museum of Argentina, CONICET,
Argentina; pBiological Oceanography Division, CSIR-National Institute of Oceanography, Dona Paula, Goa, India; qNational Institute of
Oceanography, Israel Oceanographic and Limnological Research, Haifa, Israel; rDepartment of Marine Science and Applied Biology,
University of Alicante, Alicante, Spain; sKepez Unit, Mediterranean Fisheries Research Production and Training Institute, Antalya,
Turkey; tStockholm Resilience Centre, Stockholm University, Stockholm, Sweden; uBeijer Institute of Ecological Economics, Royal
Swedish Academy of Sciences, Stockholm, Sweden; vAquatic Ecology Department, Faculty of Fish and Fisheries Technology, Aswan
University, Aswan, Egypt; wHigher Institution Centre of Excellence (HICoE), Institute of Tropical Aquaculture and Fisheries, University
Malaysia Terengganu, Terengganu, Malaysia; xDepartment of Ichthyology and Fisheries Science, Rhodes University, Grahamstown,
South Africa; ySoulfish Research and Consultancy, York, UK; zDepartment of Biology and Friday Harbor Laboratories, University of
Washington, Friday Harbor, WA, USA; aaNational Institute of Oceanography and Applied Geophysics – OGS, Sgonico, Italy;
abNortheastern University Marine Science Center, Nahant, MA, USA; acSouth China Sea Fisheries Research Institute, Chinese Academy
of Fishery Sciences, Beijing, China; adDepartment of Earth and Environmental Sciences, University of Milano-Bicocca, Italy;
aeDepartment of Biology, Faculty of Science, Mugla Sıktı Koçman University, Mugla, Turkey; afAquaculture Department, Southeast
Asian Fisheries Development Center, Tigbauan, Philippines; agBachok Marine Research Station, Institute of Ocean and Earth Sciences,
University of Malya, Bachok Kelantan, Malaysia; ahFaculty of Biosciences, Fisheries and Economics, UiT the Arctic University of Norway,
Tromsø, Norway; aiDepartamento de Ciencia Animal, Universitat Polit
ecnica de Val
encia, Val
encia, Spain; ajInstitute of Biological
Resources and Marine Biotechnologies, National Research Council (IRBIM-CNR), Messina, Italy; akInstitute of Anthropic Impact and
Sustainability in Marine Environment, National Research Council (IAS-CNR), Palermo, Italy; alCawthron Institute, Aquaculture Unit,
Cawthron Institute, Nelson, New Zealand; amNorwegian Research Centre (NORCE), NORCE Environment, Marine Ecology, Bergen,
Norway; anDepartment of Water and Environment, Faculty of Natural Sciences and Life, University Hassiba Benbouali of Chlef, Ouled
Fares Chlef, Algeria; aoDepartment of Oceanography, Faculty of Science, University of Alexandria, Alexandria, Egypt; apCentre for
Marine and Coastal Studies, Universiti Sains Malaysia, Penang, Malaysia; aqThe Swire Institute of Marine Science and Division of
Ecology and Biodiversity, The University of Hong Kong, Hong Kong, Hong Kong SAR
CONTACT Gianluca Sar
a gianluca.sara@unipa.it Laboratory of Ecology, Earth and Marine Sciences Department, University of Palermo, Viale delle
Scienze Ed. 16, 90128 Palermo, Italy.
Supplemental data for this article is available online at https://doi.org/10.1080/23308249.2021.1876633

 2021 The Author(s). Published with license by Taylor and Francis Group, LLC
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-
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or built upon in any way.
REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 123
ABSTRACT KEYWORDS
The rapid, global spread of COVID-19, and the measures intended to limit or slow its propaga- SARS-CoV-2 pandemic;
tion, are having major impacts on diverse sectors of society. Notably, these impacts are occur- supply chain; food
ring in the context of other anthropogenic-driven threats including global climate change. insecurity; climate change;
Both anthropogenic stressors and the COVID-19 pandemic represent significant economic multiple stressors;vulnerability; stakeholder
challenges to aquaculture systems across the globe, threatening the supply chain of one of perceptions; socio-
the most important sources of animal protein, with potential disproportionate impacts on vul- ecological systems
nerable communities. A web survey was conducted in 47 countries in the midst of the
COVID-19 pandemic to assess how aquaculture activities have been affected by the pandemic,
and to explore how these impacts compare to those from climate change. A positive correl-
ation between the effects of the two categories of drivers was detected, but analysis suggests
that the pandemic and the anthropogenic stressors affect different parts of the supply chain.
