Review Article |
Corresponding author: Mark Auliya ( m.auliya@leibniz-lib.de ) Academic editor: Franco Andreone
© 2023 Mark Auliya, Sandra Altherr, Charlotte Nithart, Alice Hughes, David Bickford.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Auliya M, Altherr S, Nithart C, Hughes A, Bickford D (2023) Numerous uncertainties in the multifaceted global trade in frogs’ legs with the EU as the major consumer. Nature Conservation 51: 71-135. https://doi.org/10.3897/natureconservation.51.93868
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The commercial trade in frogs and their body parts is global, dynamic and occurs in extremely large volumes (in the thousands of tonnes/yr or billions of frogs/yr). The European Union (EU) remains the single largest importer of frogs’ legs, with most frogs still caught from the wild. Amongst the many drivers of species extinction or population decline (e.g. due to habitat loss, climate change, disease etc.), overexploitation is becoming increasingly more prominent. Due to global declines and extinctions, new attention is being focused on these markets, in part to try to ensure sustainability. While the trade is plagued by daunting realities of data deficiency and uncertainty and the conflicts of commercial interests associated with these data, it is clear is that EU countries are most responsible for the largest portion of the international trade in frogs’ legs of wild species. Over decades of exploitation, the EU imports have contributed to a decline in wild frog populations in an increasing number of supplying countries, such as India and Bangladesh, as well as Indonesia, Turkey and Albania more recently. However, there have been no concerted attempts by the EU and present export countries to ensure sustainability of this trade. Further work is needed to validate species identities, secure data on wild frog populations, establish reasonable monitored harvest/export quotas and disease surveillance and ensure data integrity, quality and security standards for frog farms. Herein, we call upon those countries and their representative governments to assume responsibility for the sustainability of the trade. The EU should take immediate action to channel all imports through a single centralised database and list sensitive species in the Annexes of the EU Wildlife Trade Regulation. Further, listing in CITES (the Convention on International Trade in Endangered Species of Wild Fauna and Flora) can enforce international trade restrictions. More joint efforts are needed to improve regional monitoring schemes before the commercial trade causes irreversible extinctions of populations and species of frogs.
amphibians, biodiversity, CITES, disease, over-exploitation, sustainability, taxonomic status, wildlife trade
Three decades ago, initial signs of global declines in amphibian populations were reported (
The international trade of live amphibians infected with either Bd or Bsal has since been highlighted (e.g.
While the international amphibian pet trade includes a broader range of species with many frogs still coming from the wild (
Enforcement of laws, regulations and quotas or harvest limits is particularly challenging for the transport and trade of frogs’ legs. Many species are very similar in their morphology and as products are skinned, processed and frozen, gross mislabelling is likely and hard to verify (
Herein, we provide an overview on the EU’s central role as the primary ultimate destination for the global trade in frogs’ legs and its corresponding responsibility for resulting ecological risks and impacts. Furthermore, our review summarises knowledge on the current status of international trade in both live frogs and parts for human consumption. We primarily outline certainties (e.g. loss of biodiversity, destabilisation of ecological communities in their ecosystems, flawed farming operations, genetic pollution) against the manifold uncertainties underlying this trade (lack of documentation to assess sustainability of trade; species identification of individual frozen frogs, skinned frog bodies or parts thereof; and international regulation of species not listed in the appendices of CITES). Clear identification of these deficiencies should oblige policy-makers from responsible consuming countries to follow revised and newly-implemented legislation and, where appropriate, apply the precautionary principle as a crucial safeguard for the survival of many amphibian species. Understanding the dimensions of the frogs’ legs trade is challenging (since much of the global data is not available after 2009, as monitoring stopped), even when we had better data (Suppl. material
The EU as the major consuming region of frog’s legs in the period 2010-2019, with major supplying countries in SE-Asia (Indonesia, Vietnam) and eastern Europe (Turkey, Albania) and major importing countries (Belgium, France, Netherlands, Italy and Spain). Sources:
Apart from information retrieved from previous studies (
Taxonomy largely followed
A study was simultaneously conducted for a current snapshot/analysis of the French market (the EU’s major consuming nation of frogs’ legs). Data were retrieved from the French Customs statistics for the period 2010–21 (LeKiosque.finances.gouv.fr; accessed 16 April 2019 and 26 April 2022). Additionally, in December 2021, an online survey of the French market was carried out. Websites used for this included major supermarkets, frozen food brands, Asian food supermarkets (i.e. Auchan, Cora, Monoprix, Picard, Tang Frères etc.). Another market survey of e-mail alerts was conducted between 23November 2021 and 9 February 2022. The survey was conducted using Google Alert with the keywords “frog legs” in French and in singular and plural forms, asking to receive all new content regardless of the source (News, Blogs, Web). The commercial offers were sorted and analysed.
An advanced search on “The IUCN Red List” (conducted August 2022), based on the following filters; (a) Taxonomy > Amphibia, (b) Threats > Biological Resource use > Intentional use and (c) Use and Trade > Food (Human), was also completed. The resulting species were assigned to their native regions/countries and tabulated with information on current IUCN Red List status ([
CITES Appendix listings were checked with the species filtered in the IUCN Red List where international trade for consumption (food) was indicated. Those species were entered in the CITES trade database (https://trade.cites.org/, see Suppl. material
Once we had a list of species potentially traded for food, we were able to pair that list with the IUCN data mapping species distributions. First, we downloaded amphibian ranges from the IUCN website (https://www.iucnredlist.org/). We then uploaded these into ArcMap 10.8 and selected all species in trade using the “joins and relates” function, before extracting these species. Species ranges were then dissolved so that each species was represented by a single polygon (though this could be a multipart polygon). This was then split into groups of 30 species before overlaps were counted using the “count overlapping polygons” toolbox for each subset. This was purely for processing and all species were included in total. These were then all converted to a raster with a 10 km resolution and each stack was summed using the “mosaic to new raster” function to sum values and map the number of species being consumed in each geographic area.
