The European Market Remains the Largest Consumer of Frogs’ Legs from Wild Species

: The loss of biodiversity due to overexploitation is well known, but a review and regulation of species used in the frogs’ legs trade has yet to be accomplished. This problem relates to supply (the capture and trade of wild populations) and demand (the main consumer being the EU). The EU’s responsibility should not be ignored, since unsustainable imports of certain species drives population decline and increases risk of extinction. For most organisms, including frog species in the frogs’ legs trade, commercial international trade remains unregulated, includes species in extinction-threat categories on the IUCN Red List, and is not economically sustainable. With a tradition of frogs’ legs consumption anchored in western EU countries, demand for many species from the principal supplying countries (Indonesia, Vietnam, Turkey, Albania) has resulted in the overexploitation of the regional populations of many species. Unfortunately, legal trade takes place in the midst of numerous uncertainties, including unresolved taxonomic status for many frogs, no database or regulation of trade-relevant species, unknown population status, and no health standards for the animals involved in the trade. In addition, regional overharvest may increase the use of pesticides, there is uncertain but likely spread of disease along the trade chain, and certiﬁcation schemes for frog farming operations are both not standardised and can lead to exotic invasive species escaping into naïve ecosystems. Mechanisms to help make the international trade in frogs’ legs sustainable are essential, and require international agreement and targeted efforts, ideally ﬁnanced by the trade sector itself.


Background
We are experiencing the greatest species extinction rate in human history and holistic efforts to halt this trend require prudence and responsibility. The use and over-exploitation of natural resources for short-term economic gain while disregarding long-term losses can no longer be deemed justifiable. In addition, within the environmental issues we face, recognition of the importance of biodiversity conservation has lagged behind that of climate change for many years. Now, the conservation of biodiversity is finally being brought back into the public and decision-making spheres. Despite this, legal and exploitative wildlife trade continues to be overlooked, and for amphibians (with >1200 species in trade), this represents a major threat to the survival of many species since they lack basic standards to ensure sustainability [1]. Whilst global loss of wildlife is often blamed on developing regions, we cannot afford to ignore the role of the West in fueling global biodiversity loss through the unsustainable import of various species (see Table 1). One such example is the massive international frogs' legs trade to the European Union (EU) (especially Western Europe) representing the largest and almost entirely unregulated market.
In November 2022, 2500 delegates from governments, scientific institutes, non-governmental organisations, and industry met in Panama City for the 19th Conference of the Parties to CITES (the CoP19 of the Convention on International Trade in Endangered Species of Wild Fauna and Flora) with 184 member States. Based on 52 proposals and ca. 100 working documents, the conservation status of almost 600 species in commercial trade was discussed [2]. Despite an extensive agenda, however, only a fraction of wildlife trade was covered. For the vast majority of the commercial international trade in wildlife, including threatened and "Data Deficient" species (as evaluated in the IUCN Red List), this trade remains largely unregulated and a serious threat to their ecological persistence, much less their economic sustainability. Table 1. Historical and current characteristics of the global frog's legs trade (for details see [3,4]

Europe's Hunger for Frogs' Legs-A Threat to Biodiversity
The global trade in frogs' legs was not on the agenda of CITES CoP19, despite being a serious threat for an increasing number of amphibian species across a growing number of regions, mainly in Asia but also in South-Eastern Europe [3]. The substantial trade in frogs' legs, with annual EU imports of 4070 tonnes (cf. Figure 1), correlating roughly to 81-200 million frogs [4], is a good example of how the exploitation of wild populations can not only put the survival of targeted species at risk through unsustainable harvest rates, but can also have deleterious consequences for entire ecosystems (see Table 1). Wherever frogs are vanishing, an essential ecosystem service for pest control is lost, causing insect populations to dramatically grow and crop failures/damage, trophic cascades as communities change, and results in increased application of pesticides [6]. This, in turn, has negative consequences for remaining amphibians [7] as well as other species, including humans. The largely unmonitored overexploitation of frog populations, especially for consumption in Europe, has been going on for several decades.