The immediate measurable reported losses varied with aquaculture typology (land vs. marine,
and intensive vs. extensive). A comparably lower impact on farmers reporting the use of inte-
grated multitrophic aquaculture (IMTA) methods suggests that IMTA might enhance resilience
to multiple stressors by providing different market options under the COVID-19 pandemic.
Results emphasize the importance of assessing detrimental effects of COVID-19 under a mul-
tiple stressor lens, focusing on areas that have already locally experienced economic loss due
to anthropogenic stressors in the last decade. Holistic policies that simultaneously address
other ongoing anthropogenic stressors, rather than focusing solely on the acute impacts of
COVID-19, are needed to maximize the long-term resilience of the aquaculture sector.
1. Introduction int/news-room/fact-sheets/detail/climate-change-and-
health) and the impacts of climate change continue
The COVID-19 pandemic broke out in late 2019 and
largely unabated. The World Health Organization
continues to spread across the planet. As of the mid-
estimates that annual excess deaths due to climate
dle of 2020, more than 81 million people have been
change will exceed 250,000 in the next decade, while
infected globally with deaths exceeding well over one
a recent report by the World Wildlife Foundation
million, and numbers continue to increase (https://
estimated annual economic losses of 479 billion USD
covid19.who.int/). While it is still impossible to esti-
by 2050 and a cumulative loss at about 10 trillion
mate exactly what the ultimate total economic damage USD, between 2011 and 2050 (Roxburgh et al. 2020).
from the global COVID-19 novel coronavirus pan- The ecological, social and economic impacts of the
demic will be, economists agree that it will have pandemic and their interactions with ongoing
severe negative impacts on the global gross domestic anthropogenic-driven changes are still unfolding (Baker
product (GDP). Economic costs of the COVID-19 et al. 2020), but they offer an opportunity to explore
pandemic for 2020 are estimated to be at least 2.4% of the perceived impacts and effectiveness of resilience
the GDP for the most major economies, resulting in strategies in addressing multiple stressors of both cli-
an unprecedented fiscal policy response of, to date, matic and non-climatic origin (O’Brien et al. 2004).
close to 11 trillion USD worldwide. This response rep- Here, these concepts were examined with a focus
resents a mobilization of economic resources from on global aquaculture, recognized as one of the fastest
local, regional and national governments, including growing sources of protein globally (FAO 2020a).
funds for maintaining the continuity of the global Interpreting how multiple stressors are likely to affect
food supply (International Monetary Fund https:// key stakeholder perceptions among aquaculture sys-
blogs.imf.org). Food sectors such as agriculture, fish- tems is not straightforward. The COVID-19 pandemic
eries and aquaculture have already reported severe has (nearly) simultaneously impacted (either directly
economic impacts and job losses due both to reduced or indirectly) much of the world’s population, as have
production capacity, as well as disrupted supply measures to limit or slow the spread of the virus. In
chains (FAO and CELAC 2020). Potential disruptions stark contrast, the impacts of anthropogenic stressors
to food production and supply chains remain of such as climate change on terrestrial food production
imminent concern as food insecurity, like the virus, sectors are often perceived not as a constant
will disproportionately affect vulnerable populations “pressure” (i.e. chronic/press stressor), but instead as a
(Gregory et al. 2005). series of short term, local or regional pulses (i.e.