In addition, we used “union” to combine species’ ranges with a map of the world (from thematic mapper), the species range country combinations dissolved to list each species once for each country it was in and the summary statistics tool was used to calculate the number of species being traded for consumption for each country. This table was then related to the original country map to show the number of species being traded for consumption per country. This was then repeated for just those species being traded internationally for consumption.
After describing current import volumes of frogs’ legs into the EU and the main supply regions, we highlight the species that make up the international frogs’ legs trade, describe national consumption trends and finally provide information on threats impacting species/populations, indicate amphibian population trends and broader ecological impacts of the frogs’ legs trade.
In the study period 2010 to 2019, total imports of frog’s legs into the EU numbered 40.7 million kg. This total weight can be converted, when 1 kg equals 20–50 individual frogs (
The EU’s role of responsibility should also imply sustainable harvest and trade of species in supplier countries. The following example makes it clear what abuses accompany this trade; (1) according to Indonesia’s annual harvest/export quotas for F. cancrivora (there is no information on how Indonesia derives its annual quotas, so there is no data basis for sustainable trade), in the period 2016–2020, ca. 295.3 million kg were exported (1 kg equates to 15–22 individual specimens [cf. with
Regarding the export of live animals, wholesalers have been found to have mortality rates of around 45% for amphibians, meaning live trade levels may need to be in higher volumes to satisfy demand when many frogs die in transit, with many coming from the wild (
In the study period 2010–19 (
Main EU importers/consumers and suppliers of frogs’ legs (in tonnes) for the period 2010-2019. Source:
Major EU importers | Major suppliers of frogs’ legs into the EU | ||
---|---|---|---|
Belgium | 28,429 | Indonesia | 30,019.4 |
France | 6794.4 | Vietnam | 8439.4 |
Netherlands | 2621.5 | Turkey | 1593.7 |
Italy | 1787.2 | Albania | 586.5 |
Spain | 923.4 |
Due to the introduction of advanced technologies of freezing methods in the 1970s, storage constraints were reduced and transport routes of frogs’ legs became possible. This transformed the traditional frogs’ leg trade in France, bringing some local frog populations to the brink of extinction (
From 2010–19, France imported 30,015 tonnes of fresh, refrigerated or frozen frogs’ legs (ca. 600–1500 million frogs;
Results of the online market survey in December 2021 indicate 20 frogs’ legs food products readily available. Of these 20 products, 11 originated from Indonesia, three from Vietnam, one from France and one from the “EEC (Turkey, Albania etc.)”. This last indication is confusing because the European Economic Community (EEC) was dissolved in 1993 excluding Turkey and Albania and both are not EU member States. With regard to the indication of France as a source country, these products are pre-cooked frogs’ legs that do not originate from France and the species indicated is “wild Limnonectes [Rana] macrodon” endemic to western Indonesia (cf. Table
Indonesian export quotas of species known to be consumed nationally and internationally; cons = consumption; indiv. = individuals; SVL = snout-vent length. Sources:
2015 | 2016 | 2017 | 2018 | 2019 | 2020 | 2021 | 2022 | |
---|---|---|---|---|---|---|---|---|
Fejervarya cancrivora | 2250 (pet) | 83,599,250 (cons.) [1kg = 22 indiv.] | 78,498,000 (cons.) [1kg = 22 indiv.] | 72,086,805 (cons.) [1kg = 15 indiv.] | 4,100,850 (cons.) [1kg = 15 indiv.] | 56,985,845 (cons.) [1kg = 15 indiv.] | 56,985,845 (cons.) [SVL ≥ 9 cm] | 56,985,845 (cons.) [SVL ≥ 9 cm] |
Fejervarya limnocharis | 12,150; (10,000 for cons.) | 3600 (pet) | 11,270 (pet) | 630 (pet) | 1080 (pet) | 1235 (pet) | 1235 (pet | 1235 (pet) |
Limnonectes kuhlii | 540 (pet) | 540 (pet) | 588 (pet) | 0 | 90 (pet) | 95 (pet) | 95 (pet) | 95 (pet) |
Limnonectes macrodon | 10,350; 10,000 (skin) | 10,350; 9000 (skin); 1350 (pet) | 0 | 0 | 0 | 0 | 0 | 0 |
For six sources, both product description and packaging do not indicate a species name. With regard to EU legislation, lack of information (species or country of origin) is a violation of EU rules [Commission Regulation (EC) No 2065/2001 of 22 October 2001 detailing rules for the application of Council Regulation (EC) No 104/2000 as regards informing consumers about fishery and aquaculture products; https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:32001R2065&from=FR). In eight sources, origin is highlighted as “wild”, three refer to “fishing” (e.g. fresh water, rice fields) and, in one, “collected” is indicated as the source. Not a single product, however, indicates a captive bred or farmed source. Besides raw or cooked frogs’ legs, “frairine” is also offered for sale, a mixture of pork and frogs’ legs seasoned with white wine. For this mixed product, there is no information on the origin or species involved.
An additional market survey through Google Alert for more than 10 weeks (see Methods) identified 38 commercial offers for frogs’ legs (20 from Belgium and 18 from France). Regarding the offers from France, trends from the December 2021 study are largely confirmed, with only one offer indicating an origin “Vietnam and/or Indonesia captive bred”.
In addition to imports, the French market is also supplied with wild-caught native species. Short marketing circuits, such as local restaurants, are supplied with Rana temporaria, a nationally protected species in France (https://www.legifrance.gouv.fr/loda/id/JORFTEXT000017876248/, accessed April 2022, see Suppl. material
There is no doubt that the trade in frogs’ legs for consumption is a global issue, with most countries involved in the trade as exporter, importer or some combination (
Anuran species imported for the purpose of consumption into the US in the period 2015-20, in which weight (left) is compared to the number of individuals (right) to illustrate how unequally these variables are aligned with each other. Source:
For most recent trade routes from source countries to importers and consumers into the EU, see Fig.
