11
Wildlife Forensics
11.1 Introduction
Wildlife forensics is a sub‐discipline of forensic science and provides evidence to enforce the legislation that protects wild animals and plants. The procedures and analytical techniques are essentially the same as those used to investigate human criminal offences. If the evidence is to be used in a court of law, the investigation must be performed with the same attention to detail with careful record keeping and the maintenance of a ‘chain of evidence’. However, wildlife forensics presents its own unique challenges, especially when it comes to funding and DNA analysis. For example, wildlife criminal offences are often considered to be ‘low priority’ and therefore lack resources. When it comes to DNA analysis, there is strong statistical support for the reliability of the techniques used to identify individual humans, but this is generally lacking for other organisms.
Although more plant species are covered under CITES legislation, this chapter will focus almost entirely upon animals. The illegal trade in plants is covered in Chapter 12. Within this chapter, we consider what is meant by wildlife crime, why it is important, factors that drive it, how it is carried out, and the forensic techniques used to investigate it. We will finish with a consideration of specific examples of illegal wildlife trade. Cooper and Cooper (2013) and Huffman and Wallace (2012) provide detailed accounts of wildlife forensics.
11.2 When it is Legal to Kill or Exploit Wildlife
The killing of all animals, whether domestic or wild, is an emotive topic on which people hold strong views. It is therefore important to keep a sense of perspective and to realise that the question of whether or not the killing of an animal is ‘legal’ depends upon a number of variables that can be summarised as ‘which animal, where, when, how, and why’.
In many parts of the world, it is legal to kill certain wild animals for food, clothing, and ornaments. This can provide nutrition and revenue for indigenous people who lack alternative sources of food or employment. For example, in Alaska, indigenous people are permitted to hunt walruses for food and for their ivory. In this instance, an indigenous person is defined as someone who can prove that they are at least 25% ‘Alaskan Indian, Aleut or Eskimo, or that they are enrolled under the Alaskan Native Claims Settlement Act’. The killing of walrus by any other persons is illegal. Although killing game animals might provide food, nowadays hunting is primarily a recreational activity. This is not intended to trivialise a pursuit that many people take seriously and undoubtedly has its challenges and requires skill and patience. Nevertheless, the game hunter usually does not rely on the animal for their livelihood and goes hunting for personal enjoyment. Big game hunting can be a major source of revenue. If properly managed it generates money that can be used for conservation. For example, in 2014, an auction was held for the right to hunt and kill a single black rhinoceros in Namibia – the winning bid was US$ 350 000. In some African countries, the licence to kill a single lion costs over US$ 19 000. On top of this will be the costs of guides, food, travel, accommodation, etc. Consequently, a few big game hunters can provide a country with more foreign currency than several busloads of backpackers. Current estimates indicate that European game hunters shoot (legally) over 200 lions in Africa every year. The lions return as trophies – mostly to Germany, France, and Spain. The number of trophies that go to the USA, Russia, and Asia is not known but probably much higher. The killing of wild animals is permitted if they threaten peoples' lives and it is impossible to scare them away or capture and transport them to a region where they will not pose a danger. The killing of animals considered as pests (e.g. rats) or a threat to our health and livelihood is also allowed (Figure 11.1). Provided all of this killing is undertaken in a controlled and regulated manner, it need not affect animal populations and causes the targeted animal the minimum of suffering. Unfortunately, the rules governing the capturing and killing of wild animals and the harvesting of wild plants are frequently broken and many animals and plants are being driven to extinction.
Figure 11.1 Tunnel trap used to capture stoats and weasels on a grouse moorland. The design avoids the capture of non‐target animals, such as birds, hares, or sheep.
11.3 The Extent of the Trade in Wildlife
The extent of the worldwide trade in wildlife (plants and animals) is enormous: according to the organisation TRAFFIC www.traffic.org/trade the legal trade in wildlife was worth US$ 323 billion in 2009 and will undoubtedly have increased since then. By its nature, it is difficult to estimate the extent of the illegal trade but in 2016, one estimate suggested that it was probably in the region of US$ 23 billion per annum. The organisms that are being illegally traded range from orchids to baleen whales and salamanders to tigers.
The consequences of the illegal trade extend beyond the destruction of the population or even extinction of the animal or plant being traded. To begin with, if the species that is lost is what ecologists refer to as a ‘keystone species’, it results in disruption of the ecosystem. For example, the loss of wolves can result in the deer population increasing to the point at which there is overgrazing and the local ecosystem becomes degraded. The pursuit of the target animal or plant also causes habitat destruction – for example, the cutting down of forests and the driving of 4 × 4 vehicles over fragile tundra. Animals that are illegally hunted are seldom killed with a view to causing the minimum of pain and suffering and therefore animal welfare legislation is frequently contravened. Similarly, illegally traded live animals are often transported in cruel ways and many die en‐route to their destination. Because the trade in both live and dead animals (and plants) is unregulated, they are not checked or treated for pathogens and therefore animal, zoonotic, and plant pathogens are transported around the world with potentially catastrophic consequence. Illegal wildlife trade is also linked with other criminal activity that can lead to societal breakdown. For example, sometimes poachers are paid in drugs rather than cash.
11.4 CITES
CITES is the acronym for the Convention on International Trade in Endangered Species of Wild Flora and Fauna. It came into being in 1963 at a meeting of the World Conservation Union (IUCN). Its purpose is to establish a framework that provides protection for wildlife and regulates the trade in wildlife and wildlife products. Member states that agree to be bound by the Convention are referred to as ‘Parties’. CITES legislation does not override national laws but when a country agrees to become a Party it must adjust its laws to ensure that the CITES framework is adopted. This does not stop a country providing more stringent protection laws for its wildlife, but they cannot be more lax. In 2017, there were 183 Parties – this represents 93.8% of the countries of the world (193 members of the United Nations plus 2 non‐member observer states: the Vatican City and the State of Palestine). Currently, 5600 animal species and 30 000 plant species are covered by CITES. Sometimes a whole group is covered, such as cetaceans (whales, dolphins, and porpoises) and sometimes it will be a single species, a sub‐species, or local population in a single country. The organisms are said to be ‘listed’ in one of three Appendices according to how much protection they require.
Appendix I: Organisms in this appendix are those that are the most vulnerable and without serious protection they are in danger of becoming extinct. Examples include rhinoceroses and tigers. All international trade in these organisms is forbidden, except when it is not for commercial purposes and both an exporting and importing permit have been granted. This might take place for scientific purposes such as when researchers need to move rhino horn or ivory between laboratories in different countries to conduct specific analytical tests. Unfortunately, regulations can be wilfully misused. For example, Japan, a CITES party, continues to hunt whales despite these being listed in Appendix I, by claiming that they are undertaking ‘scientific whaling’. Animals listed in Appendix I that are captive bred and have documentation proving their parentage, age, and ownership can be traded as if they were Appendix II organisms.
Appendix II: These are organisms whose populations are reduced to the point at which they are of serious concern, but they are not considered to be in immediate danger of extinction. Limited trade is allowed but with strict regulations to prevent over‐exploitation. Species whose populations are not in danger, but look similar to ones that are at risk, are often included in Appendix II. This is to stop traders hiding protected species among similar non‐protected species. An export permit is required before an organism listed in Appendix II can be traded and the granting authorities must be satisfied that the animal was killed or collected lawfully and the survival of the wild population has not been compromised. For example, a big game hunter could export a lion's head from South Africa if he had a permit that allowed him to shoot a lion on a named game park and this had been done according to the law. Although an import licence is not required under CITES legislation, some countries have their own stricter regulations concerning the importation of animals and plants.