In parallel, the year 2020 has been forecasted to be extreme events such as those generated by heatwaves,
among the hottest years on record (https://www.who. droughts, fire and floods, heterogeneous in space and
124 G. SARÀ ET AL.
time; Harris et al. 2018). Anthropogenic-driven stres- resilience of IMTA to external threats, while hypothe-
sors typically manifest themselves as asynchronous sized, has seldom been tested empirically (IFAD 2014).
and heterogeneous; different locations around the There is thus a critical need to determine the potential
globe experience climate-driven stressors that vary in effects of the COVID-19 pandemic on socioecological
type, magnitude and frequency (Pelham 2018). For and economic dynamics of the aquaculture sector.
example, while one region may be experiencing Understanding the magnitude of the perceived negative
drought, another, sometimes at the same time, may impacts of pandemic control measures and of climatic
suffer from floods; coastal environments experience and other anthropogenic stressors on aquaculture pro-
sea level rise, which has no direct effects on inland duction on a global scale should be a priority. Such an
populations. In part because of these asynchronies, understanding can guide capacity building and regula-
coordinated adaptation strategies to bolster resilience tions associated with sustainable development (SDGs,
to environmental threats in food production sectors is Agenda 2030) for a faster response in future scenarios.
difficult (Kaufmann et al. 2017). Many terrestrial
farmers, in particular those from Low-Income, Food-
2. Questionnaire structure and global
Deficient Countries (LIFDCs) and Small Island
distribution strategy
Developing States (SIDS) work in the most vulnerable
regions characterized by the highest values of Global To investigate the perceptions of COVID-19 effects
Climate risk index 2020 (e.g. Southeast Asian coun- on stakeholders operating in the aquaculture sector
tries). They experience detrimental effects to their (both land- and sea-based) a global web survey based
livelihood, while many in developed nations are reluc- on a semi-structured questionnaire was launched
tant to acknowledge climate-related impacts (Prokopy (study approved by the Ethical Committee at the
et al. 2015). Far less is known of the perceptions of University of Palermo, UNPA-183-Prot. 767-05/05/
the aquaculture sector to anthropogenic stressors 2020 n. 1/2020 29/04/2020).
including climate change, and while several studies The semi-structured questionnaire (see Appendix,
have been conducted at local and national scales, supplementary material) was designed with the pri-
none have been implemented on a global scale mary objective to collect stakeholder perceptions on
(Dubey et al. 2017). two main questions:
Aquaculture represents the fastest growing industry
in the fish and shellfish production sector and is rec- 1. Could you please indicate if there was an economic
ognized worldwide as among the most sustainable loss (direct or indirect economic loss) in your farm
options for improving food security and eradicating due to COVID-19?
poverty (Barange et al. 2018) tackling at least 7 out of 2. Among the following environmental causes that
17 United Nation Sustainable Development Goals have brought socio-economic loss in your farm in
(UN SDGs; Hambrey 2017). It also is among the most the last decade, which was more negative with
vulnerable to climate change (Froehlich et al. 2018; respect to that caused by COVID-19?
Sar
a et al. 2018). Aquaculture practices are not con-
fined to any one place and exist everywhere there is Data were also collected regarding type of aquacul-
water: in contained facilities on land, in freshwater ture systems, country, nation and role in the farm.