Within the study period 2010–19, Indonesia clearly represents the leading supplier for the European Union’s frogs’ legs with 30,019.4 tonnes (74%), followed by Vietnam (8439.4 tonnes; 21%), Turkey (1593.7 tonnes; 4%) and Albania (586.5 tonnes; 1%) (Table
Comparatively smaller amounts were supplied by China (37.7 tonnes), India (15 tonnes), Thailand (9.2 tonnes), Malaysia (7.6 tonnes) and South Korea (0.3 tonnes), resulting in less than 1% of the EU’s total imports (
Europe has been the major importer of frogs’ legs for many decades, with exports from Indonesia contributing to 83% of all European imports (
Species involved in the international food trade are mainly represented by members of the family Dicroglossidae (Fejervarya and Limnonectes) (
Anuran species in the European frogs’ legs trade where overexploitation and/or taxonomy is/are important limiting factor(s) for sustainable commercial trade. Distribution: Information here is based on IUCN Red List assessments and more recent literature. Country codes follow acronyms provided in the CITES Trade Database, https://trade.cites.org/cites_trade_guidelines/en-CITES_Trade_Database_Guide.pdf; “?” next to country denotes uncertainty; RLA: Red List Assessment and year when the species was most recently assessed, with ‘outdated’ used to designate RLAs > 10 years old; LC: Least Concern, DD: Data Deficient, NT: near threatened, VU: vulnerable; Pop. trend: population trend (↑: increasing; →: stable; ↓: decreasing; ?: unknown); CITES: listed in either appendices I-III or in the annexes of the European Union Wildlife Trade Regulations (EU-WTR) A-D; Information: *): Assessment involving uncertainty. Sources:
Species | Distribution | RLA (year) | Pop. Trend | CITES / EU WTR | Information on taxonomy, threat, trade, farming operations & exploitation levels |
---|---|---|---|---|---|
Fejervarya cancrivora Crab-eating grass frog | ID, MY, TL | LC (2020) last assessment of 2004! | ↓ | – | • assumed overharvest*(IUCN SSC Amphibian Specialist Group 2022a) |
• utilised locally, nationally and internationally | |||||
• export quota sharply increased in 2016 to more than 83 million animals for consumption and since then strong fluctuations. | |||||
• 2022 harvest/export quota Indonesia: | |||||
• 59,985,100 / 56,985,845 specimens | |||||
• Imported to the EU by millions as frogs’ legs | |||||
• taxonomy remains uncertain in some populations | |||||
Fejervarya limnocharis Common Asian grass frog | BD, BN, KH, CN, HK, IN, ID, JP, LA, MO, MY, MM, NP, PK, PH, SG, TW, TH, VN | LC (2004, outdated) | → | – | • harvested for human consumption, found in local and national trade ( |
• probably also in international trade | |||||
• 2021 harvest/export quota Indonesia: 1300 /1235 specimens for the pet trade, in 2015, also harvested for consumption (cf. Table |
|||||
• cryptic species complex | |||||
Fejervarya moodiei Northern crab-eating grass frog | BD, IN, MM, PH, TH, KH? | LC (2020) last assessment of 2004! | ? | – | • originally thought to be known only from the type locality Manila (Luzon Island, Philippines, with unclear taxonomic validity |
• identified by DNA barcoding in French frogs’ legs imports ( |
|||||
• locally consumed in the Philippines ( |
|||||
Hoplobatrachus rugulosus Asian rugose bullfrog | KH, CN, HK, LA, MM, TW, TH, VN | LC (2020) last assessment of 2004! | ↓ | – | • large individuals may be overharvested locally |
• wet rice agroecosystems appear to balance the impact of exploitation | |||||
• locally, nationally and internationally traded for food | |||||
• harvest of large numbers of wild individuals is ongoing, either directly to be marketed or to restock farms, for example, in Vietnam | |||||
• large numbers of frogs’ legs imported into the EU | |||||
• meat is considered a delicacy in restaurants in Vietnam ( |
|||||
Hoplobatrachus tigerinus Asian bullfrog | AF, BD, BT?, CN?, IN, MM, NP, PK | LC (2008, outdated) | → | II / B | • introduced to Madagascar |
• intense harvest before the 1990s has detrimentally impacted populations (India, Bangladesh) | |||||
• legal export banned in India and Bangladesh since the late1980s | |||||
• utilised locally, nationally, internationally (frogs’ legs industry) | |||||
• taxonomic confusion with H. rugulosus* | |||||
• species is farmed (e.g. in Vietnam or Thailand), occasionally hybridisation with H. rugulosus to increase production | |||||
Limnonectes blythii Blyth‘s giant frog | ID, LA?, MY, MM, SG, TH | LC (2021) last assessment of 2004! | ↓ | – | • major threat is consumption (locally / nationally / internationally) |
• population decline > regional overharvest | |||||
• taxonomic uncertainty > blythii complex*( |
|||||
• relatively large species, attractive for frogs’ legs trade | |||||
• in the 1980s, one of the dominating species in Indonesia’s exports to Europe ( |
|||||
Limnonectes ibanorum Rough-backed river frog | BN, ID (Kalimantan), MY (Sarawak) | LC (2018) | ↓ | – | • large body size make species attractive for food trade |
• probably utilised locally and possibly also for the international frogs’ legs trade* | |||||
• life history traits make this species vulnerable to overharvest | |||||
• declining populations indicate over-exploitation | |||||
Limnonectes ingeri Inger’s wart frog | BN?, ID (Kalimantan), MY (Sabah, Sarawak) | LC (2018) | ? | – | • large body size make species attractive for food trade |
• potentially exported for the frogs’ legs industry* | |||||
• locally consumed in Kalimantan and Sarawak | |||||
• life history traits make this species vulnerable to overharvest | |||||
Limnonectes kuhlii Kuhl‘s broad-headed frog | ID | LC (2020) last assessment of 2004! | ↓ | – | • cryptic taxon, species complex* |
• presence in several range States remains uncertain (see |
|||||
• in some of these potential range States, populations are locally overexploited for consumption, for example, China | |||||
• the meat is highly priced in Vietnam ( |
|||||
• look-alike species of L. macrodon, included in EU imports ( |
|||||
Limnonectes leporinus Giant river frog | BN, ID (Kalimantan), MY (Sabah, Sarawak) | LC (2018) | ↓ | – | • potentially exported for the frogs’ legs industry* |
• regionally > overharvest of large individuals > suggesting demographic change | |||||
Limnonectes macrodon Giant Javan frog | ID (Sumatra, Java) | LC (2017) | ↓ | D | • locally, nationally exploited as food; Javan populations are exploited for the international market |
• has been heavily harvested for the frogs’ legs trade ( |
|||||
• according to |
|||||
Limnonectes malesianus Malesian river frog | ID, MY, SG, TH | LC (2021) last assessment of 2004! | ↓ | – | • significant decline initially reported in 2004 |