Appendix III: These organisms are listed at the specific request of a Party member. This is because they wish to regulate the trade in a plant or animal in their country, but need the support of other Party members to control the international trade. The trade in Appendix III species is permitted only if trader (and buyer) is in possession of the appropriate certificates or permits.
There are regular meetings and conferences held by the Party members that determine whether an organism's Appendix I and Appendix II status should change. Where total agreement cannot be obtained, a species may be listed under two appendices according to the country in which it is found. Individual countries do not need general agreement at a conference or meeting in order to add or remove Appendix III status to an organism living in their country.
11.5 Factors that Contribute to the Illegal Trade in Wildlife
Five key factors help maintain the illegal trade in wildlife: tradition, the pet trade, organised crime, governments, and the internet. These factors do not operate in isolation and often two or more factors interact.
11.5.1 Tradition
All societies value their traditions and resent ‘outsiders’ telling them that what they are doing is wrong and must stop. As mentioned above, humans have always exploited the wild animals and plants living around them and many feel that it is part of their normal way of life. Whilst this was usually sustainable when our population was low, now that the human population has grown, the demand frequently exceeds supply. A particular case in point is Chinese Traditional Medicine that is a major consumer of wild animals and plants and is mentioned several times in this chapter.
11.5.2 Pet Trade
As societies become more affluent, people have more disposable income. They therefore have more opportunities for expressing their individuality through dress, diet, and possessions. Pets are but one form of possession and a global multi‐million pound pet industry has arisen that caters for increasingly exotic, unusual, and totally unsuitable pets. This is further exacerbated by crazes for animals associated with popular films or fads. For example, the series of Harry Potter films sparked a demand for owls as pets, whilst the film ‘Finding Nemo’ resulted in a huge trade in clownfish (Amphiprion spp.). Virtually all animals from corals to tigers can be purchased as pets. However, the trade in fish, amphibians, and reptiles is causing serious problems for some wild populations. A large proportion of the pet trade involves the movement of tropical species in Asia and South America to buyers in Europe and North America, but there is also a substantial ‘home market’. Although there are rules in most countries governing the sale and ownership of pet animals, these are often weakly enforced. Similarly, in many developing countries, it is illegal to keep animals caught in the wild as pets, but there is usually little enforcement. Animals that are normally considered wild but have been bred in captivity, can be kept as pets if there is documentation proving their provenance. However, this would depend upon the local regulations. For example, in England it would be legal for an individual living in an ordinary house to keep a captive born peregrine falcon in his home but not a captive born tiger. In some US states, the individual could keep both a peregrine falcon and a tiger.
11.5.3 Organised Crime
The extent of the wildlife trade is enormous and the potential for huge profits attracts organised criminal gangs. For example, illegal wildlife trade is often linked to criminal activities such as drug trafficking and gun running. This is partly because organised criminal gangs already have knowledge and expertise in moving contraband around the world. They can therefore utilise existing distribution networks and contacts in both the exporting and importing countries. This is not a new phenomenon: in 2001, there was a newspaper report that in Brazil 40% of illegal drug shipments were combined with wildlife.
The illegal wildlife trade appeals to criminal gangs, because it combines the twin attractions of having a high profit: low volume ratio and relatively low risk. For example, 1 kg of rhino horn is worth approximately US$ 65 000 and is easily transported hidden among legal items. Furthermore, the penalties for wildlife trafficking are much lower than those for trafficking in either drugs or firearms. For example, in the UK a first‐time offender caught smuggling 1 kg of heroin – which is worth about the same amount as rhino horn (based on street prices per gram) – can expect a minimum jail sentence of around 10 years. By contrast, if he was caught with 1 kg of rhino horn he might escape with 1 year in jail. To give a typical example, in the Republic of Ireland in 2013, two men who were caught attempting to smuggle rhino horns worth €500 000 received fines of only €500.
11.5.4 Governments
Only governments have the power to pass legislation. Governments decide what the laws of the country will be and whether they are going to abide by international conventions such as CITES. Without laws that specifically protect wildlife, it is vulnerable to exploitation. In addition, those laws must not have loopholes that can be exploited. For example, South Africa used to have a law that allowed a hunter to export one set of rhino horns per year as a trophy. This law was exploited by a Vietnamese smuggling ring that sent a succession of ‘proxy hunters’ to stand by an unscrupulous professional South African hunter when he shot a rhino. The proxy was then photographed standing rifle in hand by the dead rhino and left on the next plane home with his ‘trophy’. Once back home the proxy handed the horn over to his employer and it was ground up for use in Chinese Traditional Medicine. However, in terms of the CITES paperwork needed for the export and import of body parts from a protected species of animal, everything was in order. In a similar manner, only governments have the power to enforce legislation. Therefore, if a government is weak, lacks the will, or officials are corrupt, then it does not matter what laws are in place because they will not be enforced. For example, although China has passed legislation banning the import and use of tiger body parts in traditional medicine, the practice continues. This is not helped by official support from the State Forestry Administration for the ‘Xiongsen Tiger and Bear Mountain Village’. At this establishment, over 1500 tigers are confined in small cages or allowed to roam about treeless enclosures. The bones of dead tigers are used in the preparation of a rice wine. A bottle of tiger wine sells for around US$ 260 and consuming a glass a day is said to be efficacious at alleviating joint stiffness and rheumatism and, inevitably, ‘increasing sexual vigour’. The Xiongsen Wine Company claims that they only use bones of tigers that die of old age. However, if a government is simultaneously both preventing and supporting the use of body parts from a protected species of animal, it sends out mixed messages about what is acceptable. A similar lack of will to enforce certain legislation is common to many governments. The funding made available to fund the prosecution of wildlife crime in the UK is nowhere near sufficient to meet the scale of the problem and it is likely that the situation is similar in many other industrialised countries.
11.5.5 Internet
The Internet is one of the main contributors to wildlife crime, because it has few controls and no borders. One can buy virtually anything on the net at the click of a button and one does not have to enter the ‘dark web’ to find animals, plants, and wildlife products that are being traded illegally. For example, the tiger bone wine mentioned above is easy to find. Similarly, the market for a product within a country may be small, but the Internet allows a dealer to advertise his wares to the whole world. For example, within a country, there will be few people willing to pay US$ 300 for a Kaiser's spotted newt (Neuregus keiseri), but on an international scale there is a viable market. There are probably fewer than 1000 of these newts left in the wild and these are all in Iran. However, some people continue to advertise (with who knows what validity) that they can supply wild caught specimens. It should also be noted that there are many fake adverts designed to trap the unwary (money is taken and no goods sent or they are not of the advertised species) and some are placed by law enforcement agencies in the hope of entrapping those who seek to purchase protected species of wildlife or wildlife products.
11.6 Poaching
The term ‘poaching’ refers to either the killing of a game animal (e.g. roe deer, Capreolus capreolus; carp, Cyprinus carpio) in an illegal manner or the killing of a protected species of wild animal for food or profit. The killing of game animals almost invariably requires a permit that limits the number of animals that can be killed and where and when they can be killed. For example, in Scotland, red deer (Cervus elaphus) stags (males) can be killed only between 1 July and 20 October, whilst red deer hinds (females) can be killed only between 2 October and 15 February. Furthermore, the deer can be killed only within estates on which hunting is licensed and the animals may be shot with a rifle but not with a crossbow or bow and arrow. Individual estates give named individuals permission to hunt and sometimes set more restricted dates than those mentioned above during which hunting is permitted. In the UK, many people still think of poaching as being a quaint rural pursuit in which a humble villager supplements his meagre diet with the occasional pheasant or deer stolen from the local squire's estate. The truth is rather different and often involves gangs of men with criminal associations who kill large numbers of animals with the aid of vicious dogs and 4 × 4 vehicles. The poaching of wild animals is also often associated with serious criminal activity.
