An overview of the Brazilian frog farming

Highlights

• There are ca. 150 bullfrog farms in Brazil, producing approximately 400 tons of bullfrog and moving 1.9 million USD / year.

• Bullfrog trade in Brazil is largely focused to local sales, however interstate and international trade also occur.

• The lack of regulation and standards in the production are key obstacles to the activity.

• We highlight potential improvements to the activity for the consumer market, production workflow, and environmental awareness.

Abstract

World population growth demands an accelerated increase in food production especially that of animal origin. One of the main global challenges is to couple such a production with environmental health. The production of aquatic animals, i.e., aquaculture, tends to be less harmful to the environment due to the reduction of crop yield requirements and the decrease in land areas for cultivation and grazing. In addition, it is associated with a wide range of cultivated species and production systems, which is related to the resilience of the global food system. The bullfrog, Aquarana catesbeiana (Shaw, 1802), production, known as frog farming or ranaculture, could represent an economically competitive and environmentally conscious production opportunity. Brazil is a pioneer and one of the world's largest bullfrog producers. However, up to this date there is no data compilation about its current and past production. Here, we present current data on bullfrog production, national and international trade, and relevant environmental issues related to frog farming in this country. We compiled information about Brazilian bullfrog farms from February 2019 to January 2020, and obtained information on production and trade directly from the producers. We described the frog farming workflow and classified the farms by the processes they accomplish. We mapped 151 bullfrog farms distributed mostly in southeastern Brazil. In 2019 we estimated a production of about 400 tons (gross weight), which generated roughly 200 net tons of bullfrog meat, moving about 1.9 million USD. In addition, we mapped the local, interstate, and international bullfrog production commercial routes. Brazilian frog farming has great expansion potential; nevertheless, improvements are required, both in the consumer market, as well as in the production and overall frog farming workflow. We highlight the main aspects that need improvement to expand and generate visibility for frog farming in Brazil, from an economic and environmental feasible perspective.

Introduction

Human population growth and the increase of individual income in many countries are intensifying the global consumption of animal food source (Godfray et al., 2018; Steinfeld et al., 2006; Vranken et al., 2014). Feeding a growing population and reducing the pressures of food production on the environment is a major challenge (Froehlich et al., 2018b; Herrero et al., 2015; Macdiarmid et al., 2016). The assessment of negatives impacts caused by animal production is generally centered on land use (Froehlich et al., 2018b). For instance, livestock uses about 80% of the planet's agricultural land, the vast majority of which are represented by extensive ruminant systems (Herrero et al., 2015). There are major differences on the impact level, which can vary according to the produced species, the type of product, and the applied production method (Hilborn et al., 2018). A more efficient and diversified food system, whether due to the number of species produced, places of production and/or feeding strategies is linked to resilience in the global food system (Troell et al., 2014).

The adoption of a diversified diet, consisting of small daily portions of different types of meat or other products of animal origin (Willett and Skerrett, 2005) implies in a reduction of the required areas of arable land and pasture (Stehfest et al., 2009). The land area required for food production will increase in all future scenarios, but millions of hectares could be spared by an increase in human diets based on a higher proportion of aquatic animal protein (Froehlich et al., 2018b). Human diets in which aquatic organisms are dominant when compared to livestock could reduce annual crop yield requirements by 34 million tons and decrease land areas for cultivation and grazing, saving ca. 750 million hectares (Froehlich et al., 2018b). Furthermore, while terrestrial food production is based on a limited number of species, aquaculture uses a wide range of cultured species and different production systems (Subasinghe, 2005). More than 330 species are farmed, including a variety of taxa, such as crustaceans, mollusks, fish, amphibians, and alligators (FAO, 2019; Metian et al., 2020).

Currently, aquaculture represents the fastest growing food production sector in the world, increasing its global production almost fivefold from 1990 to 2015, and it is expected to double by the middle of this century (Froehlich et al., 2018a; Ottinger et al., 2018; Tacon, 2020). In 2012 the cultivation of aquatic species exceeded the production of beef, which has always remained the main protein source in the world (Larsen and Roney, 2013). In 2017 aquaculture production was about 80 million tons, with over 66.7% represented by fish, followed by mollusks (21.7%), crustaceans (10.5%) and others, such as sea cucumbers, sea urchins, frogs, and turtles (1.1%) (FAO, 2019). Most of this production comes from developing countries (Subasinghe, 2005), especially in South America, which are recognized for their large production and high economic impact on local and global aquaculture (Valladão et al., 2018). In addition to extensive fish production, South American countries also produce a variety of aquatic organisms, including shrimp, shellfish, and frogs (Valladão et al., 2018).

Aquaculture systems require large amounts of good quality water sources to sustain the long-term growth and health of the produced species (Qing et al., 2021). Besides, environmental impacts are associated with aquaculture such as the degradation and contamination of water systems due to the increase in nutrient concentration in the aqueous medium, which relates to the accumulation of excretion and uneaten feed residues (Qing et al., 2021; Viegas et al., 2021). Organic and inorganic nutrients figure among the main contaminants, such as ammonia, nitrite, and phosphorus, as well as a diversity of microorganisms, including pathogens (Díaz et al., 2011; Rosa et al., 2020).