• overharvest is considered a major threat | |||||
• collected for subsistence use and trade & utilised locally, nationally | |||||
• sympatric occurrence with the larger Limnonectes blythii that is favourably collected; however, harvest impact is not well understood due to a lack of harvest/trade data ( |
|||||
• look-alike species of L. macrodon, included in EU imports ( |
|||||
Lithobates catesbeianus American bullfrog | CA, US | LC (2020) | ↑ | – | • introduced in many other countries across the globe ( |
• commercially farmed for food (in non-range countries, for example, in Thailand, Vietnam and Brazil) | |||||
• considered a pest & invasive species, for example, in large parts of Europe, Central and South America, East and Southeast Asia | |||||
• considered a vector of pathogens* ( |
|||||
Lithobates pipiens Northern leopard frog | CA, US, PA, MX? | LC (2021) last assessment of 2004! | ↓ | – | • taxonomy unresolved; species complex |
• previously commercial overexploitation was considered a major threat ( |
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• information on international trade is vague, other than trade for research/educational purposes ( |
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Pelophylax bedriagae Bedriaga‘s marsh frog | CY, EG, GR; IL; JO; LB, SY, TR | LC (2021) last assessment of 2008! | → | – | • harvest/exports for food from Turkey to western Europe > considered a significant threat |
• large numbers are exported from Turkey ( |
|||||
• high extinction risk in Turkey until 2032 if exploitation level continues ( |
|||||
• utilised local and internationally for consumption) ( |
|||||
Pelophylax caralitanus Beyşehir frog | TR | NT (2008, outdated) | ↓ | – | • largest edible frog in Turkey; commercially overexploited for the frogs’ legs trade in France, Italy and Switzerland ( |
• high extinction risk until 2032 ( |
|||||
Pelophylax epeiroticus Epirus water frog | AL, GR | NT (2019) | ↓ | – | • locally, nationally utilised for food |
• intensively utilised in Albania for consumption, at present no evidence for excessive collections in Albania | |||||
• Bd-infected populations in Albania | |||||
• Potential hybridisation with the sympatric P. ridibundus | |||||
Pelophylax kurtmuelleri Balkan frog | AL, BG, GR | LC (2019) last assessment of 2008! | ↓ | – | • nationally and internationally utilised for consumption |
• in northern parts of its native range > significantly threatened through commercial overexploitation for consumption ( |
|||||
• another threat is considered in the unintentional introduction of commercially traded non-native water frogs | |||||
Pelophylax ridibundus Eurasian marsh frog | Western Europe across the Arabian Peninsula, Central Asia to Russia | LC (2008, outdated) | ↑ | – | • harvested for educational and medical research and food |
• populations extensively collected for food in Turkey (~ 1,000 t/yr) ( |
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• trade for frogs’ legs may detrimentally impact populations in Turkey* ( |
|||||
• frogs’ legs trade has led to declines in populations in eastern Asia, former Yugoslavia and possibly in Romania* | |||||
• Rana ( Pelophylax) kl. esculenta considered a synonym | |||||
Pelophylax shqipericus Albanian water frog | AL, ME, | VU (2019) | ↓ | D | • introduced to Italy and Croatia |
• nationally and internationally utilised for consumption | |||||
• no management plan in Albania; significantly threatened by overexploitation | |||||
• potentially threatened by unintentional introduction of commercially traded non-native water frogs |
Export quotas within Indonesia list species, but on reaching the EU, species level information is not recorded (see Table
Annually, Indonesian authorities publish harvest and export quotas of CITES and non-CITES species native to the Indonesia (but possibly not the actual export values). For species listed in Table
Amongst quotas established for edible frog species, trade for the purpose of “consumption” is indicated for both Fejervarya cancrivora and F. limnocharis. However, only in 2015, for F. limnocharis, a specific number of individuals was designated for consumption (Table
In 1982, commercial frog farming was established in Indonesia only involving non-native species (
Indonesia and Vietnam represented the largest exporters of frogs’ legs in the period 2003–2007 (
It is challenging to determine sources of current frogs’ legs from Vietnam, whether they are farmed or wild-caught. According to
According to
The many risks associated in frog farming in southern Vietnam, Tien Giang Province and Ho Chi Minh City, have been highlighted by
India, formerly considered the country with the largest frogs’ legs exports (
In response to the export ban of frogs’ legs for the international market imposed in 1987, initial establishment of frog farms was reported one year later. At that time, the frogs’ legs trade was organised under the Seafood Exporters Association, who proposed that the Indian government set up frog breeding centres (
However, it seems that a nationwide establishment of commercially operating frog farms is still in its infancy in India, compared to some SE-Asian countries. In a more recently published study, possibilities for establishment of commercial frog farming in Goa were explored, based on the known issues of the frog trade (e.g. wild harvest); thus, to commercially produce frogs would in turn “minimise illegal poaching” (see
In 2017, Turkey exported 547 tonnes of frogs for the food trade (
According to
Between 2010 and 2019, Albania’s share of the EU market was 1% (= 590 tonnes) and, according to
To the best of our knowledge and research, we were unable to uncover any evidence of established farms for the commercial breeding of Pelophylax spp. for export and little documentation exists of export levels. In 1996, a French businessman invested in a frog farm, motivated in part by the fact that in the mid-1990s frogs’ legs in France became rare (cf. above). Mainly due to a socio-economic and political crisis, this farming project failed (https://www.discover-cee.com/roadtrip-cee-albania-how-a-french-guy-discovered-tirana-as-best-place-to-start-his-fintech/, accessed May 2022, see Suppl. material
Import data for the period 2010–19 were compared with data of the previous decade (see
Forensic studies have shown that the species composition and labelling in Indonesia’s trade has changed over recent decades (
While this study focuses on the EU, the current role of the United States is briefly highlighted, as the US also represents a major consumer of frogs’ legs (cf.