The evidence available at a scene of suspected poaching depends upon the animal concerned, the weapon(s) used, and the body part collected. For example, in the UK, deer poaching takes place for their meat. These animals are often shot with an air rifle and because the body is heavy, they are butchered quickly to remove the best cuts of meat. The guts, head, and forelegs are therefore left at the site where the animal fell. By contrast, in Africa, rhinoceroses are killed for their horns and after this is removed the whole body is left to rot.
11.6.1 Animal Evidence in Poaching Cases
A variety of evidence can be retrieved from the body of an animal that dies because of poaching. This includes the species of animal, its PMI, the cause of death, and molecular and trace evidence that links a person (or persons) to the poaching incident. A case of poaching is approached in exactly the same manner as that used for investigating a case of suspicious death of a human – although the same resources are seldom available. First, one must identify the species of animal and then the time of death. The latter is determined by considering the environmental conditions, the stage of decay, and entomological evidence. The likely cause of death is determined from a consideration of the crime scene, wound analysis, and an autopsy.
Large animals that are poached are often butchered at the site where they are killed. When an animal such as a deer is butchered, the poacher usually has to grasp the animal's limbs forcibly. This results in the transfer of human DNA onto the carcass and it is possible to extract it using adhesive water‐soluble tape (Tobe et al. 2011). It is also likely that the animal's blood (and hence DNA) will be transferred to the poacher's hands, clothing, and knife. However, although it is possible to demonstrate that a suspected poacher has deer blood (or that of some other animal) on his clothing it is not yet possible to link this to an individual game or wild animal with the same accuracy that can be done with human STR profiles. Trace evidence linking a poacher to an animal can be found in the form of clothing fibres transferred from the poacher to the animal when it is handled and in the transfer of animal hairs onto the clothing and possessions (e.g. car boot) of the poacher. Butchering a large animal is hard work and it is possible that the poacher will pause for a cigarette, drink, or snack during his efforts. In this case, fingerprints, and/or DNA might be recoverable from cigarette butts, drink cans, or wrappers that are left nearby. Evidence of dogs being used to hunt an animal may be obtained from wounds, hairs, paw prints, and nearby faeces. STR profiling can identify an individual dog and therefore canine DNA isolated from wounds or hairs link the dog's owner to the poaching incident.
Organised gangs often poach rhinos and elephants with the aid of military grade semi‐automatic weapons. Large calibre ammunition causes massive injuries that are immediately obvious. By contrast, the wounds caused by airguns and smaller calibre weapons may be obscured by fur or feathers. In this situation, radiography reveals pellets in the victim's body. Although some poachers use shotguns, these make a lot of noise and poachers seldom wish for attention.
Especially in USA, crossbows and bows and arrows are now popular for hunting. These are virtually silent and modern versions are extremely powerful but easier to draw than their forebears are. The arrowheads and crossbow bolts used for hunting usually have flanges that prevent them being pulled out easily and they are usually cut out. The presence of an arrow or bolt in an animal's body indicates the probable cause of death. It is not possible to link an arrow or bolt to a particular weapon but the user's DNA or a fingerprint might be on the shaft. Because they are silent, in parts of Africa some poachers are reverting to using spears and bows and arrows to hunt elephants. In this case, the spears and arrows are laced with an extract prepared from the roots, bark, and wood of the shrub Acokanthera spp. The extract contains ouabain that is a highly poisonous cardiac glycoside. The elephant does not die immediately and the poachers track it until it succumbs or is weak enough for them to finish it off. Because the animal is only killed for its tusks, it does not matter that it dies from poisoning. The use of crossbows and bows and arrows for hunting is banned in the UK and many other countries but is legal in Canada and some states in the USA. Poachers will also poison watering holes. For example, in Zimbabwe the poisoning of elephant watering holes with cyanide and paraquat is common. The poachers are only interested in collecting ivory from the dead elephants but many other animals that drink the water or attempt to feed on the dead elephants are also killed. The use of poisons for hunting is banned in most countries and is detectable by toxicological analysis.
11.6.2 The Use of Snares for Poaching
Snares are either designed to capture and kill or capture and restrain. They are popular with hunters who wish to capture animals for their pelt because damage is limited to one of the victim's limbs or its neck. Snares are, however, indiscriminate and capture any animal that steps or walks into the snare.
The typical snare consists of a length of rope, wire, or cable that at one end is fashioned into a noose and at the other is firmly attached to a tree trunk, post, or rock. The noose's position is such that a passing animal either puts its neck through the noose or treads in it. The noose then tightens around the neck or limb and because the other end of the snare is firmly anchored, the animal becomes trapped. There are two basic types of snare: free‐running snares and self‐locking snares. Free‐running snares are designed to tighten only to the point at which the animal is firmly held whilst self‐locking snares will continue to tighten and therefore result in strangulation or the blood supply to a limb being cut off. The use of self‐locking snares is banned in the UK and several other countries.
Animals trapped in snares may die from strangulation if caught by the neck or because of internal injuries resulting from excessive struggling. Foxes and other carnivores will attempt to chew their own limb off in an attempt to escape with potentially fatal consequences. If the snare is not inspected for a prolonged period, the animal dies from starvation, dehydration, or exposure. The animal may also be killed by the hunter when he inspects his snares: an unintended victim is as likely to be killed as released unharmed.
In the UK, there are laws governing the use of snares and they must only be employed to capture animals classed as pests such as rabbits and foxes. Snares cannot be used intentionally to catch birds, badgers or deer – although it is quite possible that they will. Only free‐running snares can be used and they must be inspected at least twice a day: once soon after sunrise and once at dusk. Failure to do so results in prosecution under the Animal Welfare Act 2006. Because snares are indiscriminate, they should not be located close to houses where they might catch domestic cats and dogs.
The presence of a snare, its type, and location are all obvious examples of forensic evidence. Similarly, an animal caught in a snare and its condition provides further evidence of whether snaring was taking place illegally. The person setting snares usually checks them periodically (even if not at the legal minimum intervals). Therefore, a snare can be observed discretely from a distance until they turn up. Snares can also be tested for human DNA to link a person to illegal snaring. Because snares consist mostly of thin wire, it may be impossible to retrieve fingerprint evidence from them. However, fingerprints and fibre evidence may be present on the object to which the snare is attached.
11.6.3 The Use of Spring Traps for Poaching
Spring traps are designed to capture and kill small animals such as rats, stoats, and grey squirrels (Figure 11.1). Unfortunately, like snares, they are indiscriminate and will snap shut on any organism that steps into them. Spring traps are usually made from metal and consist of two spring‐loaded jaws and a central pressure plate. When an animal steps on or otherwise triggers the pressure plate it releases the spring that holds the jaws apart and these then snap together. Either the animal is then crushed to death or its limb is held firmly in the grip of the jaws. Sometimes the traps are baited or bait is placed in the vicinity to attract the target animal. Because of their potential to cause suffering and the risk they pose to non‐target animals, the Spring Traps Approval Order 1995 governs the use of spring traps in England and Wales. Similar laws operate in other countries. So‐called ‘break back traps’ can be used against rats and mice in domestic settings whilst ‘mole traps’ are designed for placing within mole burrows. The traps should never be placed in areas in which another animal is likely to step on them. They should therefore be employed in natural or artificial tunnels or in locations such as cupboards or rooms which pets, domestic animals, and wild birds cannot gain access. It is illegal to set a spring trap on open land or on the top of a post, although gamekeepers sometimes do this and others who wish to kill birds of prey. In some countries, large spring traps, sometimes referred to as gin traps, are used to capture animals such as lions or coyote. Gin traps are large spring traps and may have toothed jaws that dig into the flesh – they can virtually sever a limb. In the 1700s, large gin traps were employed by landowners to capture poachers. They are often tethered to a tree or other solid object to ensure the animal (or human) does not escape. Their use became illegal in the UK in 1958 although they can still be purchased on line as antiques.
