Research Article |
Corresponding author: Thomas Ziegler ( ziegler@koelnerzoo.de ) Academic editor: Klaus Henle
© 2019 Hai Ngoc Ngo, Truong Quang Nguyen, Tien Quang Phan, Mona van Schingen, Thomas Ziegler.
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:
Ngo HN, Nguyen TQ, Phan TQ, van Schingen M, Ziegler T (2019) A case study on trade in threatened Tiger Geckos (Goniurosaurus) in Vietnam including updated information on the abundance of the Endangered G. catbaensis. Nature Conservation 33: 1-19. https://doi.org/10.3897/natureconservation.32.33590
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Tiger geckos of the genus Goniurosaurus are considered as a susceptible reptile group, due to their restricted distribution ranges, specialisation to specific microhabitats and generally low population densities. While still new species have been discovered recently, Goniurosaurus species are threatened by extinction through habitat loss and collection for the pet trade. Of the 19 described species, for only eight species, the conservation status has been assessed within the IUCN Red List between 2016 and 2018 and all have been classified in the threat categories VU (Vulnerable), EN (Endangered) and CR (Critically Endangered). Goniurosaurus spp. are popular in the international pet market at least since the 1990s and several species experienced local extirpations as a consequence of massive over-collection in the past. However, tiger geckos have not been paid much attention for conservation, amongst others, due to the lack of comprehensive knowledge on their conservation status and biology. This study provides an overview of international trade in Goniurosaurus based on available data from 1999 to 2018 in the U.S. as well as data from online surveys and interviews in Europe and Vietnam, with the main focus on species native to Vietnam. All five tiger gecko species known from Vietnam were found in the local trade as wild captures for the national and international market and / or in the U.S. and Europe for relatively higher prices. We found that entire trade chains are very long (including several transfers and dealers involved) and that keeping and transport happen under poor conditions. We herein provide updated information on the abundance of the Endangered Cat Ba Tiger Gecko, which was recently shown to not only occur at its type locality, Cat Ba Island, Hai Phong City, North Vietnam, but also to inhabit small offshore islands in the Ha Long Bay, Quang Ninh Province. While the wild effective population was found to be relatively stable on four islands in Ha Long Bay, consisting of about 124 and 129 individuals in July 2017 and April 2018, respectively, the abundance of other sub-populations, impacted by anthropogenic pressures were found to be very low (2–10 individuals). Based on our findings, we propose stringent conservation measures to more efficiently protect wild tiger gecko populations, such as the inclusion in the Governmental Decree in Vietnam, the assessment of remaining species in the IUCN Red List of Threatened Species and the inclusion in the Appendices of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES).
Pet markets, Vietnam, abundance, anthropogenic pressures, conservation
Tiger geckos of the genus Goniurosaurus currently comprise 19 species with a disjunct distribution in Southeast Asia and East Asia (
Tiger geckos have been recorded in the international pet market at least since the 1990s (
The insular Cat Ba Tiger Gecko (Goniurosaurus catbaensis) was originally discovered on Cat Ba Island in Hai Phong City, north-eastern Vietnam (
Recently,
To obtain an overview on the availability and evidence for trade in Goniurosaurus spp. in Vietnam, we surveyed several pet markets in both southern and northern Vietnam (including Hai Phong City, Quang Ninh Province, Ha Noi City, Ho Chi Minh City and Dong Nai Province) in March 2018, based on public information on the internet. Five local dealers were questioned in order to determine the origin, availability, demand, price and use of traded species. To investigate the reptile market in the European Union (EU) for the availability of Goniurosaurus spp., we further screened online markets (online shops, internet platforms and forums, Facebook) and visited the largest reptile fair “Terraristika” in Hamm, Germany in March and June 2018. Names of interviewees were kept anonymous to ensure data privacy rights.
Furthermore, we analysed import volumes of Goniurosaurus spp. into the United States (U.S.). Data were obtained from the LEMIS database of the U.S. Fish & Wildlife Service, which included all recorded imports of Goniurosaurus spp. into the U.S. from 1999 to 2018. The purpose of trade in Goniurosaurus was categorised as (B) “breeding in captivity or artificial propagation”, (H) “hunting trophies”, (P) “personal”, (S) “scientific”, (T) “commercial” and (Z) “zoo”. The source of specimens was differentiated between wild (W), captive bred (C), captive born (F) and ranched (R), animals following the CITES definition in Res. Conf. 12.3 (Rev. Cop17).