As can be seen in the individual IUCN Red List assessments on exploited amphibian species (Suppl. materials
The conservation of species in trade only makes sense if the species or species complexes are known. The trade in animals with unclear taxonomic status ignores a fundamental condition, namely the lack of any data basis for taxa to, for example, conduct a non-detriment finding for the species to evaluate threat (see below). In order to obtain an overview of the species involved in the food trade (whether at local, national or international level) and their respective origins, the IUCN Red List was filtered (Fig.
Number of species per country in trade for consumption, see Suppl. material
At least 187 species of anurans and salamanders/newts are collected locally/nationally for food and for the international frogs’ legs industry (Suppl. material
Amongst the 30 species compiled in Table
When we submitted the first version of this work in August 2022, several Red List assessments for these species were outdated with 16 species last assessed ≥ 15 years ago, i.e. 11 species assessed in 2004 and five species assessed in 2008, while in 2022/23, several of those species had been re-assessed, leaving six species with outdated assessments (see Table
Current Red List assessments of aforementioned 30 amphibian species, now refer to 24 that have been evaluated “Least Concern”, three “Near Threatened (NT)”, one “Vulnerable (VU)”, one “Endangered (EN)” and one “Critically Endangered (CR) (Table
Population trends of the 30 species indicate 20 species “decreasing”, five species “stable”, two species “increasing” and three species with an “unknown” population trend; it is worth mentioning here in addition that 14 species assessed “Least Concern” have a decreasing population trend (Table
Notable is the fact, that the two large-legged species, i.e. Limnonectes blythii and L. malesianus had been assessed “Near Threatened” in 2004 with decreasing populations in both species (
Outdated assessments are further exacerbated by the fact that the species are regionally overharvested for consumption as well as being involved in the international trade at uncertain levels. However, of all 30 species known to be consumed, 16 species have special mention of harvest that might influence their conservation status. Of these, 13 species (Leptodactylus fallax, Limnonectes blythii, L. kuhlii, L. leporinus, L. macrodon, L. malesianus, Lithobates pipiens, Pelophylax caralitanus, P. kurtmuelleri, P. ridibundus, P. shqipericus, Rana amurensis and R. chensinensis), have either “regional overexploitation-collection” or “harvest leading to declines” explicitly stated in their IUCN Red List assessments. Another three species (Fejervarya cancrivora, Hoplobatrachus rugulosus, Limnonectes microtympanum), have these same parameters as ‘presumed’ within their Red List assessments (Table
Of the 187 species filtered from the IUCN Red List that are collected for either local, national or international consumption (Suppl. material
Red List status of 187 amphibian species globally utilised for consumption that have been assessed in eleven assessment periods between 2004 and 2021. Source:
Population trends assessed in 187 amphibian species, consumed for food, in eleven assessment periods between 2004-2021 (cf. Suppl. material
It is noteworthy to mention that 57 species of the respective 187 species, have a decreasing population trend, but categorised as “Least Concern” (see Suppl. material
Assessments of 28 species were re-evaluated in 2022/23, in seven species, the Red List status was changed (see Suppl. material
The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) currently lists 220 amphibian species in their appendices, equating to ca. 2.6% of all amphibian species (8,386 spp.;
All seven CITES listed anuran species are utilised on a local/national scale and three (i.e. Pelophylax shqipericus, Limnonectes macrodon and Hoplobatrachus tigerinus), are involved in the international frogs’ legs trade (cf. Table
Seven anuran species listed on the appendices of CITES (I-III) and annexes of the European Wildlife Trade Regulations (A-D) that are currently known to be consumed locally/nationally and those utilised within the international frogs’ legs industry. Country codes follow acronyms provided in the CITES Trade Database (https://trade.cites.org/cites_trade_guidelines/en-CITES_Trade_Database_Guide.pdf); RLA: Red List Assessment and year, when the species was assessed, LC: Least Concern, VU: vulnerable, EN: endangered, CR: critically endangered; Pop. trend: population trend (→: stable; ↓: decreasing). CITES: listed in either the appendices I-III or in the annexes of the European Union Wildlife Trade Regulations (EU-WTR) A-D; Sources:
Species | Distribution | RLA(year) | Pop. Trend | CITES &EU-WTR (year when listed) | Consumption & Trade |
---|---|---|---|---|---|
Calyptocephalella gayi Helmeted water toad | CL | VU (2018) | ↓ | III (2011) C (2012) | National, international (likely only pet trade) |
Conraua goliath Goliath frog | CM, GQ, GA? | EN (2018) | ↓ | B (1997) | National |
Euphlyctis hexadactylus Indian green frog | BD, IN, NP?, LK | LC (2004, outdated) | → | II (1985) B (1997) | National |
Hoplobatrachus tigerinus Asian bull frog | AF, BD, BT?, CN?, IN,MM, NP, PK | LC (2008) | → | II (1985) B (1997) | National, international |
Limnonectes macrodon Giant Javan frog | ID(Sumatra, Java) | LC (2017) | ↓ | D (2009) | National, international |
Pelophylax shqipericus Albanian water frog | AL, ME | VU (2019) | ↓ | D (2009) | National, international |
Telmatobius culeus Titicaca water frog | BO, PE | EN (2019) | ↓ | I (2017) A (2017) | National, international |
Four species are listed in CITES App. II and one in CITES App. III that are consumed either locally/nationally and/or internationally traded for consumption, while another four species are only listed in the annexes of the EU-WTR (Table
The farming and regional/international trade activities involving amphibian species for consumption purposes is associated with numerous risks. Here, we outline these more specifically.