Forensic evidence comes from the physical nature of the spring trap and its location. It is also possible to link a person to a spring trap from fingerprints and DNA evidence. A bird of prey that is killed in an illegally set spring trap will usually be disposed of a distance away to avoid bringing attention to the trap. The animal often dies of shock before the trap setter returns to check his trap. Any bird of prey that is found without an immediately obvious cause of death (e.g. it suffered trauma from a collision) should be checked for signs of limb damage because this would suggest it had been caught in a spring trap.
11.7 Bushmeat
‘Bushmeat’ is the term given to the meat of wild terrestrial animals that are not normally considered ‘game animals’. Game animals are those such as red deer (C. elaphus), moose (Alces alces), wild boar (Sus scrofa), pheasant (Phasianus colchicus), and red grouse (Lagopus lagopus scotica) that are hunted for sport as well as for meat. The hunting of game animals is regulated and there are strict quotas on the number of animals that can be killed and where, when, and how animals are hunted. By contrast, the hunting of bushmeat species is unregulated and includes a huge variety of animals ranging from cane rats (Thyronomys spp.) to gorillas (Gorilla spp.). Many of these animals have been hunted for generations by local people either for their own consumption or for sale in the village market. If this practise remains ‘low key’ it need not harm the wildlife population – indeed, it may be beneficial because it makes the local people more aware of the need for conservation. However, in recent years there has been a large increase in the killing of animals for bushmeat. This is because of the same local and international factors that drive much of the illegal trade in wildlife (Table 11.1).
Table 11.1 Factors driving poaching and the illegal trade in wildlife.
| Increases in human population Increased local market Increases in affluence among the general population Increased international market Availability of high velocity firearms Increased access to remote areas through logging roads Availability of rapid motorised transport (e.g. 4 × 4 vehicles) Cheap air travel and airfreight transport Improved communication (mobile phones and internet) Corruption Lack of resources to implement regulations |
Karesh et al. (2005) estimated that the African bushmeat trade is worth several hundred millions of dollars (US) per annum and 4.5 million tonnes of bushmeat is harvested every year from the Congo basin alone. The factors driving the trade in bushmeat are similar to those involved in other aspects of illegal wildlife trafficking. The human population is increasing and that means more mouths to feed and more people in need of an income. Villagers in all parts of the world have always exploited the local wildlife as a source of food and for trade, and this will continue until there are viable alternative sources of food and income. A major difference, however, is that many hunters now have high‐powered rifles rather than bows and arrows. This means that more prey can be killed more quickly. Economics and societal factors are seeing more people move from villages to the cities, both in their own country and overseas. For those who are fortunate, their movement is associated with an increase in income and some of this is used to buy a ‘taste of home’ or the high status foods that they previously could not afford. This fuels the sale of bushmeat on both the national and international market. This is further facilitated by ownership of mobile phones and the internet that can put traders, intermediaries, and purchasers in contact with one another. The animals being killed are not just the ‘obvious’ large mammals. In Ghana, it is estimated that 128 000 fruit bats (Eidolon helvum) are killed every year for food. This is not only decimating the bat population but is also having harmful consequences for those plants that are pollinated and/or dispersed by bats (Kamins et al. 2015). Logging roads, motorised transport, and air travel now mean that previously remote regions that took weeks to reach can now be accessed from the capital cities of the world within 24 hours. The movement and sale of bushmeat is also facilitated by widespread corruption in many developing countries and a lack of resources and priorities in industrialised countries. This results in little effort being made to combat a trade that contravenes the laws in all of them. Although the term ‘bushmeat trade’ is most commonly discussed in relation to African animals, there is a similar problem in parts of Asia and South America.
Much of the trade in bushmeat is geared towards local consumption, but as the potential profits increase it is starting to involve organised criminal gangs: a single suitcase of bushmeat may have a street value of up to £1000 in the UK. Consequently, bushmeat is being seized with increasing frequency at airports on its way to immigrant communities. According to Chaber et al. (2010), somewhere in the region of 273 tonnes of bushmeat is imported illegally into Paris Charles de Gaulle airport every year on Air France carriers. It is probable that large amounts are also entering on other carrier networks.
Bushmeat is seldom stored and transported in accordance with food hygiene regulations and therefore poses a risk of food poisoning. There is also the risk of the transmission of zoonotic diseases such as the nematode Trichinella spiralis, the bacterium anthrax (Bacillus anthracis), and a host of zoonotic viral infections. For example, simian foamy virus (SFV) has been detected in primate bushmeat illegally imported into the USA (Smith et al. 2012). SFV can be transmitted from non‐human primates to humans, but its importance as a human pathogen is uncertain. However, SFV is a retrovirus and when a certain other retrovirus, simian immunodeficiency virus (SIV), crossed the species barrier, it became human immunodeficiency virus (HIV).
When the authorities seize a consignment of bushmeat, it seldom includes helpful morphological evidence such as teeth or skin. Furthermore, the suspect will claim the meat originated from a domestic species such as a cow or pig. Provided DNA can be extracted from the sample, it is usually possible to quickly confirm whether the suspect is telling the truth. However, if he is lying, then it is more difficult to determine from which animal the meat originated. To facilitate identification of African bushmeat, Gaubert et al. (2015) developed a reference database using sequences of mitochondrial genes for COI, cytochrome b, 12S rRNA, and 16S rRNA for 59 of the most commonly exploited African bushmeat species. They then developed a ‘DNA typing decision pipeline’ that allows one to compare sequence data from an unknown sample to identify which animal it had originated from.
11.8 Ivory
Ivory is another word for dentine – the main component of all mammalian teeth. However, most animals have relatively small teeth and consequently the majority of objects crafted from ivory are derived from the large tusks of elephants (e.g. Loxodonta africana), hippos (Hippopotamus amphibius), walruses (Odobenus rosmarus), and narwhals (Monodon monoceros). Some ivory is also derived from the tusks of mammoths (Mammuthus primigenus) that are retrieved from the permafrost regions of Siberia and Alaska. The trade in mammoth ivory is legal in many countries and large amounts are recovered each year in Siberia (36 tons were exported into the US alone in 2007). In Asian elephants (Elephas maximus), only the male has tusks and poaching has resulted in dramatic changes in the sex ratios of their populations. Some female Asian elephants have rudimentary tusks, whilst many males in certain populations (i.e. Sri Lanka) lack tusks.
11.8.1 The Trade in Ivory
Ivory has been coveted, carved, traded for millennia by both Western and Eastern societies (Figure 11.2a). Many people consider ivory objects innately beautiful from an artistic perspective but, in Asian societies, they also convey status and an investment equivalent to gold in terms of its potential for growth (Harvey et al. 2017). High‐quality elephant ivory is extremely valuable: in 2014, raw ivory traded for around US$ 2100 per kg in China. When it is considered that the two tusks (modified upper incisors) of an adult male African elephant (L. africana) can together weigh over 80 kg (an adult female's tusks weigh in the region of a more modest 18 kg), the existence of a large illegal market is hardly surprising. Indeed, although African elephants with combined tusk weights of over 200 kg existed in the recent past, currently such remarkable individuals are shot long before they reach their full potential.
Figure 11.2 (a) Carved elephant ivory. The shape and a size of the tusk identify it as elephant ivory. However, chemical and/or DNA analysis would be required to determine whether it derived from an African or Asian elephant. (b) Store selling mammoth ivory at a German Christmas market.