Field surveys were conducted in Ha Long Bay in July 2017 and April 2018 during the non-hibernation season of Goniurosaurus catbaensis (
Study sites (Transect) | Transect Length (m) | Area of survey sites (m2) | Elevation a.s.l. (m) | Habitat types |
---|---|---|---|---|
Island 1 (T-1) | 380 | 5 000 | 4–99 | Shrub vegetation on limestone karst |
Island 2 (T-2) | 300 | 2 180 | 5–20 | Shrub vegetation on limestone karst |
Island 3 (T-3) | 200 | 1 180 | 10–72 | Shrub vegetation on limestone karst |
Island 4 (T-4) | 410 | 5 560 | 14–67 | Shrub vegetation on limestone karst |
Total | 1290 | 13 920 | 4–99 | Shrub vegetation on limestone karst |
To estimate population, a “mark-recapture method” was applied. In case of one-time mark and recapture event at two sites (T1, T3), the “Lincoln-Peterson Index” and, in the case of several recapture events at two remaining sites (T2, T4) (e.g.
To assess the population structure of G. catbaensis, lizards were categorised into three age classes, based on the snout-vent length (juvenile with SVL < 85 mm, sub-adult with 85 mm ≤ SVL < 105 mm and adult with SVL ≥ 105 mm) (
Potential threats to G. catbaensis were investigated in Ha Long Bay and Cat Ba Archipelago. Evidence for harvesting of G. catbaensis was obtained through interviews with local dealers, market surveys and a literature survey. Other potential anthropogenic impacts, namely “tourist activities” and “habitat degradation” were recorded by our own observations and interviews with local fishermen (
Most, if not all Goniurosaurus species were found being sold in the international pet market in Europe and the U.S. during the present study. According to the LEMIS database of the U.S. Fish & Wildlife Service, a total of 16,714 specimens of Goniurosaurus spp. have been imported into the U.S. (mean of 835 ± 1082 individuals annually) between 1999 and 2018 (Fig.
International trade in Goniurosaurus species between 1999 to 2018 to or from the U.S. A Annual volumes of import into the U.S. B number of exported specimens per exporting party (CA = Canada; CN = China; CZ = Czech Republic; DE = Germany; HK = Hong Kong; ID = Indonesia; NL = Netherlands; PL = Poland; TH = Thailand; TW = Taiwan) C number of imported specimens per species into US. Source: LEMIS database of the U.S. Fish & Wildlife Service (1999–2018).
International trade in Goniurosaurus species from 1999 to 2018 to or from the U.S. A Source of animals B purpose of trade. Source: LEMIS database of the U.S. Fish & Wildlife Service (1999–2018).
In March 2018, market surveys showed that the trade in Goniurosaurus in the EU mainly takes place online, but also in reptile fairs. It was recorded that specimens for sale fetch prices between US$35–200 on the international internet markets, e.g. price for two unsexed juveniles or one male of G. araneus was recorded for sale for US$150, G. bawanglingensis for €175 per pair (US$200), G. catbaensis for US$195–230 per specimen or for €300 (US$340) per pair, G. hainanensis for US$45–150 per specimen, G. huuliensis for US$400 per pair or US$150 for one male, G. lichtenfelderi for US$70–100 per specimen and G. luii for US$175 per two juveniles or for US$40–60 per pair or one (Table
International trade in several Goniurosaurus species in Europe based on online investigations and interviews with dealers on reptile fairs (own surveys in 2018 and data from Altherr et al. in lit. 2019).
