COVID-19 disease

The COVID-19 disease, caused by the SARS-CoV-2 coronavirus, affects the respiratory system, producing symptoms similar to those of a cold with fever, joint and headache pain, and even oxygenation difficulties, which may lead to hospitalization and intubation in severe cases. In people with chronic degenerative problems such as diabetes, hypertension, and obesity, or with pneumonic affectations, infection with SARS-CoV-2 can produce clinical complications that increase the risk of death. SARS-CoV-2 is an RNA virus of zoonotic origin that was first observed in chiropterans and later mutated to infect humans. It appeared in China’s Wuhan province in December 2019 and is currently distributed throughout the world. It was officially declared a pandemic on March 11, 2020, by the World Health Organization (WHO). Mexico adopted health emergency measures on March 20 of the same year (^{DOF, 2020}). As of February 8, 2021, 105 million positive cases of SARS-CoV-2 and 2.3 million deaths had been reported worldwide (WHO, 2021). In Mexico, 2.13 million positives and 192866 deaths were estimated by that time (^{SSa, 2021}). Nine months later, at press time, Mexico recorded 3.78 million cases and 286 thousand deaths, an increase of 69 and 48%, respectively, despite an active vaccination program (Editor’s Note). The COVID-19 pandemic has affected the labor and productive sectors in several ways: 1) the amount of employment (both in terms of unemployment and underemployment); 2) the quality of work (with respect to wages and access to social protection); 3) the ability of the most vulnerable groups to stay afloat in the face of the adverse consequences in the labor market (ILO, 2020).

Agricultural activity during the COVID-19 contingency

In the context of the COVID-19 emergency, the Mexican Government considered agriculture, together with the inputs and supply chains associated with it, like an essential activity (^{DOF, 2020}). This included agricultural labor, fuel, seeds, fertilizers, chemical, and organic synthesis pesticides, biopesticides, and the production of biological control agents such as fungi, bacteria, insects, and mites. In Mexico, 38 crops are considered of strategic importance from a socio-economic perspective (^{SRE, 2016}). However, the Mexican agricultural production is more extensive due to the diversity of agroecosystems, cultivated plants, and culinary tradition, with a productive reserve of 2,500 species of plants. Although the human diet throughout the world is traditionally based mainly on wheat (Triticum aestivum), rice (Oryza sativa), and corn (Zea mays) (^{UNCSN, 2020}), other products have become part of the diet of many people as food supplements as a consequence of globalization. One of these products is avocado (Persea americana), which is native to Mesoamerica and currently among the 10 most important crops worldwide. Mexico is the main supplier, with a cultivated area of 231 thousand hectares and an annual production of 2.3 million tons (SIAP, 2019). Michoacán, the largest avocado-producing state in Mexico, has 28 to 30 thousand producers and 64 packing plants. In this state, avocado production generates an annual income of 2.7 billion dollars and 400 thousand jobs (^{APEAM, 2020}). Michoacan accounts for 34% of the international market for this fruit (SADER, 2019). Avocado is an important food supplement that provides a rich source of vitamins and minerals (^{Rajendran et al., 2017}; ^{SRE, 2016}; ^{Atlas Agroalimentario, 2018}; ^{SIAP, 2019}). The nutraceutical properties of avocado block the reduction of nitric oxide and has a protective effect against lipid peroxidation, a key contribution to the well-functioning of the immune system. It also acts as an antioxidant by reducing reactive forms of oxygen (^{Raya-Farías et al., 2018}). Its high content of unsaturated fats makes it a rich source of oils for the cosmetic and pharmaceutical industries.

In Ciudad Guzmán, Jalisco, an expanding productive region, avocado crops are affected by several pests, including thrips (Frankliniella bruneri, Heliothrips haemorrhoidalis, Scirtothrips perseae, S. aguacatae, S. kupandae, and Pseudophilothrips perseae), mites (Oligonychus punicae and O. perseae), bone and branch borers (Heilipmasus lauri), armored scales (Abgrallaspis aguacatae and Hemiberlesia lataniae), (^{Equihua-Martínez et al., 2007}). Avocado diseases include avocado sadness (Phytophthora cinnamomi) and verticillium wilt (Verticillium albo-atrum). The nematodes Helicotylenchus sp., Rotylenchulus sp., and Pratylenchus sp., have also gained importance in nurseries and seedlings (^{Tamayo, 2007}).

The present work aims to provide information on the effects of COVID-19 on the health of avocado plants cultivated in Ciudad Guzmán, Jalisco, Mexico.

Increased damage to crops by pests and diseases

The COVID-19 pandemic disrupted the phytosanitary management of avocado crops by hindering the sampling of thrips (Scirtothrips aguacatae), brown mites (O. punicae), and crystalline spiders (O. perseae) due to the reduced number of technical personnel responsible for monitoring and management. These activities are part of state technical assistance programs. The disruption led to an increase in infestation, external damage to flowering and fruits. It has been reported that these pests can reduce the photosynthetic rate of plants by up to 50% and decrease production by 20% (Moaz et al., 2010).