Today, the majority of ivory is ultimately consumed in China, although it may pass through several countries to get there. For example, between 2010 and 2015, the UK was the world's largest re‐exporter of legal ivory – most of this was in the form of antiques and most of it was en‐route to Asia. Because of the bad publicity, in October 2017 the UK government announced plans to ban the export of ivory of all ages. The illegal ivory trade is much larger than the legal trade, although by its nature it is difficult to obtain accurate figures. To give an indication, in 2014, the Hong Kong customs burnt 32.6 tonnes of raw ivory tusks that they had seized over the previous 11 years. Similarly, in 2016, in Kenya, 95.3 tonnes of confiscated elephant ivory were burnt. This ivory came from seizures that had been stockpiled over several years. It can be certain that in both cases the amounts of ivory that were not seized were many times bigger than this.
The illegal trade in walrus ivory and narwhal ivory does not capture the headlines in the same way as that in elephant ivory, but there is concern that it could become a problem in the future. The populations of both walruses and narwhals are not yet under threat, but this could quickly change. Currently, only native Inuit are permitted to hunt both species in Canada and Greenland and there are strict quotas. However, managing these quotas is difficult and with ground narwhal tusks reportedly selling for around £7000 per kilogram in Japan, the temptations will be huge. The gullible believe that ground narwhal tusks are efficacious for the treatment of a range of conditions including fevers and venereal disease.
In 1990, a global ban on the trade in elephant ivory was instigated by CITES. This was sufficiently effective to allow the elephant populations in some parts of Africa (e.g. Botswana) to recover from the brink of extinction. However, elephant poaching remains a serious problem. At the time of writing, the situation regarding the conservation of elephants and the trade in ivory is complicated. In most countries in which elephants are found, they are on Appendix I of CITES, but in Botswana, Namibia, South Africa, and Zimbabwe, they are on Appendix II. However, an annotation prohibits trade in ivory from these four countries. In Thailand, the sale of Asian elephant ivory was still permitted in 2017, but not its export by tourists. The sale of ivory from African elephants is prohibited in Thailand, although conservation organisations claim that the legal trade in Asian elephant ivory is used as a cover for its sale. Distinguishing between ivory from Asian and African elephants is therefore important in this context. There is currently a programme to use DNA techniques to identify individually all the domestic Asian elephants in Thailand and thereby have a means of tracing the ivory that originates from them. Although there is a ban on the international trade in elephant ivory, the sale of antique ivory is permitted in many countries. The definition of ‘antique’ varies, but generally relates to worked ivory that was created before 1 June 1947. However, in some countries, ‘antique ivory’ means at least 100 years' old. In 2016, CITES Parties agreed that the domestic market in ivory should also be closed – the USA and France have already enacted this and China banned all ivory processing and sales on 31 December 2017.
11.8.2 Identification of Ivory from its Morphology
Whole tusks can usually be identified as belonging to a particular species based on their gross morphology (Figure 11.2a), but once they are cut up and carved, it is much more difficult. A person accused of selling elephant ivory or smuggling an ivory object through customs will usually claim that it is not ivory, came from a mammoth or non‐protected species, or is antique ivory and therefore legal.
The trade in mammoth ivory is currently legal in many countries (Figure 11.2b). However, there is a call for it to be banned because it facilitates elephant ivory being sold and trafficked among shipments of mammoth ivory. The sale of mammoth ivory is currently banned in some US states (e.g. New York and California) and India. Mammoth ivory can sometimes be distinguished from elephant ivory based on coloration: mammoth ivory often has a brownish or blue‐green discoloration owing to iron phosphate deposits and these are lacking in Asian and African elephant ivory. However, mammoth tusks that were preserved in ice can retain their white coloration and they are then difficult to distinguish from elephant ivory without a more detailed examination.
A relatively simple method of distinguishing elephant and mammoth ivory is to prepare polished cross‐sections of the tusks. These reveal a series of markings called Schreger lines in the dentine and where these lines overlap, they form a crosshatch pattern. In the outer region (i.e. adjacent to the cementum) the angles formed where the lines overlap are mostly acute (<90°) in mammoths but obtuse (90–180°) in African and Asian elephants. However, there is a degree of overlap in the range of 90–115° and therefore the average of several measurements should be used. This method is not suitable for carved objects.
Antler carvings can have a superficial similarity to those made from ivory. If the outer surface of the antler is retained, then the object will have a dark brown, wrinkled surface unlike the smooth surface of ivory. When viewed in cross‐section, an object made from bone will exhibit a spongy middle and a harder (bone) outer region, whilst ivory would be uniform in consistency. Genuine ivory will have striations along its length, but these are lacking in antlers.
Bone carvings are hollow because of the loss of the marrow and therefore usually have an end cap. By contrast, ivory carvings are solid and they are also heavier than bone objects of a similar size. In addition, the Haversian canals that are manifested as black or brown pits, dots, and irregular lines permeate bones; these are not found in ivory.
Modern plastics can be manufactured to appear extremely similar in appearance to genuine ivory and may even have a similar density. Genuine ivory that is exposed to Long Wave Ultra Violet (LWUV) light fluoresces with a faint to strong blue light: the whiter the ivory, the stronger the fluorescence. Plastics exposed to LWUV tend to fluoresce dully or in odd colours, such as mauve. Sometimes powdered ivory or bone is added to the plastic and this results in an apparently ‘normal ivory’ fluorescence. Plastic items cannot replicate the patina of genuine ivory and usually have a uniform appearance or obvious streaks where dye was injected. Natural ivory also has complex growth patterns, whilst in manufactured items any patterning is uniform. In poor‐quality imitation ivory, there will be an obvious seam line and there may be trapped bubbles.
11.8.3 Molecular Identification of Ivory
One can confirm which species a tusk or ivory object has originated from by extracting DNA. For example, Kitpipit et al. (2017) describe an assay based on the identification of species‐specific mitochondrial single nucleotide polymorphisms (SNP) in the cytochrome b gene that will identify ivory and distinguish African from Asian elephants. Molecular analysis is not a reliable means of identifying mammoth ivory because, although it can be done, the DNA is often severely degraded and may be absent entirely.
11.8.4 Stable Isotope Identification of Ivory
The stable isotope profile of ivory cannot prove species identity. However, it excludes possible ‘sources’ if DNA cannot be isolated from the specimens. For example, the profile from walrus ivory differs from elephant ivory. This is because elephants are terrestrial and feed on vegetation, whilst walruses live in the sea and their diet includes bivalves. Similarly, profiles from mammoth ivory are distinct from those of extant elephant species. This is because mammoths never lived in the regions currently occupied by elephants and they had a different diet.
Because the stable isotope composition of an animal is indicative of its diet and the local geochemistry, one can determine the region from which it originated. This procedure is known as ‘isotopic fingerprinting’. Ziegler et al. (2016) used this approach to identify the region of Africa from which an elephant tusk came. There is some variation in the stable isotope profile, both within samples taken from an individual elephant and between elephants living in the same locality. However, by combining isotopic fingerprinting with molecular analysis (see case study above), it is possible to identify the provenance of ivory with some confidence.
11.8.5 Spectroscopic Methods for the Identification of Ivory
Although DNA and stable isotope fingerprinting are both extremely useful techniques, they currently suffer from being expensive and there is a considerable ‘lag time’ between sample discovery and the availability of test results. There is therefore a need for techniques that are cheaper and can give a rapid result under field or ‘near field’ conditions (i.e. the samples do not have to be sent to a central processing laboratory in the capital city). It is possible that this could be provided by spectroscopic techniques.