ponds and lakes, and in marine waters both under The semi-structured questionnaire was translated
intensive (e.g. species cultivated at high densities in into 14 languages (English, Italian, Spanish, Chinese,
artificial cages or tanks with feed added by growers) Croatian, Portuguese, Arabic, Hebrew, Turkish,
and extensive (e.g. species cultivated at lower densities Swedish, Greek, Maltese, Divehi, Albanian). A brief
in natural and created lakes and ponds, enclosed mar- presentation of the project and authors was added on
ine bays, rivers) conditions. In this context, integrated the first page, mainly to explain the reason for collect-
multitrophic aquaculture (IMTA) is recognized as a ing information and the potential final outcomes, as
sustainable form of aquaculture (Alexander et al. well as to obtain the informed consent of the respond-
2016). IMTA is a practice that incorporates species ents. Specific questions were designed to rapidly assess
from different trophic levels (e.g. not only herbivorous the perceptions of global aquaculture stakeholders –
bivalves or carnivorous fish cultivated alone but sev- specifically people involved in production at the farm
eral species representing different trophic levels being or within the company – of the direct or indirect eco-
farmed together) that results in reduction in organic nomic loss associated to COVID-19 and related con-
and inorganic wastes and their impacts. The increased trol measures (i.e. lockdown and social distancing)
REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 125
scaled from 1¼no economic loss at all, to 10¼ very that was distributed to stakeholders by asking all the
high economic loss (Appendix, supplementary mater- coauthors to serve as focal point, or rather to promote
ial). The reported economic impact due to COVID-19 the compilation of the survey among their communi-
was divided into four categories: no loss, low (2–4); cation and dissemination channels linked to aquacul-
moderate (5–7) and high (8–10). Respondents were ture sector. To ensure that the data collected were
also asked if they had previously experienced any representative of the reactive phase of the emerging
impacts from anthropogenic-driven changes in last COVID crisis, the web survey distribution had a dur-
decade that had led to greater economic losses than ation of three weeks, while the COVID-19 pandemic
those from the current COVID-19 pandemic. The was still fully active in most countries (5–29th May
anthropogenic stressors (more than one could be 2020). While we are aware that respondents were
chosen) included: heatwaves, hypoxia/anoxia, harmful experiencing different stages of the pandemic during
algae, local pollution, storms, diseases caused by bac- the survey, we decided to keep the survey active dur-
teria, viruses and parasites affecting target species, ing a short temporal window to both facilitate a rapid
sudden changes in salinity, flooding and eutrophica- assessment and to avoid including any later, post-
tion. Farmers were also asked about their use of pandemic stages. Replies were coded as a function of
IMTA and compared this information with the per- geographic position of the farms and the typology of
ceived economic loss of either COVID-19 or aquaculture (land vs. sea-based, and intensive vs.
anthropogenic stressors. extensive). The survey reached 54 countries across five
The semi-structured questionnaire was transferred continents (Figure 1).
on Qualtrics https://www.qualtrics.com, an online Data were analyzed with multivariate techniques
platform that allowed the creation of a web survey (permutational analysis of variance and principal
Figure 1. Countries covered by the global web survey (launched on 5th and closed on 29th May 2020), colored dots have been
grouped per each of the 54 countries reached across the five continents (see legend). Of a total of 585 respondents to our survey,
483 (83%) from 45 over 54 involved countries, reported that anthropogenic stressors had greater impacts than the pandemic.
None of the respondents from Bangladesh, Belgium, California, Germany, Maldives, S~ao Tome and Prıncipe, Slovenia, South Korea,
or Venezuela reported impacts of anthropogenic stressors that exceeded the impacts of COVID.
126 G. SARÀ ET AL.
component analysis). A 3-way Permutational aquaculture or the country. All the statistical analysis
Multivariate ANOVA (PERMANOVA, Anderson 2001) and graphical ordinations were performed using
– performed on a triangular matrix based on Jaccard PRIMER6 and PERMANOVA and R [R version 4.0.2
index – was used to test significant differences between (2020-06-22)]. The R package used were: “vegan” and
multivariate response data, represented by the presence “stats” (http://www.R-project.org/; http://vegan.r-forge.
or absence of each type of “anthropogenic stressors” r-project.org/).
