Research Article |
Corresponding author: Thomas Ziegler ( ziegler@koelnerzoo.de ) Academic editor: Mark Auliya
© 2020 Katharina Kasper, Jonas Schweikhard, Max Lehmann, Cara Leonie Ebert, Petra Erbe, Sengdeuane Wayakone, Truong Q. Nguyen, M. D. Le, 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:
Kasper K, Schweikhard J, Lehmann M, Ebert CL, Erbe P, Wayakone S, Nguyen TQ, Le MD, Ziegler T (2020) The extent of the illegal trade with terrestrial vertebrates in markets and households in Khammouane Province, Lao PDR. Nature Conservation 41: 25-45. https://doi.org/10.3897/natureconservation.41.51888
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Wildlife is one of the most important food resources in rural areas and popular among all social layers of Lao PDR. Numerous vertebrate species are sold at the local markets, but a comprehensive understanding of people’s involvement and their impact on survival of local populations remains insufficient. This study provides the first interdisciplinary assessment using a questionnaire-based survey approach to investigate both markets and households in Khammouane Province in central Lao PDR. Data were recorded during the dry season (October and November 2017), as well as the rainy season (June and July 2018). We documented 66 traded species, mainly intended for consumption purposes, with more than half of them protected under either national law or international convention/red list. Furthermore, an evaluation of wildlife use from urban to the most accessible rural areas, indicated differences in affordability and trapping behavior. Our results suggest that wildlife availabilities can less and less satisfy the unchanged demands.
Biodiversity crisis, interdisciplinary, Southeast Asia, sustainability, wildlife trade
The ongoing biodiversity crisis exceeds past rates drastically (
The use of wildlife can be found in all classes of society, but a majority of Lao people lives under rural conditions (
Regulations and enforcements have been insufficient to control wildlife trade at both international or national level (
Lao PDR’s regulations on wildlife use and trade are mainly based on the Lao Wildlife and Aquatic Law (LWAL) (No.7, 2007), in which species are classified according to the Government’s recognition of social values and protection requirements. Nonetheless, the regulations largely disregard international statuses and other biological factors. The LWAL lists three protection categories: species considered at risk of extinction and of high value to the society are listed in the Prohibition Category I; their use is prohibited without permission. Species in the Management Category II include those of national economic, social and environmental interest and importance for livelihoods; their use is attempted to be controlled (
Khammouane / Hin Nam No Khammouane Province holds three protected areas, representing the remaining major forest areas: Phou Hin Poun NPA, Nakai Nam Theun NP and Hin Nam No NP (HNN), which is most relevant for this study. Covering an area of 92,000 hectares on the Lao-Vietnamese border in Boualapha District, HNN forms one of two largest protected continuous karst areas in the world (
In a former study we provided data towards an annual overview and an evaluation of seasonal market fluctuations regarding offered species (
We investigated the trade of wild-sourced terrestrial vertebrates, namely: mammals, birds, reptiles and amphibians. These four vertebrate classes cover the higher terrestrial fauna of the study area, Khammouane Province (~ 7,200 km2). Located in central Lao PDR (17°30'N, 105°20'E) and bordering two other Lao provinces, as well as Vietnam and Thailand, the area connects important trade hubs and sets an ideal example for thriving trafficking (Fig.
Map of Khammouane Province showing the locations of the household (black, 1–14) and market (white-filled, I–XI) survey sites. Source: Own map, compiled using self-collected GPS data and open source shapefiles (‘Laos protected areas and heritage sites’ by Open Development Laos (CC-BY-SA); ‘Laos-Admin Boundaries’ provided by Office for the Coordination of Humanitarian Affairs.
To gain a year-round overview, the study took place in October and November 2017, as well as in June and July 2018, corresponding to dry and rainy season of the prevailing tropical monsoon climate. We surveyed local food markets (Fig.
We conducted 66 observational surveys at 15 trade hubs (Fig.