Europe's Hunger for Frogs' Legs-A Threat to Biodiversity
The global trade in frogs' legs was not on the agenda of CITES CoP19, despite being a serious threat for an increasing number of amphibian species across a growing number of regions, mainly in Asia but also in South-Eastern Europe [3]. The substantial trade in frogs' legs, with annual EU imports of 4070 tonnes (cf. Figure 1), correlating roughly to 81-200 million frogs [4], is a good example of how the exploitation of wild populations can not only put the survival of targeted species at risk through unsustainable harvest rates, but can also have deleterious consequences for entire ecosystems (see Table 1). Wherever frogs are vanishing, an essential ecosystem service for pest control is lost, causing insect populations to dramatically grow and crop failures/damage, trophic cascades as communities change, and results in increased application of pesticides [6]. This, in turn, has negative consequences for remaining amphibians [7] as well as other species, including humans. The largely unmonitored overexploitation of frog populations, especially for consumption in Europe, has been going on for several decades. The development of the commercial trade in frogs' legs is global and has a history of mismanagement and unsustainability. For example, after local frog populations collapse and protective measures are put in place, the trade shifts to new countries or regions for supply. Subsequent frog populations are then exploited to the point of collapse and the cycle continues. International calls by several experts have voiced for the need of regulations to stop the "extinction domino effect" based on an ecological cascade stemming from the initial loss of a small number of species [3,4]. Furthermore, the lack of sustainability in the frogs' legs trade not only harms wild frog populations, but also impacts human livelihoods with insect pests (both for crop damage as well as arboviruses The development of the commercial trade in frogs' legs is global and has a history of mismanagement and unsustainability. For example, after local frog populations collapse and protective measures are put in place, the trade shifts to new countries or regions for supply. Subsequent frog populations are then exploited to the point of collapse and the cycle continues. International calls by several experts have voiced for the need of regulations to stop the "extinction domino effect" based on an ecological cascade stemming from the initial loss of a small number of species [3,4]. Furthermore, the lack of sustainability in the frogs' legs trade not only harms wild frog populations, but also impacts human livelihoods with insect pests (both for crop damage as well as arboviruses and other mosquito-mediated human diseases), increased pesticide use, and direct financial losses. and other mosquito-mediated human diseases), increased pesticide use, and direct financial losses. With its European Green Deal and Biodiversity Strategy 2030, the EU has defined ambitious targets to combat dramatic global loss of biodiversity and environmental degradation [9,10]. In practice, however, the EU remains a leading destination for legal and illegal wildlife and its products, with much of this trade neither regulated nor sustainable [11]. For instance, according to EUROSTAT, the European statistics database, the EU imported about 40,700 tonnes of frogs' legs between 2010-2019 [4], roughly 814-2000 million individual frogs. The vast majority of these frogs are taken from the wild, mainly in Indonesia, Turkey, and Albania, where large-legged frog species are primarily targeted, and local population declines have been documented. Only in Vietnam, the second largest supplier for the EU market (after Indonesia), are frogs farmed on a large scale. Wild native frog populations there are in double jeopardy: native species are collected to restock farms [12] and simultaneously displaced by highly invasive non-native species such as the American bullfrog (Lithobates catesbeianus) [13]. Indeed, there is an additional threat from the risk of pathogens (e.g., the fungus Batrachochytrium, which has driven widespread extinction in other regions) from invasive species introduced via the trade.
Problematic issues related to the EU's import of frogs' legs have been highlighted in 2011 [5], but no changes since then have been implemented to ensure a sustainable trade. Disregarding the extent of exploitation [4,14] and our inability to identify species that characterises the frogs' legs trade [3,15] only exacerbates prioritising short-term economic benefits that are deemed more important than the development of a sustainable international trade. This comes despite numerous efforts at multilateral international conventions, e.g., the CBD to halt the loss of biodiversity, including the Aichi Biodiversity Targets [16] and prior CITES exposure to the issues. A further reminder of the importance of understanding all dimensions of trade is from the ninth session of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES 9) in July 2022 in Germany, the new IPBES assessment report on sustainable use of wild species was launched [17]. Much of the current work on the report focuses on science-based valuation of natural resources as the central focus of economic decision making [18]. The frogs' legs trade also falls under the purview of the United Nations Sustainable Development Goals With its European Green Deal and Biodiversity Strategy 2030, the EU has defined ambitious targets to combat dramatic global loss of biodiversity and environmental degradation [9,10]. In practice, however, the EU remains a leading destination for legal and illegal wildlife and its products, with much of this trade neither regulated nor sustainable [11]. For instance, according to EUROSTAT, the European statistics database, the EU imported about 40,700 tonnes of frogs' legs between 2010-2019 [4], roughly 814-2000 million individual frogs. The vast majority of these frogs are taken from the wild, mainly in Indonesia, Turkey, and Albania, where large-legged frog species are primarily targeted, and local population declines have been documented. Only in Vietnam, the second largest supplier for the EU market (after Indonesia), are frogs farmed on a large scale. Wild native frog populations there are in double jeopardy: native species are collected to restock farms [12] and simultaneously displaced by highly invasive non-native species such as the American bullfrog (Lithobates catesbeianus) [13]. Indeed, there is an additional threat from the risk of pathogens (e.g., the fungus Batrachochytrium, which has driven widespread extinction in other regions) from invasive species introduced via the trade.
Problematic issues related to the EU's import of frogs' legs have been highlighted in 2011 [5], but no changes since then have been implemented to ensure a sustainable trade. Disregarding the extent of exploitation [4,14] and our inability to identify species that characterises the frogs' legs trade [3,15] only exacerbates prioritising short-term economic benefits that are deemed more important than the development of a sustainable international trade. This comes despite numerous efforts at multilateral international conventions, e.g., the CBD to halt the loss of biodiversity, including the Aichi Biodiversity Targets [16] and prior CITES exposure to the issues. A further reminder of the importance of understanding all dimensions of trade is from the ninth session of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES 9) in July 2022 in Germany, the new IPBES assessment report on sustainable use of wild species was launched [17]. Much of the current work on the report focuses on science-based valuation of natural resources as the central focus of economic decision making [18]. The frogs' legs trade also falls under the purview of the United Nations Sustainable Development Goals (SDGs), wherein SDG 15 indicates clear guidelines to protect and promote sustainable use of natural resources and prevent the loss of biodiversity. Data collected as part of the IUCN Red List assessments should be carefully assessed for compliance with the SDGs [19]. Unfortunately, this allows the trade to ignore species with out-of-date assessments (as well as unassessed species), assenting these species to continue to be exploited despite their unknown conservation status. With the upcoming CITES conference CoP 19 in November 2022, there is the opportunity to re-initiate the process of thoughtful legal and scientific conservation measures that has been on pause since 1985, when the most traded species in the trade were first listed in CITES Appendix II, a status that requires export permits to ensure sustainable levels of international trade.