Evidence clearly demonstrates that the commercial trade of amphibians infected with pathogens contributes to the spread of diseases within and between countries, on a global scale and involves species traded for food (
The intercontinental spread of two fungal pathogens i.e. Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal), has led to the decline of more than 500 amphibian species and currently more than 1000 species are known to be infected by one of these two emergent infectious diseases (
Interactions between ecological factors and amphibian-pathogen dynamics are extremely complex and pose major challenges for management decisions (
Exports of Pelophylax [Rana] esculentus from Albania for consumption to foreign markets also revealed Salmonella, Vibrio cholerae, Listeria spp. and Aeromonas spp., the latter two being clearly more common (
One internationally commercialised species for consumption is particularly striking: the North American bullfrog (Lithobates catesbeianus), a known vector of ranavirus detected in cultured specimens in South American exports to the USA (
Two more species involved in the food trade (see Table
Challenges with regard to the spread of diseases with live animals intended for the food trade are multi-layered. On one hand, trade of live amphibians poses a potential risk of cross-infection into naïve wild populations via escape and contamination through waste water disposal. On the other hand, commercial breeding farms also pose risks of escaped animals and disposal of water and housing materials that can be carriers of pathogenic diseases. This demonstrates two predominant pathways for spreading pathogenic diseases: translocation and commercial farming operations (cf.
We cannot provide comprehensive information on residues and effects (on the end consumer) of toxins used in regional agriculture and ingested indirectly (via the nutrient cycle) by frog species. Nor are we able to tease apart the effects of ingestion of veterinary cocktails of commonly-used antibiotics, i.e. oxytetracycline and doxycycline (see
Here, we address the questions: (1) What are the most common habitat types and species that are captured for the international consumption trade? (2) How are these habitats managed with regard to the use of pesticides, herbicides and other agricultural chemicals? (3) Do these agrochemicals negatively affect faunal assemblages and their ecosystems? (4) Are these chemicals detectable in imported frogs’ legs? (5) Have veterinary drug residues been detected in aqua-cultured frogs’ legs? and finally, (6) Is there evidence that the consumption of frogs’ legs contaminated with medicinal or pesticide residues can be hazardous to human health?
Probably the most common frog involved in the global frogs’ legs industry is Indonesian F. cancrivora (75% of reported species). This species is considered the most abundant frog species inhabiting rice fields in Indonesia (see
It appears that Javan populations of F. cancrivora are predominantly harvested for the international frogs’ legs trade (cf.
The question now arises whether pesticide residues or other toxins have been detected in traded animals or parts thereof for commercial consumption by humans. Information on the potential of bioaccumulation has rarely been analysed and more work is needed (
The question of whether pesticide residues and other potentially toxic substances in frogs that are imported into the EU have been monitored could not be determined in the course of this work. This in itself is shocking and in view of the situation in exporting countries and the lack of transparency and management in the application of agrochemicals and veterinary medicinal substances within commercial farms, we strongly recommend that this monitoring become an urgent near-future task for importing countries.
In 2010, Holsbeek and Jooris reported that, in the preceding decade, humans translocated individuals of Pelophylax spp. either unintentionally (for example, escaped animals from nurseries and markets) or intentionally (for example, for stocking garden ponds and for local culinary harvest) almost everywhere they exist. A study conducted by
Another example that does not explicitly address commercial trade of frogs’ legs in the EU, but names taxa that are traded regionally for this purpose (see also Table
Furthermore, the commercial frogs’ legs industry already contributes to the unintentional release of specimens into naïve habitats and displacing native species (e.g.,
The use and trade of species in their country of origin and whose taxonomic status is uncertain affects at least four species involved in the international frogs’ legs industry as well. Amongst these, three are designated as species complexes (i.e. more than one species under one current scientific name) and species with unresolved taxonomy in IUCN Red List assessments. They are: Fejervarya cancrivora, Hoplobatrachus tigerinus and Limnonectes blythii. There are many other species complexes, wherein the taxonomy is extremely complex and uncertainties are even more fraught with problems. Fejervarya moodiei was described from “Manila”, Luzon Island Philippines and, hence, taxonomic studies should initially be conducted on that population. In another two species (Limnonectes grunniens and L. kuhlii), where the impact of international trade for frogs’ legs has not been explicitly ascertained within their assessments (but is very high), taxonomy remains unresolved. In these species of Limnonectes, both their geographic range and number of cryptic species ‘hiding’ under one scientific name are still unclear (
Of the three “species” that clearly represent complexes of many different species, we highlight what is known here, but reiterate that the dearth of data is staggering, considering that these are the most economically valuable species in terms of the known trade in commercial frogs’ legs.