In addition to the permanent markets, temporary vending stalls along the highways Route 12 and Route 13 were documented, because they offered large amounts of wildlife (
We conducted household surveys for a broader understanding of people’s involvement in wildlife trade, use or trapping behavior. Here, trapping refers to a wide spectrum of wildlife harvesting including the use of snares, hunting with guns, slingshots or dogs, as well as the use of poisoned baits. We surveyed a total of 63 households at 14 sites (Fig.
Statistical analyses were carried out in R environment for statistical computing (version 3.5.1,
Out of all listed terrestrial vertebrate species present in Lao PDR, large proportions could be found in trade, with majorities in highest conservation statuses (Tables
Numbers of species native to Lao PDR and listed on CITES Appendices (
Vertebrate | Conservation Status | ||||||||
---|---|---|---|---|---|---|---|---|---|
LWAL | CITES | IUCN Red List | |||||||
Class | I | II | I | II | CR | EN | VU | NT | LC |
Mammalia | 44 | 15 | 35 | 24 | 11 | 23 | 19 | 8 | 172 |
Aves | 36 | 21 | 6 | 77 | 7 | 6 | 18 | 36 | 656 |
Reptilia | 8 | 13 | 3 | 26 | 5 | 10 | 17 | 5 | 121 |
Amphibia | 1 | 0 | 0 | 0 | 0 | 6 | 11 | 6 | 112 |
% found | 23.7 | 4.3 | 35.0 | 12.2 | 56.5 | 75.6 | 67.7 | 89.1 | 1.89 |
Overview of observed species/genera at risk and their conservation status according to CITES Appendices, the IUCN Red List [Not Evaluated (NE), Data Deficient (DD), Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN) and Critically Endangered (CR)] and the Lao Protection List [Prohibition Category (P) and Management Category (M)], by taxonomic classes and orders. Large amphibian sales units were rounded to each full 5 or 10. Nat. = National Conservation Status; No.S.= number of sightings; Ind.= individuals.
Taxon | Species | Common Name | CITES | IUCN | Nat. | No.S. | Ind. |
---|---|---|---|---|---|---|---|
Mammalia | |||||||
Artiodactyla | Muntiacus sp. | Muntjac | 1 | 1 | |||
Muntiacus vaginalis | Northern Red Muntjac | none | LC | M | 2 | 2 | |
Sus scrofa | Wild Boar | none | LC | none | 5 | 10 | |
Tragulus kanchil | Lesser Mouse-deer | none | LC | none | 1 | 1 | |
Carnivora | Helarctos malayanus | Sun Bear | I | VU | P | 1 | 1 |
Herpestes javanicus | Javan Mongoose | none | LC | none | 2 | 2 | |
Ursus thibetanus | Asian Black Bear | I | VU | P | 2 | 2 | |
Lutrogale perspicillata | Smooth-coated Otter | II | VU | P | 1 | 1 | |
Melogale personata | Burmese ferret-Badger | none | LC | M | 1 | 1 | |
Paradoxurus hermaphroditus | Asian Palm Civet | none | LC | M | 4 | 5 | |
Prionailurus sp. | Wild Cat | 1 | 2 | ||||
Prionailurus bengalensis | Leopard Cat | II | LC | none | 4 | 5 | |
Chiroptera | Cynopterus sphinx | Greater Short-nosed Fruit Bat | none | LC | M | 1 | 5 |
Eonycteris spelaea | Cave Nectar Bat | none | LC | M | 2 | 32 | |
Hipposideros armiger | GreatHimalayan Leaf-nosed Bat | - | LC | M | 1 | 9 | |
Miniopterus sp. | Bent-winged Bat | M | 1 | 4 | |||
Rousettus amplexicaudatus | Geoffroy’s Rousette | none | LC | - | 1 | 1 | |
Lagomorpha | Lepus peguensis | Burmese Hare | none | LC | M | 1 | 1 |
Pholidota | Manis sp. | Pangolin | II | CR | P | 2 | 5 |
Primates | Nycticebus bengalensis | Bengal Slow Loris | I | EN | P | 3 | 3 |
Pygathrix nemaeus | Red-shanked Douc Langur | I | CR | P | 1 | 1 | |
Proboscidea | Elephas maximus | Asian Elephant | I | EN | P | 1 | 1 |
Rodentia | Atherurus macrourus | Asiatic Brush-tailed Porcupine | none | LC | M | 2 | 2 |
Bandicota savilei | Savile’s Bandicoot Rat | none | LC | none | 1 | 1 | |
Belomys pearsonii | Hairy-footed Flying Squirrel | none | DD | none | 1 | 1 | |