reported by respondents, and the different levels of the
three explanatory variables: “Country,” “Type of aqua- 3. COVID-19 and anthropogenic stressors: a
culture,” “Degree of Salinity.” The experimental design global analysis through stakeholder
comprised: factor “Country,” fixed with 25 levels, factor experiences
“Type of aquaculture,” random and nested in Of a total of 585 respondents (colour labeled in
“Country,” with 4 levels, factor “Salinity,” random and Figure 1), 483 (83%) reported that anthropogenic
Nested in “Country,” with 5 levels. Nested design and stressors had greater impacts than the pandemic, and
permutational analysis of variances have been chosen to here responses from that subset were analyzed. This
deal with non-balancing data (Primer V.7 http:// subset represents respondents from 45 countries and
updates.primer-e.com/primer7/manuals/User_manual_ did not include farmers from Bangladesh, Belgium,
v7a.pdf). Germany, Maldives, S~ao Tome and Prıncipe, Slovenia,
The visualization of multivariate data was obtained South Korea, or Venezuela. Farmers from China,
through a principal components analysis (PCA). PCA Turkey, Brazil, Spain, Egypt, Ireland, Portugal, Italy,
was performed on similarity matrix based on Jaccard and Tunisia comprised about 70% of these replies;
index derived from multivariate presence/absence 13% and 42% of the respondents worked in land-
dataset as described above (Borcard et al. 2011). The based intensive and extensive aquaculture, respect-
first two components accounted for over 50% of the ively, and the rest in marine open water farming, both
variance (PC1 37%; PC2 18%). The function intensive (21%) and extensive (24%). The low
“envfit,” which fits environmental vectors or factors response rate from some countries precludes a
onto an ordination, was used to graphically display detailed analysis on a country-specific basis. Of all
correlation between responded variable and explana- respondents, 92% reported being impacted by the
tory variables. Redundancy analysis was used to test COVID-19 pandemic but at the same time 83% also
significant relations between the amount of economic reported impacts caused by environmental stressors
losses, represented by four categories: “no-losses,” such as heatwaves, hypoxia or eutrophication (among
“low,” “medium” and “high,” and the type of other anthropogenic stressors examined). Responses
Figure 2. Reported economic loss due to COVID-19 ranked into four categories: no effect (1), low (2–4); moderate (5–7) and high
(8–10) with associated experience of any impacts from anthropogenic driven. Respondents were asked to scale the economic loss due
to COVID-19 from 1¼ no economic loss at all, to 10¼ very high economic loss and to report any impacts from anthropogenic-driven
changes in last decade recognized to have led to greater economic losses than those from the current COVID-19 pandemic. The
anthropogenic stressors (more than one could be chosen) included: heatwaves, hypoxia/anoxia, harmful algae, local pollution, storms,
diseases caused by bacteria, viruses and parasites affecting target species, sudden changes in salinity, flooding and eutrophication.
REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 127
Figure 3. Principal component analysis (PCA) on stakeholder responses on economic-loss perception associated with anthropo-
genic stressors analyzed (heatwaves, hypoxia/anoxia, harmful algae, local pollution, storms, diseases, sudden changes in salinity,
flooding and eutrophication – light blue) depending on the four explored aquaculture systems (land-based intensive L-INT, land-
based extensive L-EXT, sea-based intensive S-INT, sea-based extensive S-EXT – orange upper panel – A) and countries (black lower
panel – B).
128 G. SARÀ ET AL.
Table 1. PERMANOVA results (SS¼ sum of squares; MS¼mean squares; p¼ probability; perms¼ 0 number of permutations)(ns¼ no significant difference; difference at p< 0.05; difference at p< 0.01; difference at p< 0.001).
Source df SS MS Pseudo-F P (perm) Perms P (MC)
Country (Co) 21 1.12Eþ 05 5320.1 1.405 0.018 999 0.006
Typology (Co) 42 1.39Eþ 05 3317.7 1.3765 0.106 999 0.006
Salinity (Co)  47 1.53Eþ 05 3263.3 1.3497 0.116 998 0.004

Typology (Co)salinity(Co) 22 49103 2231.9 0.78615 0.938 997 0.961ns
Residuals 248 7.04Eþ 05 2839.1
Total 391 1.30Eþ 06
Table 2. Countries for which respondents reported to have previously experienced any impacts from anthropo-
genic-driven changes - in last decade - that had led to greater economic losses than those from the current
COVID-19 pandemic (significant values are reported) (ns = no significant difference; * = difference at p < 0.05;
** = difference at p < 0.01; *** = difference at p < 0.001).
Significant Factors Country PC1 PC2 r2 p
Salinity, flooding, harmful algae, Algeria −0.41115 −0.91157 0.0124 0.057 ns
hypoxia, pollution, eutrophication, China −0.64939 −0.76045 0.0528 0.001***
heat waves Croatia −0.80307 −0.59589 0.011 0.087 ns.