Visible (400–800 nm) and near infrared (800–2500 nm) spectroscopy are effective means of discriminating between mammoth and elephant ivory (Shimoyama et al. 2004). These methods are non‐destructive and can identify hippopotamus and sperm whale ivory. Another non‐destructive test is X‐ray fluorescence (Buddhachat et al. 2017). This has the advantages of not requiring any sample preparation and of the availability of hand‐held devices. Therefore, rapid testing is possible in field situations. However, X‐ray fluorescence is subject to misclassifications and therefore further confirmatory tests would be required if evidence was required for a prosecution.
11.8.6 Determining the Age of Ivory
As long as the sale of antique ivory is permitted, it will remain important to determine the age of ivory. In addition, it is known that ivory is being stockpiled in some countries in the hope that the ban on trading will be relaxed in the future. As ivory ages, its patina changes from white to creamy white and yellow. Unscrupulous ivory traders therefore soak modern ivory in tea in order to make it appear older than it actually is.
The age of ivory can be determined from the levels of strontium‐90 and carbon‐14, as well as the ratios of thorium‐228 and thorium‐232 (Brunnermeier et al. 2012). Obviously, because mammoth ivory is thousands of years old, carbon dating provides absolute certainty of its provenance. However, this is expensive and time‐consuming and not something that can be done on a routine basis. For example, although Hong Kong is a major importer (and exporter to mainland China) of both legal and illegal ivory, in 2017 it was still sending abroad all its samples for carbon dating (Wong 2017).
11.8.7 ‘Mermaid Ivory’
Mermaid ivory is one of those wonderful misnomers in that it is neither ivory nor derived from a mermaid. In fact, it refers to the bones of the Steller's sea cow (Hydroamalis gigas). Appropriately, Steller's sea cow was no more a marine cow than it was a mermaid, but instead a close relative of the dugong (Dugong dugon). It was a huge animal that could grow to 9 m in length and weigh around 10 tonnes. It used to live in the seas around Alaska until it was hunted to extinction in around 1768. The bones can still be found and because the animal is extinct, there are no restrictions on their trade. The bones are carved into knife handles, statuettes, and other trinkets. However, there is a concern that, as with mammoth ivory, the legal trade in ‘mermaid ivory’ is being used as a cover for the trafficking in the bones of protected species of marine mammals, such as whales and dolphins.
Although Steller's sea cow has been extinct for over 200 years, one can extract DNA from the bones. Crerar et al. (2017) used Sirenia‐specific (i.e. dugong and manatees (Trichechus spp.)) primers to isolate the mitochondrial D‐loop_2 region. These fragments were then amplified by PCR. Therefore, only D‐loop_2 segments from Steller's sea cow and other sirenian mammals were targeted and sequencing could then distinguish between the species. Therefore, an initial screening test could determine whether a bone was likely to come from a Steller's sea cow. After PCR, DNA electrophoresis would demonstrate whether the primers had worked: if they had, there would be a line in the gel. A positive reaction would indicate that the bone came from a sirenian and this would almost certainly be a Steller's sea cow, because no sirenians currently live in the Alaskan region. If the reaction was negative, there would be no line and therefore the bone must have originated from another animal or the DNA was too degraded and further tests would be needed.
11.9 Antlers
Antlers are bony outgrowths from the frontal bone of the skull. They are a characteristic feature of many deer species (Cervidae). Giraffes are often said to have antlers, but these are more correctly referred to as ‘ossicones’ since they are formed from ossified cartilage rather than bone and they remain covered by vascular skin throughout life. Antlers usually only develop in male deer and they are used for display and fights with rival males. Female reindeer (Rangifer tarandus) develop antlers, albeit much smaller than those of the males. Antlers form anew every year and whilst growing they are covered with vascularized tissue called ‘velvet’. Once antlers are fully formed, their blood supply ceases. Consequently, the velvet dies and is sloughed off. The antlers are then hard, dry, and ready for combat. After the mating season finishes, the antlers fall off and new ones form.
The size and shape of antlers is often indicative of the species of deer. Within some species, the size and complexity of the antlers is also affected by age. Antlers that fall off naturally at the end of the mating season have a rounded base. In some countries (and states of the USA), it is illegal to collect naturally shed antlers, so one must be aware of the local rules. If the antlers are attached to the skull plate then the animal must have been killed or died of natural causes. It is usually illegal to possess these antlers, unless there is documented proof to indicate that the animal was lawfully killed. The presence of velvet and/or tool marks (e.g. saw cuts) at the base of the antlers indicates that they were forcibly removed at the time of death.
Whole antlers are taken by hunters as trophies and there is a market for antlers as artistic objects (much of this comes from shed antlers, farmed deer, or legally shot game animals). There is, however, a much bigger market for antlers for use in Asian traditional medicine. Deer farms exist in several countries to meet this market (Figure 11.3), but this has not curbed the problem of deer being poached for their horns. For example, in Mongolia the red deer population declined by 92% between 1986 and 2004, partly as a consequence of the poaching of male deer for their antlers (Zahler et al. 2004).
Figure 11.3 Deer farm in the Ukraine. These deer are kept primarily for their antlers.
It is the young antlers still covered in velvet that are used in Asian traditional medicine and in particular those from the Red deer (C. elaphus) and Sika deer (Cervus nippon). These antlers sell for over US$ 1000 per kg. The antlers allegedly stimulate male sexual activity and bring about rejuvenation among a wide range other properties. In Western societies, deer antlers are increasingly used in ‘alternative medicines’ and as a supplement for sports performance.
Deer antlers are usually cut into thin slices for use in traditional medicines. This leaves few morphological species indicators. Consequently, there is a lot of fraud in which antlers deemed to be from low value species are substituted. For example, traditional medicine practitioners consider reindeer antlers to have few beneficial properties. Whether this is genuine or because men fear that using antlers from a female animal would compromise their virility is uncertain. A variety of molecular techniques can identify the species of deer from antler slices and medicines containing antler products (Jiang et al. 2017) and these tests can be used to detect illegal trafficking.
11.10 Horns
There are three types of horn: hollow horns, pronghorns, and midline keratin fibre horns.
11.10.1 Hollow Horns
Hollow horns are characteristic of cattle, sheep, goats, and many (but not all) of the cloven‐hooved ungulates. In some species, both males and females have horns (although the males' are usually larger) but in others, only the male has them. The horns are used for defence, competition, grooming, thermoregulation, and (sometimes) an aid to feeding (e.g. digging up roots). They are formed from bony outgrowths of the frontal bone of the skull but unlike antlers, they are never shed. In addition, they are covered with a layer of keratin that is formed by the epidermis. If a horn is damaged or lost, it does not regrow. After an animal dies, the keratin layer separates from the underlying bone and hence these horns are known as ‘hollow’. This allows the keratin sheath to be fashioned into a drinking vessel or a musical instrument (i.e. a ‘horn’).
The size and shape of a hollow horn is a good indication of which species it comes from. Horns are prized as hunting trophies and this has driven several species such as the Oryx (Oryx leucoryx) and the argali (Ovis ammon) close to extinction. The import and export of horns from protected species of wild animals is governed by CITES legislation and they are usually identified from their morphology, although DNA provides confirmation.
11.10.2 Pronghorns
Pronghorns are found in only the pronghorn antelope, Antilocarpa americana. This species lives in western and central states of the USA, with populations also found in Canada and Mexico. It is allegedly the second fastest land animal, after the cheetah, with a top speed of around 100 km hour−1. The pronghorn is not a true antelope and is currently placed in its own family, the Antilocapridae. The horn consists of a permanent bony outgrowth of the frontal bone of the skull, but the keratin layer that covers this is shed each year. On each horn, the keratin layer forms a single spur (prong) that lacks a bony core. This spur is shed with the rest of the keratin each year. The horns can grow up to 50 cm in length in the males, but seldom reach 10 cm in the females. The horns are therefore distinctive enough to be recognised based on their morphology. Although the population has declined, the pronghorn is not covered by CITES legislation in most states in which it occurs.