Biswamoyopterus laoensis | Laotian Giant Flying Squirrel | none | DD | none | 5 | 8 | |
Callosciurus erythraeus | Pallas’s Squirrel | none | LC | none | 14 | 26 | |
Callosciurus finlaysonii | Finlayson’s Squirrel | none | LC | none | 1 | 1 | |
Dremomys sp. | Red-cheeked Squirrel | - | - | none | 1 | 2 | |
Rodentia | Dremomys rufigenis | Asian Red-cheeked Squirrel | none | LC | none | 8 | 16 |
Hylopetes sp. | Flying Squirrel | - | - | none | 1 | 4 | |
Hylopetes alboniger | Particolored Flying Squirrel | none | LC | none | 1 | 3 | |
Hystrix brachyura | Malayan Porcupine | none | LC | M | 2 | 2 | |
Laonastes aenigmamus | Laotian Rock Rat | none | LC | P | 2 | 3 | |
Leopoldamys edwardsi | Edwards’s Long-tailed Giant Rat | none | LC | none | 5 | 5 | |
Leopoldamys sabanus | Long-tailed Giant Rat | none | LC | none | 12 | 80 | |
Menetes berdmorei | Berdmore’s Ground Squirrel | none | LC | none | 7 | 18 | |
Niviventer fulvescens | Chestnut White-bellied Rat | none | LC | none | 3 | 4 | |
Petaurista sp. | Flying Squirrel | none | LC | 5 | 7 | ||
Petaurista elegans | Spotted Giant Flying Squirrel | none | LC | none | 1 | 6 | |
Petaurista philippensis | Indian Giant Flying Squirrel | none | LC | P | 1 | 2 | |
Ratufa bicolor | Black Giant Squirrel | II | NT | M | 7 | 7 | |
Rhizomys pruinosus | Hoary Bamboo Rat | none | LC | none | 2 | 2 | |
Rhizomys sumatrensis | Large Bamboo Rat | none | LC | M | 1 | 1 | |
Scandentia | Tupaia belangeri | Northern Treeshrew | II | LC | none | 2 | 3 |
Aves | |||||||
Columbiformes | Spilopelia chinensis | Spotted Dove | none | LC | M | 3 | 10 |
Cuculiformes | Centropus sinensis | Greater Coucal | none | NE | P | 2 | 12 |
Passeriformes | Acridotheres tristis | Common Myna | none | LC | M | 2 | 2 |
Strigiformes | Ketupa ketupu | Buffy Fish Owl | II | LC | M | 1 | 1 |
Reptilia | |||||||
Squamata: Sauria | Gekko gecko | Tokay Gecko | II | NE | none | 1 | 15 |
Physignathus cocincinus | Chinese Water Dragon | none | NE | M | 3 | 10 | |
Varanus nebulosus | Clouded Monitor | I | NE | M | 4 | 5 | |
Varanus salvator | Asian Water Monitor | II | LC | M | 4 | 4 | |
Squamata: Serpentes | Naja sp. | Cobra | II | DD | M | 1 | 1 |
Ophiophagus hannah | King Cobra | II | VU | P | 3 | 15 | |
Ptyas korros | Chinese Ratsnake | none | NE | none | 4 | 8 | |
Testudines | Heosemys grandis | Giant Asian Pond Turtle | II | VU | none | 3 | 3 |
Malayemys cf. subtrijuga | Mekong Snail-eating Turtle | II | VU | M | 14 | 78 | |
Trionychidae sp. | Softshell Turtle | 1 | 1 | ||||
Amphibia | |||||||
Anura | Babina chapaensis | Chapa Frog | none | LC | none | 1 | 10 |
Fejervarya limnocharis | Asian Grass Frog | none | LC | none | 19 | 2083 | |
Glyphoglossus guttulatus | Burmese Squat Frog | none | LC | none | 2 | 110 | |
Hoplobatrachus rugulosus | East Asian Bullfrog | none | LC | none | 41 | 2962 | |
Humerana miopus | Three-striped Frog | none | LC | none | 5 | 395 | |
Kaloula pulchra | Banded Bullfrog | none | LC | none | 3 | 107 | |
Leptobrachella sp. | Asian Leaf-litter Frog | none | LC | none | 6 | 1162 | |
Occidozyga martensii | Round-tongued Floating Frog | none | LC | none | 1 | 70 | |
Raorchestes parvulus | Karin Bubble-nest Frog | none | LC | none | 1 | 6 | |
Sylvirana guentheri | Gunther’s Amoy Frog | none | LC | none | 9 | 575 | |
Sylvirana nigrovittata | Sap-green Stream Frog | none | LC | none | 5 | 389 |
Bengal Slow Loris (Nycticebus bengalensis) (left); squirrels (Callosciurus erythraeus, Menetes berdmorei or Dremomys rufigenis), bats (Hipposideros armiger and Rousettus amplexicaudatus) (right) offered at a local food market. Phot. C.L. Ebert.