Frog production, frog farming, or ranaculture, has been recorded since the 20th century (Altherr et al., 2011; FAO, 2021), although frog consumption dates back at least to the 16th century (Neveu, 2004). Frog meat, especially frog legs, has white color, soft texture, and mild flavor (Herbst, 1995), being considered a delicacy in Europe (Tyler et al., 2007). In the 1980's, Asian countries had high exports, which had been accompanied a world consumption of 6500 tons of frog legs per year (Beebee, 1996). In recent years, it has attracted the attention of consumers who are increasingly concerned with health, due to its nutritional characteristics, such as low lipids percentage and high quality of proteins and amino acids (Oliveira et al., 2017; Paixão and Bressan, 2009). Frog production requires special facilities for different life stages (tadpole vs. post-metamorphic) and several specifications for breeding practices, such as temperature and water quality control, nutrition, and adequate sanitation (Cribb et al., 2013; Lutz and Avery, 1999). Prominent technological advances have maximized frog farming expansion, increasing the production under controlled conditions (Olvera-Novoa et al., 2007). Currently, the main frog producers are based in Asia (Taiwan and China) and Latin America (especially Brazil and Mexico) (FAO, 2019; Mello et al., 2016), while Europe and the USA represent the largest consumers and importers in the world (Altherr et al., 2011; FAO, 2019; Neveu, 2004).

Few frog species are used as meat source, including the European green frog [Pelophylax ridibundus (Pallas, 1771)], the East Asian bullfrog [Hoplobatrachus rugulosus (Wiegmann, 1834)], and other Rana spp. However, the North American bullfrog (Aquarana catesbeiana; hereafter bullfrog), is the most farmed amphibian globally (FAO, 2021) (Fig. 1A). Due to its ease of handling, rapid growth, prolificacy, large size, and fleshy legs, it is favored by producers (Cribb et al., 2013; Lutz and Avery, 1999). As a result, it has been introduced in more than 40 countries for frog farming (FAO, 2021; Frost, 2021; García et al., 2020).

Frog production has either increased or maintained stable over the years. We observed an increase of over 100% in world production in 2018 when compared to 2010. From 2010 to 2018 the world average production was approximately 3200 tons of bullfrog per year, led by Taiwan, but with great contributions from Malaysia, Singapore, Brazil, Ecuador, and Mexico (FAO, 2021) (Fig. 1B and C). Even though bullfrog production is still not as representative as other aquatic species, its worldwide production is growing and has contributed to the global economy with an average of 11 million USD per year movement from 2010 to 2018, reaching its peak in 2013, with 14.5 million USD (FAO, 2021) (Fig. 1B). The bullfrog production is ecologically relevant as well, as the increase in its consumption could reduce beef's and add resilience to the food system (Froehlich et al., 2018b; Troell et al., 2014). On the other hand, it represents one of the worst invasive species in the world, a condition directly related to the development of frog farming and its (in)consequent introduction in several countries, including Brazil (Ficetola et al., 2007; Govindarajulu et al., 2006; Kraus, 2015; Lowe et al., 2000; Lutz and Avery, 1999).

Bullfrogs are well adapted to Brazilian climatic conditions, where numerous feral populations were reported (Both et al., 2011). In addition, a model predicted high likelihood rates of occurrence and success in the establishment of bullfrog populations in Brazilian regions, especially in the south and southeast (Giovanelli et al., 2008). Invasive species play an important role in the global amphibian crisis and can directly or indirectly affect native amphibian fitness, population size and dynamics, and community structure (Carpenter et al., 2014; Falaschi et al., 2020; Fisher and Garner, 2007; Manenti et al., 2020). Bullfrogs can prey on native anurans (Boelter et al., 2012; Leivas et al., 2013; Silva et al., 2011; Toledo et al., 2007), interfere on native amphibian acoustic communication (Both and Grant, 2012; Forti et al., 2017; Medeiros et al., 2017), and act as pathogens carriers (Brunner et al., 2019; O'Hanlon et al., 2018). Therefore, frog farmers must avoid accidental bullfrog releases into the surrounding environments.

Brazil was one of the first countries to import live bullfrogs (FAO, 2005; Schloegel et al., 2010b), and since then it represents one of the largest contributors and suppliers of technology for frog farming (Pahor-Filho et al., 2019). Brazilian bullfrog farms have promising infrastructure, environmental conditions, and a potential market in several regions of the country (Feix et al., 2006; Rodrigues et al., 2010; Sousa and Maltarolo, 2019). However, the slow process of environmental licensing and producer registration and the laboriousness in products transportation (Cribb et al., 2013) has led to the sector instability, lack of production and trade data, or even the difficulties to access them. As a result, there is great complication in carrying out studies and research for innovations, improvements in the activity, and consequently, in the development of action plans aimed at the conservation of native species. Hence, we here present an updated data on the number and distribution of bullfrog farms in Brazil, as well as economic and environmental aspects of the Brazilian frog farming, with perspectives for the sustainable development of this activity.