Egypt −0.42291 −0.90617 0.0496 0.001***
Malaysia −0.56045 −0.82819 0.0143 0.041*
Diseases, storms Brazil 0.65119 0.75892 0.0158 0.035*
Greece 0.99562 0.09349 0.0378 0.002**
India 0.99979 0.0207 0.0303 0.003**
Peru 0.95605 0.29321 0.0228 0.006**
Spain 0.61872 0.78561 0.0153 0.036*
Tunisia 0.46729 0.8841 0.03 0.005**
Storms Chile −0.76742 0.64115 0.0226 0.006**
Italy −0.37399 0.92743 0.0138 0.050*
Malta −0.13977 0.99018 0.0437 0.001***
Sweden −0.93799 0.34666 0.0163 0.026*
Diseases United Kingdom 0.98232 −0.18719 0.018 0.02
to these interactive crises tend to differ; unlike the farmers affected by moderate and low economic loss,
pandemic, climate-related effects are usually heteroge- respectively. Principal component analysis (PCA)
neous in space and time and manifest themselves showed globally that diseases, hypoxia, pollution,
more indirectly via threats such as heat waves, eutrophication and heatwaves were perceived as more
drought or flooding that act from regional to local detrimental in land-based systems, while impact of
scales. Among anthropogenic stressors, transient (i.e. storms was reported as a more relevant issue in the
pulse) disturbance factors of purely climatic origin sea-based intensive systems. Salinity increase, flooding
(i.e. heatwaves, storms and floods) accounted for and harmful algae were reported to be more detri-
33.3% of replies, while pervasive (i.e. press) local and mental in sea-based extensive systems (Figure 3A;
regional factors (i.e. hypoxia, pollution, harmful algae, Table 1). A significant difference across the covered
eutrophication, salinity changes) represented 66.7% of countries is evident (Figure 3B). Salinity increase,
replies. Overall, farmers who reported no economic flooding, harmful algae, hypoxia, pollution, eutrophi-
loss due to COVID-19 (7% of respondents) also cation and heat waves were recognized as a source of
reported a lower frequency of anthropogenic factors economic loss greater than COVID-19 in China,
affecting their activities in the last decade (Figure 2). Egypt and Malaysia while diseases and storms were
Farmers reporting an economic loss due to COVID- perceived as more damaging in Brazil, Greece, India,
19 over all other levels (low, intermediate and high) Peru, Spain, Tunisia, Chile, Italy, Malta and Sweden
also reported a significant increase in the occurrence (Table 2). Figure 4 details the levels of economic loss
of anthropogenic effects on their activities. Among due to COVID-19 and anthropogenic effects by coun-
them, flooding and eutrophication were most fre- try and aquaculture typology. Whereas extensive,
quently reported among farmers affected by the high- land- and sea-based aquaculture was seemingly the
est COVID-19 economic loss, while diseases and most vulnerable, intensive practices were able to par-
salinity increase were most frequently reported among tially buffer the effects.
REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 129
Figure 4. Anthropogenic stressors (number of occurrence, N) reported as by respondents, respectively mapped per each of the
four explored aquaculture systems (land-based intensive, land-based extensive, sea-based intensive, sea-based extensive), per each
surveyed country perceived as more negative with respect to COVID-19 in the last decade (right side). On the left side, histograms
with the percentage of replies per each stressor were reported as combined with economic loss due to COVID-19 categories: high,
moderate, low, no effect.
130 G. SARÀ ET AL.
Figure 4. Continued.
REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 131
Figure 4. Continued.
production sectors, a further crisis such as COVID-19
pandemic amplifies economic losses and food in
security. These results align with current ecological
theory explaining how multiple stressors can affect a
socioecological system’s responses (Crain et al. 2008).