Buffy fish owl (Ketupa ketupu) (top left), Mekong snail-eating turtle (Malayemys cf. subtrijuga) (bottom left), Chinese water dragon (Physignathus cocincinus) (top right), and East Asian bullfrogs (Hoplobatrachus rugulosus) with broken legs (bottom right) offered at a food market. Phot. K. Kasper, T. Ziegler.
Approximately 90% of the surveyed households confirmed use of wildlife. However, differences became apparent in their own trapping involvement and the affordability of wild meat regarding the location of the household (Fig.
Households along an urbanization gradient (rural, transition and urban area) that depicts their involvement in wildlife trapping activities, and those that claimed rate wild meats on the market more affordable than meats from a farmed source (N = 55, 46). Trapping involvement of households in rural areas differs significantly from that in the urban area (Fisher’s exact test, P = 0.032). Regarding wild meats’ affordability, households in rural areas differ significantly from the other areas (Fisher’s exact test, P=5.928-5), with a difference to transition areas by P = 0.007 and P = 0.005 to the urban area. Data was drawn from the respective interviews.
Roughly 84.1% of the respondents confirmed changes in the wildlife market over time. While a majority reported the general demand to remain the same, the availability of wild meats was reported to have decreased and accompanied by increasing prices (Fig.
Households observing market changes regarding demand trends (N = 35), offer (N = 53) and prices (N = 44) for offered wildlife. There are differences between offer and demand (Fisher’s exact test, P = 4.08∙10-13), as well as offer and prices (Fisher’s exact test, P = 1.57∙10-20). Data was drawn from the respective interviews.
Ultimately, the relationship between offer and demand as shown in the study can be a good indicator for wildlife use in the province as well as wildlife population status. By investigating local people’s reflection on wildlife availability and accessibility in markets, we demonstrated that available wildlife products fail to satisfy the constant demand. This allows a disquieting view on the issue against the background of an escalating biodiversity crisis, as biodiversity especially in the study area faces an immense loss (
Rats (Leopoldamys sabanus, Niviventer sp. or Rattus sp.) (upper left), squirrel (Menetes berdmorei) (upper right), and frogs (bottom) were most common traded wildlife. Phot. T. Ziegler.
However, the use of wildlife as meat is no longer a matter of subsistence. This was confirmed by many of our interviewees in the urban areas, who described their preference of wild meat over domesticated meat. Studies from Africa and Asia indicated that an increase in wealth may cause a significant rise in demand, resulting in expanding wildlife markets in urban towns (
Wild meat remains a primary protein source in rural areas such as in Khammouane Province (
The issue of unsustainable wildlife consumption in poor countries like the Lao PDR (Government’s Office 2014) might even worsen in the future, as the global human population growth (
The current biodiversity crisis and the issue of its driving forces, such as the unsustainable usage of wildlife (GIZ and ProCEEd 2014), are complex problems which require multifaceted efforts to be implemented. A simple ban of trading wildlife is unlikely to succeed as it might shift the sales of wildlife and derived products from open market displays to the underground (
Frogs, squirrels and rats were documented in almost every recorded instance, outnumbering other taxonomic groups by far (Fig.