Essential Considerations for a Sustainable Trade of Frogs' Legs
The path towards a more sustainable commercial trade is possible and beneficial in both the short-and long-term. Clarifying the uncertainties would allow population data to guide for a more sustainable commercial trade and better understand the impact harvest has on populations/species. This path, however, requires international agreement and focused effort, ideally funded by the trade itself. These are the very minimal essential elements for a successful sustainable trade of frogs' legs:

•
Before implementing a monitored sustainable trade of species and populations, the viability of these must be ensured to afford prescribed numbers for offtake; if necessary, some previously intensively used populations would need to be temporarily suspended from trade. Implement standardised certification schemes for frog farms to avoid negative local and regional ecological impacts.
Mechanisms to transition the international trade in frogs' legs to become sustainable and responsible are attainable, and are urgently needed before dire warnings are realised, e.g., (i) increase in overexploited species/populations, (ii) ongoing spread of (pathogenic) diseases, (iii) a regional increase in the use of pesticides, (iv) inclusion of other species harvested and traded for consumption, and (v) a more extensive detrimental impact on relevant ecosystems and their services. We strongly urge the decision-makers at CITES to enforce their mandated duty and promote a sustainable trade in frogs' legs. Data Availability Statement: Data on imports of frogs' legs were extracted from the publicly available database EUROSTAT, run by the European Union (https://ec.europa.eu/eurostat/web/main/ data/database (accessed on 27 August 2022)) and were filtered from the sub-database "EU trade since 1988 by HS2,4,6 and CN8" (categories 02082000 and 02089070 are frogs' legs fresh, chilled, or frozen) selected for the time 2010 to 2019. The IUCN Red List (https://www.iucnredlist.org/ (accessed on 27 August 2022)) was used to determine the officially evaluated conservation status of frog species relevant for this paper.

Conflicts of Interest:
The authors declare no conflict of interest.