Species | Trade type | Place | Country | Price (USD) per specimen |
---|---|---|---|---|
G. araneus | Offer | Internet Shops | Europe | 150–170 (€142) |
G. bawanglingensis | Offer | Fair, Internet Shops | Germany, Europe | €67–250 (or €175 per pair) |
G. catbaensis | Offer | Fair, Internet Shops | Germany, Europe | 195–230 (or €300 per pair) |
G. hainanensis | Demand and Offer | Internet Shops, Shops, and Private | Czech Republic, France, Germany | 45–150 |
G. huuliensis | Demand and Offer | Internet Shops and Private | Europe | €160–220 (€400 per pair) |
G. lichtenfelderi | Demand and Offer | Internet Shops and Private | Europe | 70–100 |
G. luii | Demand and Offer | Fair, Internet Shops | France, Germany, Europe | 40–170 |
Furthermore, Altherr et al. (in lit. 2019) reported a total of 835 specimens of Goniurosaurus spp. were observed for sale on 142 different online adverts with prices ranging from €35–300 (US$40–365) between September 2017 and September 2018, whereof, G. araneus (n = 56) were offered for sale of €142, G. bawanglingensis (n = 102) for €67–250 G. catbaensis (n = 29) for €170, G. hainanensis (n = 162) for €35–140, G. huuliensis (n = 41) for €160–220, G. lichtenfelderi (n = 97) and G. luii (n=150) for €35–142.
According to interviews with local dealers in Vietnam in March 2018, all five native Goniurosaurus species have been frequently recorded in local pet shops from Dong Nai Province and Ho Chi Minh City in northern Vietnam, on Social Media, e.g. Facebook, Zalo online and other internet platforms. These tiger geckos were usually wild-caught by local villagers who live within the species’ distribution range and then sold for little money to dealers to be either offered in local pet shops or be sold to other traders. Goniurosaurus specimens were found to be locally offered for sale at US$7–25 per animal in pet shops in Vietnam (Table
Information on local trade in and international trade pathways for Goniurosaurus species in Vietnam based on interviews with local dealers in 2018.
Species | Sources | Offered in pet shops | Country of destination | Minimum quantity per deal for export | Price (USD) per specimen* |
---|---|---|---|---|---|
G. araneus | China | Dong Nai Province | Thailand, Indonesia, EU and the U.S. | 50 | (2): 100–150 |
G. catbaensis | Cat Ba NP, Hai Phong city, Viet Nam | Dong Nai Province, Ho Chi Minh City | Thailand, Indonesia, EU and the U.S | >= 20 | (1): 7–25 (2): 150 |
G. huuliensis | Huu Lien NR, Lang Son Province, Viet Nam | Dong Nai Province, Ho Chi Minh City | Thailand, Indonesia, EU and the U.S. | >= 20 | (1): 20–25 (2): 100 |
G. lichtenfelderi | Yen Tu, Quang Ninh Province, Viet Nam | Dong Nai Province | Thailand, Indonesia, EU and the U.S. | >=20 | (1): 20–25 (2): 100 |
G. luii | Cao Bang Province, Viet Nam | Dong Nai Province, Ho Chi Minh City | Thailand, Indonesia, EU and the U.S. | 50 | (1): 20–25 (2): 100–150 |
We observed a total of 73 animals (54 adults) in July 2017 on four islands and a total of 93 individuals (70 adults) in April 2018 within sites covered by the shrub vegetation on three islands in Ha Long Bay. We did not find any specimens of Goniurosaurus on out-surfaces of karst formations by boat surveys. The total population size at the survey areas was estimated at 175 individuals in July 2017 and 180 animals in April 2018. Regarding the effective population size – considering only mature animals – this estimated wild population was relatively similar to about 124 and 129 individuals in July 2017 and April 2018, respectively (Table
Summary of the population assessment of Goniurosaurus catbaensis including observed individuals, densities (D) and population size estimates (N) in Ha Long Bay in July 2017 and April 2018. Ind: individuals; Asterisks indicate missing data (no survey).
Island 1 (T-1) | Island 2 (T-2) | Island 3 (T-3) | Island 4 (T-4) | Total | |
---|---|---|---|---|---|
July-2017 | |||||
Total (observed) | 27 | 7 | 20 | 19 | 73 |
Mature (obs.) | 17 | 3 | 16 | 18 | 54 |
D observed [ind/100 m of route] | 7.1 | 2.3 | 10 | 4.6 | 6 |
D [mature/ 100 m of route] | 4.5 | 1 | 8 | 4.4 | 4.5 |
Nmature | 36 | 4 | 33 | 50 | 124 |
Ntotal | 56 | 16 | 49 | 54 | 175 |
April-2018 | |||||
Total (observed) | 45 | * | 15 | 33 | 93 |
Mature (obs.) | 28 | * | 12 | 30 | 70 |
D [ind/100 m of route] | 11.8 | * | 7.5 | 8.1 | 9.1 |
D [mature/100 m of route] | 7.3 | * | 6 | 7.5 | 7 |
Nmature | 60 | * | 27 | 45 | 129 |
Ntotal | 86 | * | 45 | 49 | 180 |
The mean density of G. catbaensis, along suitable habitat sites in Ha Long Bay, was estimated to be around 6 individuals and 4.5 adults per 100 m transect length during April and 9.1 individuals and 7 adults per 100 m transect length during July. By comparing different sites, the highest abundance was estimated at nearly 12 individuals per 100 m/ transect length at site 1 in April, while we found the lowest density of 2 animals per 100 m/ transect length at site 2 in July (Table
In both investigated months, the sex ratio of adults was relatively balanced with a little higher percentage of females of G. catbaensis (57% and 55%, respectively). The percentage of gravid and non-gravid females significantly differed between both months (c2 = 21; df = 2; P < 0.001), while 44% of females (n = 14) were gravid in July 2017 (Fig.