The loss of certain species may cause a cascade of unforeseeable effects in the ecosystems. For example the loss of a species that others depend on can lead to subsequent extinctions of dependent taxa (
Sharing a border with neighbouring China, one of the major wildlife consumers, significantly increases the species decline in Lao PDR (
For his constant support during this study, the authors wish to express their sincere gratitude to the CTA of GIZ ProFEB’s Thakhek office Bastian Flury. Further, they would like to express their gratefulness to the entire staff of the GIZ office in Thakhek for support and engagement, in particular the drivers and the Lao translator Littideth Xaiyavongsa. By providing their co-operation and administrative authority, the staff from Provincial Level Offices of Forest Inspection of the Ministry of Agriculture and Forestry Laos supported this study immensely, which is highly appreciated. For scientific support and exchange in taxa identification the authors wish to thank Son T. Nguyen, Cuong T. Pham (Institute of Ecology and Biological Resources, Hanoi, Viet Nam) and Sisomphone Soudthichak (Natural Resources and Environmental Department, Khammouane). We thank Mark Auliya (Bonn) and an anonymous reviewer for their kind suggestions helping to improve a previous version of the manuscript. Ultimately, this study received support by Protection and Sustainable Use of Forest Ecosystems and Biodiversity (ProFEB) a program of the German Development Cooperation (GIZ), Cologne Zoo and the University of Cologne.
Standardized questionnaire for the household surveys, arranged by categories of interest.
Consumption | ||
1 |
Is wildlife consumed or traded
by themselves or in the household? |
94% yes; n=63 |
1.1 | If no, in the past? | 50% yes; n=4 |
1.2 | If ever, which animals? | n=61 |
Food Purposes | ||
2 | How often is wild meat consumed? | 2% daily, 39% weekly, 48% monthly, 11% annually; n=54 |
3 | What kind of meat is preferred? | 40% wild meat, 44% domesticated meat; 16% uncertain; n=63 |
4 | Is wild meat more expensive or cheaper than domesticated meat? | 38% cheaper, 35% more expensive, 27% uncertain; n=63 |
5 |
What are the reasons
for choosing wild meat? (multiple choice) |
48% taste, 43% health, 9% beliefs, 18% status symbol, 21% food variety, 29% necessity; n=56 |
Medicinal Purposes | ||
6 | Is wildlife used for medicinal purposes? | 32% yes; n=56 |
7 | What kind of medicine is preferred? | 13% wildlife-based, 67% conventional, 20% uncertain; n=63 |
Market Situation | ||
8 | Has the wildlife trade changed over time? | 84% yes; n=63 |
8.1 | Changes in prices? | 22% none, 46% increase, 2% decrease, 30% uncertain; n=63 |
8.2 | Changes in offer? | 5% none, 3% increase, 76% decrease, 16% uncertain; n=63 |
8.3 | Changes in demand? | 35% none, 13% increase, 8% decrease, 44% uncertain; n=63 |
9 |
Is open display on markets avoided
(by direct connections between trappers and costumers)? |
32% yes, 2% no, 66% uncertain; n=63 |
Trapping & Trading | ||
10 |
Is the household involved
in wildlife trading? |
16% yes; n=57 |
10.1 | Is trading important for their livelihood? | 44% yes; n=9 |
11 |
Is the household involved
in wildlife trapping? |
65% yes; n=55 |
11.1 | Is trapping important for their livelihood? | 76% yes; n=33 |
Conservation | ||
12 |
Is there awareness about
conservation statuses? |
89% yes; n=63 |
12.1 | Is the Lao Protection List known? | 7% yes; n=59 |
12.2 | If so, could protected and unprotected species be differentiated? | 25% yes; n=4 |