In general, the crisis due to the COVID-19 pandemic
adds a further stressor to already locally suffering, vul-
nerable, aquaculture systems (Froehlich et al. 2018). A
recent FAO (2020b) report showed a greater percent-
age of COVID-19 economic loss associated with the
first and final links of the supply chain (raw material
provision, product transport and sale). COVID-19
affects the aquaculture supply chain by limiting, for
instance, the ability to supply food to consumers due
Figure 5. Anthropogenic stressors (number of occurrence, N) to closed markets and restaurants (HORECA – hotels,
reported as by respondents, respectively per each of the four restaurants, cafes/catering sector), disrupting the logis-
explored aquaculture systems (land-based intensive L-INT, tics associated with transportation (both raw materials
land-based extensive L-EXT, sea-based intensive S-INT, sea-
based extensive S-EXT) in presence (IMTA) and absence of inte- and final products) and increasing border restrictions
grate multitrophic aquaculture (no-IMTA). (FAO 2020b). In contrast, anthropogenic stressors
such as climate change and pollution, more likely
drive economic loss on the intermediate links, i.e. the
Some of the respondents reported: “It [COVID-19] health status, growth and survival rate of cultivated
has no significant effect compared to local pollution (as organisms (and thus on the production) (Weatherdon
ammonia increase)” (Egypt); “It is a serious necessity et al. 2016; Peck et al. 2020) (Figure 6). Thus, the
to determine the industrial and environmental pollu- COVID-19 pandemic is adding further vulnerability
tion on bacteria and microorganisms in the water” to already stressed socioecological systems (Bennett
(Turkey); “The recurring drought of the past 3 years et al. 2020; FAO 2020b) by acting on different stages
has had a more serious effect” (Italy); “The rainy season of the supply chain. In this context, any possible man-
drops sharply and the dry season is too high!” (China). agement practices to enhance the resilience of aqua-
In addition, overall, when IMTA was used, data culture food systems must occur across the
suggested that there was a tendency to dampen the production, transformation and stages of the supply
detrimental effects of COVID-19 (Figures 5 and 6), chain, if they are to help aquaculture to cope with
with IMTA reducing the impacts of organic and inor- future pandemic crises. A holistic, multiple stressors-
ganic waste in aquatic environments. based view that can decrease the vulnerability of the
Results show that where anthropogenic-driven aquaculture sector by also safeguarding the intermedi-
changes are negatively impacting aquaculture food ate links of the supply chain (e.g. production,
132 G. SARÀ ET AL.
Figure 6. Graphical representation of the double trouble of aquaculture systems COVID-19 and anthropogenic stressors interac-
tions through the supply chain.
maintenance, growth), and not just those directly De Mazancourt 2013, 25), something to consider
affected by the pandemic is needed (e.g. market). The when planning future recovery policy in context of
potential role of IMTA in buffering the effects of both post COVID-19 and anthropogenic resilience.
anthropogenic stressors on aquaculture loss is already
described in literature from the last two decades 4. A need for multiple stressors-based
(Shpigel and Neori 1996) and its value under pan- recovery plans
demic emerged among some of the respondent com-
ments, i.e. “It is recommended to increase the use of Unlike pressing anthropogenic stressors (which can
advanced equipment and integrated approaches have a slower onset and are global) and pulse disasters
(IMTA) to reduce dependence on people” (China) (which have a rapid onset but are localised), the very
and “Focus on prevention, increase varieties of species rapid onset and global nature of COVID-19 pandemic
(IMTA), increase species with high added value, and has caught the aquaculture sector (and everyone) off-
improve survival rate” (China). guard, and affected production and supply in ways
Generally, farmers cultivating more than one spe- that had not been predicted or anticipated. The indus-
cies using IMTA protocols, also reported fewer eco- try sector, and especially aquaculture, should be better
nomic impacts due to COVID-19. By contrast, sectors equipped to deal with a world subjected to growing