With regard to the daily activity pattern, G. catbaensis was found to be active at night from approximately 20:00 h to 04:00 h. The vast majority of lizards (98 animals or 62% of the recorded lizards) were observed between 22:00 h and 24:00 h. We further found a difference in population structure amongst different times of the day (c2 = 14.39; df = 6; P = 0.026 < 0.05). Particularly, we observed that more adult specimens were active during the first four hours between 20:00 h and 24:00 h (n = 81 account 65.3% of captured adults), while juveniles were frequently found either before 22:00 h or mainly between 00:00 h and 04:00 h. Most juveniles were found between 02:00 h and 04:00 h (Fig.
The number of captured animals and the size of sub-populations of G. catbaensis from Ha Long Bay in Quang Ninh Province were compared with other differently affected sub-populations in Cat Ba Archipelago of Hai Phong City. In the Cat Ba National Park and Ha Long Bay’s tourist caves, total anthropogenic impacts were considered to be “Medium” and local populations were relatively small (2–10 individuals). A strong flood event in 2015 appeared to have caused the local extirpation of G. catbaensis at one site in Viet Hai Commune on Cat Ba Island (Table
Recorded impacts on Goniurosaurus catbaensis at known sites. Single impacts were ranked according to severity as “not recorded” defined as never being recorded, “low” as being rarely observed, “medium” as being recorded several times, or “high” as being recorded frequently, or the extent of destruction was evaluated too high.
Study sites | Population size (Mean) | Harvest | Tourist activities | Habitat degradation | Total impacts |
---|---|---|---|---|---|
Sites near the headquarters of Cat Ba National Park (NP) – |
5 | Medium | High | Medium | Medium |
Viet Hai Commune – Cat Ba NP – |
10 | Medium | Medium | Low | Medium |
One site in Viet Hai Commune – Cat Ba NP – |
0 (in August 2015) | Not recorded | Not recorded | High | High |
Ha Long Bay (4 islands) – Current study | 51 | Not recorded | Not recorded | Low | Low |
Ha Long Bay’s Caves (4 caves) – Current study | 2 (total animals) | Not recorded | High | Medium | Medium |
All tiger geckos have a restricted distribution ranges and are – like many endemic reptiles – extremely vulnerable to exploitation, so that international trade can quickly become a significant threat for extinction (
Goniurosaurus spp. have been popular in the international pet market at least since the 1990s (
We herein observed most Goniurosaurus species for sale in the EU online as well as in reptile fairs. Accordingly, Altherr et al. (in lit. 2019) spotted a total of 835 specimens of Goniurosaurus spp. for sale on different social media platforms between 2017 and 2018. These observations, during random physical as well as internet market surveys, only reflect snapshots of current EU trade in tiger geckos. Actual trade volumes remain unknown – as Goniurosaurus spp. are not as yet listed in the CITES Appendices – but are likely to be higher.