Technical personnel and pesticide applicators

The optimal management of avocado pests and diseases requires around 48.8 working days per hectare/year. When COVID-19 was declared a pandemic, Mexico´s Secretary of Health recommended voluntary confinement to the population. Despite the essential nature of agricultural work, it was estimated that the agricultural labor force decreased by 50%. This caused delays in the application of pesticides (conventional, organic, biological), which multiplied the impact by O. perseae and O. punicae, as well as the incidence (10%) of anthracnose (Colletotrichum gloeosporioides) (Personal Communication, 2020. Phytosanitary technicians) (Figure 1).

Supply of inputs and pesticides

There is a direct relationship between alterations of the immune system induced by exposure to pesticides and the prevalence of diseases associated with the immune response (^{Corsini et al., 2008}). This poses a potentially serious health risk for populations exposed to diseases like COVID-19. The lower number of agricultural workers since the declaration of the pandemic was declared caused suppliers of agricultural inputs to reduce their working hours and days, which reduced the immediate availability of synthetic and organic agrochemicals for the control of pests and diseases. At the end of 2020, respiratory diseases caused by seasonal flu and influenza type A and B increased due to the presence of cold temperatures, which also had an impact on the availability of labor. Agricultural production companies restricted access to people with possible COVID-19 symptoms to avoid the spread of the virus among production units. In this way, the production, selection, purchase, and timely application of pesticides was affected by the COVID-19 pandemic. In the absence of a global health contingency such as the current one, without the associated restrictions in the supply of inputs and labor, crop losses due to pests (e.g., mites, thrips, and scales), diseases (e.g. anthracnose), and weeds can reach up to 80% (^{Oerke, 2006}). Losses caused by plant pathogens alone cost the world economy US $220 billion each year (^{Savary et al., 2019}). The impact of the COVID-19 pandemic should be added to these costs, although there are still no global estimates of agricultural losses derived from the pandemic. However, the shortage of inputs and labor affected agricultural production in different ways, according to the production model. For example, organic agriculture and agroecological farming systems are less dependent on synthetic inputs compared to technified agricultural systems.

Figure 1 The operational management of the main avocado pests (Persea americana) was affected during the COVID-19 pandemic. It is exemplified with the mite Olygonychus punicae. Rational management is based on monitoring (A) the mite population level (B) and its natural control agents such as the predatory mite Amblyseius swirskii (C); with these criteria biorational products are applied (D). With effective management it is possible to reduce damage and obtain healthy and safety fruits (E). The growers training was not carried out with the frequency and interaction required due to social distance (F, H, I). There were delays in harvest due to lack of labor and limited transport (G). 

Marketing of agricultural products

Consumer requirements have changed over time and the agri-food industry is following new trends in health and safety. The factors that influence these trends include health considerations, marketing, work habits, idiosyncrasies, and socio-economic conditions. In Mexico, as in most countries affected by the COVID-19 pandemic, restrictions were established on the movement of people; crowd events or activities were canceled; shops, public spaces, and educational centers were closed. The restrictions on mobility in cities such as Monterrey, Guadalajara, and Mexico City, reduced the flow of food (foreign and local), which constitutes a major problem in places with high population density. The pandemic highlighted various aspects of the sustainability problems of large cities (^{Altieri and Nicholls, 2018}), mainly those related to health systems since large cities were the most affected. Avocado prices fell between 25 and 30% during the pandemic (^{APEAM, 2020}). In the first phase of the pandemic, the demand for food products increased due to panic purchases. Afterward, the demand for food decreased. Companies involved in the food chain are activating continuity plans to reduce the destructive effect of activities on the world economy. Retail companies are struggling to maintain supplies of staples, such as avocado. Manufacturers are actively adjusting their production and distribution strategies based on the needs and changing factors affecting the industry. The food products with the highest demand have been prioritized to guarantee an efficient supply in the short term. The decrease in air and land transport has limited the capacity to transport fresh produce over long distances by up to 20%, making supply a challenge (^{UWT, 2021}; ^{FAO, 2021}). Paradoxically, food is being underutilized as demand from restaurants, hotels, schools, stadiums, theme parks, and cruise ships decreases. Furthermore, transportation blockages disrupt fresh food supply chains and lead to higher levels of food loss and waste (^{Purdy, 2020}).

Conclusions

Avocado producers and phytosanitary management specialists in Ciudad Guzmán, Jalisco, estimate that the impact of the pandemic, in terms of phytosanitary conditions, might be between 10 and 20%. It is important to monitor the productive needs of avocado crops, such as inputs and labor, since agriculture, in general, has remained essentially active. Safe food production is a priority. This would allow societies and governments to be better prepared for a new health crisis. The strategy of rationally using the resources of an agroecosystem and producing artisanal products for the management of pests and diseases are alternatives that can help produce food in a sustainable way in small productive units. The use of biotechnological products is more appropriate for extensive agriculture systems (See contributions of Zelaya-Molina et al. and Ayala-Zepeda et al.). For example, the use of domestically produced plant extracts with antimicrobial or pest suppressive properties as a preventive strategy or during the early stages of the development of pests and diseases is a safe and sustainable management alternative. Plant extracts contain semiochemicals and toxins that can affect directly (^{Carrillo-Rodriguez et al., 2011}) or indirectly a wide variety of pests and pathogens (^{Roccuzzo et al., 2016}). However, further research is needed for these types of sustainable approaches. Agriculture can become an ally of human health through quality and healthy products.