with monoculture practices (i.e. large, biomass-dense global crises. Synergies of COVID-19 and anthropo-
systems with a monodirectional energy input) genic stressor effects can be critical in terms of both
(Bardach 1997) and few marketed products were more detection and policy responses. The main lesson learnt
vulnerable. Increasing the number of species under from the COVID-19 pandemic is the importance of
IMTA conditions results in a more diverse ecological taking rigorous, strict and fast disaster-risk manage-
system that is more resilient as it is more able to cope ment approaches to adapt to a novel sudden shock
with anthropogenic stressors and different market condition and to safeguard life. In the near future, as
demands (e.g. diversification of product lines to fill economic aid becomes available to rebuild economies,
alternative markets) (Worm et al. 2006; Loreau and it will be time to act. The crisis offers an invaluable
REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 133
opportunity for decision makers and stakeholders to B. Glamuzina http://orcid.org/0000-0002-5066-4599
improve communication skills, logistics and connect- O. Luthman http://orcid.org/0000-0002-6227-8484
ivity among them to generate more secure farms, to P. Makridis http://orcid.org/0000-0002-0265-4070
A. J. A. Nogueira http://orcid.org/0000-0001-7089-2508
promote food services and a framework for a long- M. G. Palomo http://orcid.org/0000-0002-9102-1282
term sustainable aquaculture industry for local people R. Dineshram http://orcid.org/0000-0002-6723-4587
and regional economies. COVID-19 provides a unique G. Rilov http://orcid.org/0000-0002-1334-4887
opportunity to unite stakeholders, managers and pol- P. Sanchez-Jerez http://orcid.org/0000-0003-4047-238X
icy makers around what is perceived as a common H. Sevgili http://orcid.org/0000-0001-8274-7391M. Troell http://orcid.org/0000-0002-7509-8140
threat (global pandemic). The policies issued in the K. Y. AbouelFadl http://orcid.org/0000-0002-4585-833X
next months, could have the added benefit of enhanc- M. N. Azra http://orcid.org/0000-0001-9333-9270
ing resilience to other stressors such as climate change P. Britz http://orcid.org/0000-0002-4436-0425
that, otherwise, may exacerbate the crisis and make C. Brugere http://orcid.org/0000-0002-1412-1044
E. Carrington http://orcid.org/0000-0001-8741-4828
recovery more difficult and expensive. I. Celic http://orcid.org/0000-0002-3438-3690
F. Choi http://orcid.org/0000-0003-4389-8087
Acknowledgments C. Qin http://orcid.org/0000-0002-3073-1563T. Dobroslavic http://orcid.org/0000-0003-3805-3186
We are grateful to all the respondents who took the time P. Galli http://orcid.org/0000-0002-6065-8192
to take the survey. The Open Access publication of the D. Giannetto http://orcid.org/0000-0002-3895-5553
MS was funded by M. Cristina Mangano FOE N. 418 at M. J. H. Lebata-Ramos http://orcid.org/0000-0001-
Stazione Zoologica Anton Dohrn (personal OA publica- 7598-038X
tion fund). People at Laboratory of Ecology have been P. T. Lim http://orcid.org/0000-0003-2823-0564
found by the PRIN-MAHRES project (Ministry of Italian Y. Liu http://orcid.org/0000-0001-6520-4854
Research; MUR) 2017MHHWBN_003 Linea C and by the S. M. Llorens http://orcid.org/0000-0002-9824-3267
HARMONY Project Italy-Malta 2016 (grant C1-3.1-31) G. Maricchiolo http://orcid.org/0000-0002-5670-6243
funded by the Sicilian Region and Maltese Government. S. Mirto http://orcid.org/0000-0003-4707-7307
A. Nogueira thanks FCT/MCTES for the financial sup- M. Pecarevic http://orcid.org/0000-0003-4665-2103
port to CESAM (UIDP/50017/2020+UIDB/50017/2020), N. Ragg http://orcid.org/0000-0002-5466-4617
through national funds. J.M.F. Babarro thanks project E. Ravagnan http://orcid.org/0000-0002-9724-3660
PID2019-106008RB-C21 for support through Spanish D. Saidi http://orcid.org/0000-0001-6382-8073
M. Shaltout http://orcid.org/0000-0002-0429-3029
Government funds. We additionally thank Gaspare
C. Solidoro http://orcid.org/0000-0003-2354-4302
Barbera for his technical feedback during the question- S. H. Tan http://orcid.org/0000-0001-8690-047X
naire design, Marko Yusup, Gavin Burnell, Mattew Slater V. Thiyagarajan http://orcid.org/0000-0002-2062-4799
and Gray A. Williams and many other colleagues for their B. Helmuth http://orcid.org/0000-0003-0180-3414
effort done in facilitating the circulation of questionnaires.
We are grateful to QUALTRICS (Inc. USA) Product
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