11.10.3 Midline Keratin Fibre Horns
Midline keratin horns are found only in rhinoceroses, of which there are five species: the African white rhinoceros (Ceratotherium simum), African black rhinoceros (Diceros bicornis), Indian rhinoceros (Rhinoceros unicornis), Javan rhinoceros (Rhinoceros sondaicus), and the Sumatran rhinoceros (Dicerorhinus sumatrensis). These are further sub‐divided into sub‐species. Both male and female rhinos have horns. Rhino horns do not contain any bone and are composed of long strands of keratin formed by the epidermis from the growth region at their base. Midline keratin fibre horns are therefore an integral part of the skin. However, they lack a blood supply and, like hair, are composed of dead cells (Figures 11.4a and b). The horns are permanent but they get knocked off during fights. The base of the horn will then bleed but the horn regrows. In an attempt to reduce poaching, some game farms in South Africa inject a combination of a pink dye and pesticides into the horns of their rhinos. The pink dye warns poachers that the horn is no longer valuable. The dye cannot be removed and is detectable by airport scanners. The pesticides are not present at lethal levels, but would make someone consuming them unwell. Rhino horns lack a blood supply and therefore the animal absorbs neither the dye nor the pesticides. However, capturing and treating rhinos is a stressful (for all concerned) and expensive business, and therefore it is only possible on a local basis.
Figure 11.4 African white rhinoceros Ceratotherium simum: (a) the horn is rough and composed of keratin fibres; (b) thermal camera image of an adult rhino. The horn appears blue because it lacks a blood supply and is therefore much colder than the rest of the animal.
The population of all rhino species is critically endangered because of poaching and they are listed as CITES Appendix I. This is because of the enormous value placed on rhino horn in Asian Traditional Medicine and the main markets are in Vietnam and China. Many believe that rhino horn is effective in treating fevers and a recent myth has arisen that it can cure cancer. There are contradictory reports about whether rhino horn is an aphrodisiac: it is not considered as such in Chinese Traditional Medicine texts. It is therefore uncertain whether reports of wine laced with rhino horn being sold in Vietnam are genuine. Conservation organisations now avoid publicising current prices of rhino horn, because of the fear that it stimulates the trade. However, it is thought to have peaked at around US$ 65 000 per kg in 2012 and therefore worth more per unit weight than gold (in 2017, gold sold in the region of US$ 41 000 per kg). The front horn of a fully‐grown white rhinoceros weighs an average of 4 kg, so it is easy to see why poaching is so attractive. The horns of the Asian rhinos are much smaller (0.27–0.72 kg), but this has not made them any less vulnerable to poaching. The price of rhino horn has reportedly declined since 2012, but remains high. Therefore, not only are wild animals being killed for their horns, but also those in zoos. After a European wide spate of thefts, museums are now replacing the horns on mounted specimens with replicas.
Whole rhino horns and large fragments of them can be identified from their gross morphology. However, in some countries, the fraudulent sale of fake rhino horns fashioned from cattle horns is common and some of these reproductions are convincing. A genuine rhino horn is composed of solid keratin, has a rough texture, and has a concave depression at the base where it attaches to the head. By contrast, a cattle horn is hollow or has a bony core, and does not have a concave base. In many countries, the marketing of any item as being (or containing) rhino horn carries the same penalties for both real and fake material.
The trafficking of rhino horn is usually undertaken by organised criminal gangs and aided by corrupt officials. Smuggling by diplomats is allegedly common, since they (and their family) do not undergo security checks at customs, unless there are serious grounds for suspecting that their luggage contains prohibited material. North Korean diplomats have been implicated in many instances of ivory and rhino trafficking: this is because it is a good source of foreign currency for the regime.
Sniffer dogs can detect the presence of rhino horn in luggage, but one needs separate dogs for different substances. For example, a dog is trained to detect drugs or explosives, but not both. It is not feasible to employ a range of sniffer dogs at every customs post. The volatiles emitted by rhino horns are detectable by two‐dimensional gas chromatography – time‐of‐flight mass spectrometry (GCxGC‐TOMS) (Ueland et al. 2016). The method is quick and sensitive enough to distinguish horns from white and black rhinos. However, it was tested using pure rhino horns and, at the time of writing, more work was required to assess its suitability under field conditions; for example, whether it can detect rhino horns where volatiles from other sources are present. IR and FT Raman spectroscopy might be useful in identifying rhino horn, but there is currently little information on this.
Molecular tests can identify rhino horn and demonstrate its presence in medicines and sculptures. Nuclear STR and sex markers can facilitate the identification of individual rhinos and a DNA database is now available for African rhinoceroses that has been successfully used to prosecute poachers (Dicks et al. 2017; Ewart et al. 2018; Harper et al. 2018).
11.11 Bear Bile
Over the centuries, Chinese and Asian Traditional Medicine has incorporated the bile of many animals, including, fish, frogs, snakes, birds, cattle, pigs, and goats. Even human bile was used in the past. Concoctions containing bile are prescribed for a range of illnesses from liver disease to gynaecological conditions and skin burns to piles. Traditional Medicine pharmacists consider bear bile (Xiong Dan or Fel Ursi) the most efficacious of the various biles and it has always been highly prized (Wang and Carey 2014). Bear bile, unlike many traditional medicines, is often taken alone either dissolved in milk, taken orally as a pill, or rubbed on topically (Figure 11.5).
Figure 11.5 Gift package of bear bile for use as Chinese Traditional Medicine.
Bear bile, like that of other mammals, contains a mixture of bile acids, bile pigments, amino acids, phospholipids, fats, and trace metals. Allegedly, the bile acids are responsible for the medicinal properties. The structure of the bile acids varies between species. For example, in bears, there is a high level of ursodeoxycholic (also called ursodiol). Although synthetic ursodiol has been available for many years, and is sold under trade names such as ‘Actigall’ and ‘Ursosan’, it has not yet been adopted as a suitable replacement for the ‘real thing’. Similarly, a variety of herbs have been proposed as bear bile substitutes (Appiah et al. 2017), but they are not yet widely used.
In the past, bear bile was sourced from hunting, but as the population of bears declined and the human population (and hence demand) increased, this source could no longer meet requirements. Consequently, in the 1980s, a large number of bear farms were set up in mainland China and, to a lesser extent, Laos, North Korea, and Viet Nam. The farms reared the Asiatic Black Bear, Ursus thibetanus, under horrific conditions. The bile was extracted from the bears via a catheter and fluid was collected daily either by gravity or by suction with an unsterilized syringe. Not surprisingly, the lifespan of the bears was short, about 5 years, but during this time, a bear would yield as much bile as 220 wild bears. Production was so successful that there was a surfeit of bear bile entering the market. This resulted in new products such as bear bile throat lozenges, bear bile shampoo, and bear bile tea. However, it did not reduce the pressure on the hunting of wild bears for their bile. As is so often the case, people usually believe that ‘wild’ must be better than farmed, and the same goes for bear bile. Consequently, an increasing number of bears around the world are killed just for their gall bladders. Evidence of this is obvious when the body of a dead bear is found with its abdomen slit open but there is no attempt to skin it or take the paws (a delicacy in some Asian communities).
Following campaigns by animal conservation and protection agencies, both outside and within China, many bear farms have shut down and the intention is to close the remainder. However, there are conflicting reports about the true extent of the closures. In addition, there remains a considerable problem with the illegal sale of bear bile products around the world and with the trafficking of bear gall bladders to Asia. There is also a lot of fraud and mislabelling. For a successful prosecution in the UK, it only needs to be demonstrated that the owner, seller, or trafficker claims or thinks that a substance in their possession contains bear bile – whether it does is immaterial to the sentence. Obviously, it helps the prosecution if bear bile is proven to be present in the evidence.