According to interviewees in Vietnam and Europe, captive-bred animals were not yet available in quantities to meet the global demand and wild animals were generally offered for much cheaper prices than captive-bred animals. Furthermore, wild-caught specimens are considered to have a high mortality rate during transport and stockpiling (
Recent population estimates of the Cat Ba Tiger Gecko at its type locality on Cat Ba Island suggested extremely low population sizes (
Similar research on another enigmatic Vietnamese gecko species, Cnemaspis psychedelica, endemic to small islands in the south of Vietnam, revealed a density of 12–19.2 animals / 100 m and an estimated population size of 365–732 individuals (
The recorded abundances in G. catbaensis also appear to be extremely low compared to other threatened and endemic geckos. The lowest abundances of G. catbaensis were found at touristic sites on Cat Ba Island. Conversely, abundances were relatively stable on the islands in Ha Long Bay, which comprised intact habitats and were not affected by human activities, as they were too small and inaccessible. Harvesting has not been recorded on these small islands so far. Thus, it is likely that the much lower densities of the species on Cat Ba Island are the result of anthropogenic pressures, especially collection for the pet trade.
As G. catbaensis was found to occur in very low densities and has extremely restricted habitat ranges (small islands) that are subject to stochastic weather events, the species appears to be extremely vulnerable to harvesting, which appears to be the case for the entire genus.
Endemic species are considered to be especially vulnerable to over-exploitation (
Some Goniurosaurus taxa are only found within protected areas in Vietnam, for example G. catbaensis in Cat Ba National Park and Ha Long Bay World Heritage site, G. huuliensis in Huu Lien Nature Reserve, G. lichtenfelderi in Bai Tu Long National Park and animals can only be collected with appropriate permits from local authorities. At the time of writing this manuscript, all Goniurosaurus species native to Vietnam have been included in Group IIB of the Governmental Decree 06/2019/ND-CP, which came into force on 10 March 2019 and prohibits the collection of and trade in respective species without permits in Vietnam (
Signboard handed over to the Ha Long Bay Management Department to point to the threats and conservation need of the Cat Ba tiger gecko in English and Vietnamese languages.
To further improve the conservation status of Goniurosaurus species, we recommend the following measures:
• The inclusion of Goniurosaurus spp. in the Appendices of CITES in order to better control and monitor trade in wild specimens. The current proposal to include all Goniurosaurus species from China and Vietnam in CITES Appendix II should be supported. Likewise, we acknowledge that the Japanese Goniurosaurus clade may warrant listing in the CITES Appendices. Therefore, a listing could be considered in the future, as also proposed by
• As the lack of adequate information on the biology and conservation status of single species can impede conservation measures, a timely assessment of the remaining Goniurosaurus species in the IUCN Red List is strongly advised. Therefore, more species specific research is needed to fully understand conservation requirements.
• It is likely that, with more research, further cryptic species or new occurrences of this genus will be discovered in the future. Thus, it is strongly recommended to conceal exact locality data as well as detailed descriptions of localities for such new species or population records in order to prevent targeted collection, as has happened in the past.
• We recommend to improve or establish coordinated ex-situ breeding programmes for all species and to build up a stable captive population in order to a) serve as the backup population for restocking measures (also in the light of extreme population declines e.g. due to stochastic weather events) and b) to meet the demand for tiger geckos in the trade and thereby reduce the pressure on wild populations.
For supporting fieldwork and issuing relevant permits, we thank the authorities of the Cat Ba National Park (CBNP), Hai Phong City and the Management Department of Ha Long Bay (MDHLB), Quang Ninh Province. We are very thankful to K. X. Nguyen (CBNP), M. L. Pham (MDHLB) and H. Q. Nguyen (Ha Noi National University of Education) for assistance in the field. We are grateful to T. Pagel and C. Landsberg (Cologne Zoo), M. Bonkowski (University of Cologne), T.H. Tran, T. H. Vu, C. T. Pham, T. V. Nguyen, N. H. Nguyen (IEBR, Hanoi), M.T. Nguyen, L.V. Vu and T.T. Nguyen (VNMN, Hanoi) for their support of conservation-based biodiversity research in Vietnam. Thanks to S. Altherr (Munich) and M. Auliya (Leipzig) for improving a previous version of the manuscript. This research is supported by the National Foundation for Science and Technology Development (NAFOSTED, Grant No. 106.05-2017.329). Field surveys were partially funded by Cologne Zoo, the Mohamed bin Zayed Species Conservation fund (Project: 170515492), equipment was supported by the Idea Wild. Cologne Zoo is partner of the World Association of Zoos and Aquariums (WAZA): Conservation Project 07011, 07012 (Herpetodiversity Research, Amphibian and Reptilian Breeding and Rescue Stations). Research of Hai Ngo in Germany is funded by the German Academic Exchange Service (DAAD).