Fejervarya cancrivora. – An initial molecular analysis, six years after F. cancrivora was evaluated in the IUCN Red List (IUCN SSC Amphibian Specialist Group 2022a), revealed three geographically distinct clades/subclades: one confined to Bangladesh, Thailand and the Philippines; another representing Malaysia and Indonesia (Greater Sundas); and the remaining one from Sulawesi (incl. one population in southern West Java, as a result of human introduction) (
Clear taxonomy is the foundation of efficient and sustainable species conservation and so is the naming of the species or parts thereof that are to be traded. Examination of 209 frozen frogs’ legs sold in supermarkets in France listed exclusively as Limnonectes [Rana] macrodon (based on product labelling), revealed that almost all (206 of the 209 or 98.6%) were in fact legs of F. cancrivora and only 2 (0.96%) could be attributed to L. macrodon, while one sample was revealed to be F. moodiei (
Hoplobatrachus tigerinus. – In their Red List assessment,
Limnonectes kuhlii. – The taxonomic status of L. kuhlii associated with the species’ currently known distribution range has been described as particularly uncertain within the Red List assessment (
Sixteen of the 30 anuran species listed in Table
Prior to export for international trade, a considerable number of live animals die on arrival to the processing facilities. For Indian exports, this loss has been estimated at 10–20%, in Indonesia it is 40–50% because quality is not sufficient for export and some frogs are killed prior to being exported (
Initial reports on the sustainability of this trade were published more than 20 years ago; however, large-scale ecological studies to assess offtake rates and their sustainability appear severely lacking. Here, we highlight studies that indicate amphibian declines associated with harvest for the food trade both regionally and internationally. Historically, overharvest was detected in Californian populations of Rana aurora draytonii (
In 2005, Kusrini noted that current harvest levels of Fejervarya cancrivora and members of the F. limnocharis-iskandari complex (F. iskandari was separated from the F. limnocharis complex through allozyme data;
The majority of frog hunters in East Java reported that the number of harvested frogs has decreased and this was also perceived by middlemen (in West and East Java) and exporters, who argued that, depending on the season, supplies were sometimes scarce (
Several regional field studies have been conducted in Indonesia to assess population densities of frog species involved in the food trade, and these clearly show these synergistic effects. In a 20 × 20 m paddy field in West Kalimantan, the density of F. cancrivora was measured at 1.01 individuals/m2 (
Limnonectes macrodon is also regionally impacted and preferred for their better taste (compared to F. cancrivora;
Overharvest of frog populations in Turkey (intended for export to France, Italy, Greece, Spain, Switzerland and Lebanon) has been reported by
A very recent study, by Çiçek and others in 2021, on the sustainability of Anatolian water frogs, is by far one of the most comprehensive studies to analyse commercial trade in frogs’ legs for the EU market. In 2013–2015, > 13,000 Pelophylax spp. (cf. Red List assessments of Pelophylax bedriagae, P. caralitanus and P. ridibundus) from two regions were tagged for population and density estimation. A population viability analyses was conducted over a 50-year period, based on catch and export data from Turkey. If this trade were to continue at the same harvest rate, extinction risk would be 90% in 50 years, affecting two to five species of the Pelophylax species complex (
During the course of this study, it became clear just how difficult it is to obtain concrete data on the current international trade in frogs’ legs. Specifically, relevant data are scattered across different unconnected databases (for example, national databases, FAO, EUROSTAT or information/services that can only be obtained/provided via payment, for example, Infofish International (http://infofish.org/v3/, Suppl. material
Our findings highlight the central role of the European Union as the main importer of frogs’ legs derived from wild individual anuran populations, the urgent need for stricter trade regulations, better monitoring and data integrity to prevent further declines of wild frog populations and to help create a more sustainable commercial trade.
The high uncertainty of the assumed number of individual frogs within total imports throughout the study period impressively illustrates the opacity of the trade. Actual harvest numbers imported into the EU for annual consumption remain unknown and very difficult to quantify. This is undoubtedly due to the fact that they are non-CITES species and, thus, international trade data (species/volumes) remain undocumented. Listing species in the appendices of CITES is justified when international trade poses a severe threat to the conservation status of a species. The scientific authority of a CITES member state must review the harvest/export for Appendix II in terms of compatible offtake numbers/quotas in order to maintain the species’ ecological function in its native habitat (https://cites.org/eng/disc/text.php#IV, accessed May 2022, see Suppl. material
Anurans involved in the international frogs’ legs trade are all r-strategists, which means that they have large numbers of offspring, a rapid developmental rate and a high reproductive output. This also makes these species more amenable to regular (monitored) harvest while remaining viable. However, r-strategists also define themselves in having highly variable population sizes over time and mortalities may be density-independent or even catastrophic (
These considerations may, however, be too complex to be actively explored within the framework of the EU. We highlighted that there are many internationally traded species/species groups with sales in the EU where unsustainable trade has been detected (cf.
However, in the context of amphibians that are, for example, imported live into the EU for the exotic pet trade industry, amongst which many are traded that are also known to be infected with Bd/Bsal, (see
Required data for the IUCN Red List are crucial for assessing the conservation status of species. In Red List assessments, trade in a species can either: (1) be mentioned at the national/ international level, (2) go unmentioned (despite the fact that trade occurs) or (3) if mentioned, in some cases be designated as an acute threat to a species/population. In such cases, it is particularly problematic when Red List assessments are up to 19 years old (Table
Several Pelophylax, Limnonectes and Fejervarya spp. are morphologically very difficult to distinguish and many taxa are taxonomically treated as cryptic species complexes (see
Sustainable international trade can only be ensured if the use and movement of species within national borders is managed in such a way that species or populations maintain their viability and do not show shifts in physical traits due to bias in selection of key traits (cf.
In this context, governments are called upon to use resources in an adaptive and sustainable manner. Furthermore, EU commitments to Environmental Impact Assessments (EIAs) of imported wildlife mean that the EU is obligated to monitor what is in trade as well as the impact it is likely to have on source populations. As soon as the species triggers international demand and sales, importing countries are equally held accountable to take responsibility, whereby relevant stakeholders must ensure that their consumption of exotic species does not lead to population declines. Clearly, this will entail other anthropogenically induced threats affecting these species/populations (e.g.
Numerous examples of overexploited species assessed in the IUCN Red List assessments are detailed (see Table
According to
A two-year field study in the Philippines compared prey items of the native Luzon wartfrog (Fejervarya vittigera) with that of the introduced cane toad (Rhinella marina) to determine the proportion of rice pests in their diets and which of the two species was more efficient feeding on rice pests. It turned out that the proportion of pests eaten by F. vittigera was significantly larger than that of R. marina, which mainly preyed on beneficial arthropods in the rice-ecosystems. The authors conclude that adult F. vittigera may provide effective pest control services and suggest protecting and promoting F. vittigera populations (as opposed to reducing R. marina populations) to minimise the use of insecticides (
Due to problems of sustainability caused by the removal of species from their ecosystems (see Table
Globally, Lithobates catesbeianus is the most widespread species involved in farming operations and has been introduced for the purpose of commercial farming into more than 40 countries (
In other parts of the world, initiatives to commercialise frog farming are also being publicised as a result of increased demand. For example, under EU funding, the CaPFish Capture and Aquaculture programmes were launched to promote aquaculture in 10 provinces of Cambodia, primarily to promote food security in line with national government plans for fisheries development. Specifically, the Minister of Agriculture, Forestry and Fisheries, “Veng Sakhon”, encouraged farmers to raise frogs due to an increased market demand (https://en.khmerpostasia.com/2020/10/16/frog-farming-encouraged-as-market-demand-rising/, accessed, June 2022, see Suppl. material
Likewise, in Thailand, establishment of commercial frog breeding facilities has been described and limited for national consumption (
A major problem underlying establishment of commercial frog farming facilities is that there are no international standards or hygiene guidelines (see
An additional complicating factor for international control is that species harvested for frogs’ legs are exclusively non-CITES species, implying that there is no documentation across international borders.
The complexity of issues underlying the frogs’ legs trade is not a priority policy item for the EU, despite several important issues reviewed herein. This neglect strongly suggests that the EU, as the main consumer of wild-harvested frogs’ legs, has deliberately shirked responsibility in addressing the many issues facing the frog’s legs trade. The important precondition for such trade must be that consumers in the EU can have a guarantee that their actions will not contribute to the decline of species they consume or cause the spread of pathogens to native species. However, to achieve this goal, all stakeholders have to work together to remove existing loopholes and implement new regulations to control the trade in the foreseeable future. Full transparency of current supply chains, including information on sourced populations or commercial breeding farms, is also critically needed. Otherwise, we suggest temporarily suspending trade in certain species until such data are available and assurances made by all stakeholders. These measures result from the uncertainties highlighted here and are to ensure maintenance of viable populations in the countries of origin. Accompanying these should be awareness campaigns and education to help foster information for consumers to help them make decisions. The role of the EU should, therefore, be guided by the problematic conditions of this trade (unclear taxonomy, unsustainable offtakes, no disease control/biosecurity measures, re-introduction of exotic and invasive species and lack of a centrally established checkpoint for imports into the EU) in order to develop a more responsible and sustainable framework of the frogs’ legs trade. The only measure the EU has in place for non-CITES species at present is TRACES and it generally fails to list species. In addition, the World Trade Organisation (WTO) does not require amphibian species to be clearly listed in trade, which makes monitoring of international trade activities almost impossible.
One fact, in particular, became clear in this review: the lack of knowledge about species conservation and factors to promote implementation of sustainable harvest. The establishment of strictly supervised commercial farming according to industry-set protocols and hygiene measures (especially in the main supplier countries) and the difficulty in implementing these, is ignored by the EU. On both sides of the trade, short-term economic benefit is more important than long-term sustainability of the trade itself. Unsustainable trade prevents continued harvest and, therefore, long-term economic viability and ultimately ecological costs will also mount unrealised until severe non-linear results accrue (for example, crop failure due to pest outbreaks because predators have gone, as in India in the 1970s). This observation is particularly sobering because the international trade in frogs’ legs has been ongoing for decades (
It is irrefutable that the international frogs’ legs trade into the EU is riddled with uncertainties (no biosecurity measures, species identity is opaque, reported source is absent or doubtful etc.). The EU, as the main consumer of frog’s legs, does not assume any obligation to responsibly solve problems listed in this review, but herein is challenged to address the problems identified. We can only presume that many departments and agencies within the EU are aware of the extreme complexity of this trade with its diffuse network and various databases, but clearly put economics before the conservation of natural resources or the long-term benefits and livelihoods of people involved in the trade internationally.
Gratwicke et al. stated in 2010 that additional CITES listings could help reduce negative impact of international commercial trade. As stated earlier, IUCN Red List assessments of several trade-relevant anurans highlight the need for improved monitoring and creating a more regulated trade. Intensively traded species should also be re-evaluated for IUCN Red List status at more frequent time intervals in order to add up-to-date information on the conservation status of vulnerable species. More specifically, we propose that the IUCN SSC Amphibian Specialist Group designate a new working group that monitors and evaluates the conservation/threat status of particularly intensively harvested/traded species involved in the frogs’ legs trade at regular annual intervals. This information is critical to be implemented into CITES for timely decisions.
The increasing incidence of infectious diseases (both within a species as well as zoonotic spill-overs) via the wildlife trade correlates closely with the loss of biodiversity in source countries and is considered a worrying environmental problem that must be counteracted as a matter of urgency (see
Modern innovative scientific methods are required to ensure a fully transparent, legal, traceable and sustainable trade. We will need to implement scientific methodologies to distinguish farmed vs. wild individuals (cf.
To prevent the spread of infectious diseases, biosecurity measures need to be established at distinct points along the trade chain. Interestingly, such measures were already proposed at the 37th Standing Committee of the Convention on the Conservation of European Wildlife and Natural Habitats, in December 2017 (https://rm.coe.int/recommendation-on-biosafety-measures-for-the-prevention-of-the-spread-/168075a4b0, accessed May 2022, see Suppl. material
Results outlined in this review provide strong clear recommendations for both source and consuming countries. Promptly counteracting abuses in the international trade of frogs’ legs by adapting existing legislation and applying the precautionary principle to prevent irreversible damage to populations or species will help to promote the sustainability of the trade in the long-term. Recommendations for source and consuming countries are listed separately below.
Consumer countries have the obligation to take appropriate responsibility for the consumption of a resource. Accordingly, it would be obligatory to transparently inform relevant societies on which information basis trade is permitted.
We wish to thank Chris Shepherd and Jordi Janssen for providing data and Andrea Höppner for her technical assistance in visualising trade routes. Special thanks also go to the reviewers, who were able to improve the manuscript with a great deal of patience and meticulousness. We also have a number of anonymous people we want to thank for being responsible for data sources of data from private companies to countries and their respective agencies involved in the trade. This review was financially supported by the German foundation “Stiftung Zukunft Jetzt!” The publication of this article was funded by the Open Access Fund of the Leibniz Association.
Three world map distribution images and 2 world trade graphs
Data type: docx file
Explanation note: Export and import data of frogs’ legs by country/regions from 1996–2009. Source:
Anuran species assessed in the IUCN Red List with uncertainties mainly prevailing in national/international trade routes, and level of exploitation
Data type: docx file
Online sources and those useful with explanatory information
Data type: docx file
Explanation note: Useful data sources available online (URLs), with data type(s), and management authority for data and websites. Other relevant information accessible online referred to in the main text.
Amphibian species assessed in the IUCN Red List that are utilized either doemticalyy/nationally and or internationally
Data type: excel file