After a gall bladder is removed from an animal, it is dried for ease of transport and storage. It is then difficult to distinguish a bear gall bladder from that of another animal. Consequently, it is easy to hide genuine bear gall bladders among those of other species. In addition, the use of gall bladders of domestic animals in Chinese Traditional Medicine has a long history and is legitimate. Although one can identify ursodeoxycholic acid by conventional analytical techniques, such as HPLC, these are time‐consuming. In addition, ursodeoxycholic acid occurs in the bile of other mammals and therefore it is not diagnostic of bear bile. In a wildlife forensics scenario, it is extremely useful to be able to obtain a rapid ‘yes or no’ answer in the field (Table 11.2). Peppin et al. (2008) developed a dipstick‐style test that fulfils this need. It is a lateral flow immunoassay designed to detect bear albumin and it works on the same basis as many bedside rapid diagnostic tests used in human medicine. First, the liquid sample is placed on the conjugate pad at the bottom of the test strip. Within the conjugate pad are anti‐bear albumin antibodies that are labelled with latex that incorporates a blue dye. If bear albumin is present, it will bind to the antibodies. The sample then migrates up the test strip through capillary action. After a short distance, it meets the ‘test line’, where there are immobilised unlabelled anti‐bear albumin antibodies. Any bear albumin molecules will get stuck at this line. Because they are carrying the anti‐bear albumin antibodies that are in turn carrying the blue dye, this will show up as a blue line. Further up the test strip is the ‘control line’, at which there is an immobilised polymer that binds to latex. Therefore, anti‐bear albumin antibodies from the conjugate pad will get stuck here and because of the dye, this will show up as a line. This proves that the sample has migrated up the test strip. Two lines (lower and upper) means that the sample contains bear, one (upper) line means that the sample does not contain bear, and no lines means that the test has not worked. If the test is positive, then one can then arrange for further confirmatory tests.
Table 11.2 Why rapid field tests are useful in wildlife forensics.
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11.12 Musk Oil
Musk deer (Moschus spp.) were the original source of the musk used in perfume. Musk smells differently on different people and is described as ‘sensual, masculine, and earthy’. Nowadays, the import of natural musk oil is banned in most countries and reputable perfumers have used synthetic musk for many years. Indeed, synthetic musk was first synthesised as long ago as 1888 and named ‘Musk Bauer’ after its creator. Nevertheless, there remains a strong demand for natural musk oil for use in Chinese Traditional Medicine. Musk oil is incorporated into a variety of medicines and is allegedly useful for the treatment of depression, inflammatory ailments, and fever. In addition, it is not hard to find perfumes for sale on the internet that, purportedly, contain musk oil derived from deer and, of course, people willingly believe that this must be better than synthetic musk.
The taxonomy of musk deer species is currently uncertain, with some authors stating that there are four species and others six species (Yang et al. 2015). They are found over a wide geographical region from Eastern Russia to mainland Asia. All musk deer species have CITES protection: those in the Himalayan region are classed as Appendix I and those found elsewhere in Appendix II. Only the adult male deer produce musk that they use to mark their territories and attract mates. Peak musk production is associated with the breeding season (May–July). The musk is formed in musk pods that are located close to the penis. To meet the demand, musk deer farms have been established in China, although some reports state that these are not self‐supporting and are only able to function with frequent introductions of wild deer. Farmed deer can be caught and then it is possible to scoop out the contents of the musk pod without killing them. However, capturing and restraining deer is stressful for them and removing the musk should be done under anaesthetic. Not surprisingly, musk deer can die during this procedure, although some reports state that after extraction the male deer continue to grow and breed successfully. Farmed musk deer cannot meet the demand for musk and the high price of musk pods ensures that there is widespread poaching of wild populations. The wild deer are killed by shooting and snaring and their whole musk pod is cut out and dried. In Nepal, snare densities of 500–600 snares km−2 have been reported. Snares do not discriminate between adult male musk deer and females or young or other species of animal. Consequently, the poaching of musk deer not only devastates the musk deer population, but also results in serious ‘collateral damage’ to other species.
Dry musk pods weigh 30–40 g and resemble small grey‐brown beef burgers: they are about 5–7 cm in diameter and 2–3 cm thick. On their lower surface is a layer of abdominal skin that is covered in hair – the morphology of these hairs can be used as forensic indicators. The contents of a musk pod are initially semi‐fluid but turn dark reddish‐brown and powdery as they dry out: this material is known as ‘grain musk’. Adulteration of natural musk pods is reportedly widespread. This typically involves removal of some of the pod contents and their replacement with substitutes that vary from stones (to make up the weight) to pharmaceuticals (to provide a curative effect) – this could affect the results of analytical tests.
The presence of hairs and musk deer tissue on dry musk pods means that it is possible to extract DNA as a confirmatory identification test. Once the contents of a musk pod are distilled to extract the musk for use in medicines or perfume, it is no longer feasible to use morphology or DNA as forensic indicators. Nevertheless, one can identify whether a substance contains natural musk by analysing its chemical composition. A natural musk pod contains about 0.5% muscone (3‐methylcyclopentadecone‐1, CH3C15H27O) and this is entirely in the laevo‐isomeric form (L‐muscone). In addition, it also contains a small quantity of muscopyridine. By contrast, synthetic musk contains a mixture of laevo‐ and dextro‐isomeric forms of muscone (L‐muscone and D‐muscone). This analysis is typically undertaken using gas chromatography–mass spectrometry. The absence of D‐muscone and the presence of muscopyridine provide good evidence that the substance contains natural musk oil.
11.13 The Illegal Trade in Invertebrates
The killing of iconic species such as rhinos and elephants always grabs the headlines, but there is also a thriving illegal market for many invertebrates. As is the case for the illegal trade in ivory and rhino horn, this is resulting in species extinction and habitat destruction and is often linked to international criminal syndicates.
Invertebrates are traded both legally and illegally for their value as food (e.g. abalone, sea cucumbers), aphrodisiacs (e.g. abalone), decoration and jewellery (e.g. corals, starfish, butterflies), pets (e.g. scorpions), and by collectors (e.g. butterflies, Cape Stag beetles (colophon beetles)). Sometimes the name alone is sufficient to stimulate the interest of collectors. For example, the carabid beetle Anophthalamus hitleri would probably have survived living a life of blameless obscurity in the caves of Slovenia had not its discoverer named it in honour of Adolf Hitler. The adult beetle is small (~5 mm), brown, blind, and undistinguished‐looking, but its name means that it is popular with those who collect anything with Nazi associations. Specimens sell for over £1000 each and consequently beetle poaching is a problem. It is possible that over‐collection of A. hitleri will drive it to extinction.
In common with many wildlife crimes, local people are often responsible for the illegal collection of invertebrates from the wild. The internet facilitates the trade in small volume sales between collectors (or an intermediary) and individual collectors, whilst international syndicates are usually responsible for the trafficking of large volume sales to commercial organisations. For example, abalone from South Africa might be traded with other products such as rhino horn. In addition, the trade often involves the exchange of illicit substances and other criminal activity.
Large and colourful invertebrates are popular with collectors and sold for artistic decorations. Some specimens change hands for large sums of money and there is a worldwide market which, for the most part, is perfectly legitimate. Unfortunately, owing to habitat loss and excessive collecting from the wild, some species are declining rapidly. This increases their ‘value’, thereby stimulating further collecting and further declines in the population until the species enters an ‘extinction vortex’. Some collectors are not content with obtaining one or two representative examples of a species and amass as many specimens as they can. This causes further damage to small local populations. Consequently, an increasing number of invertebrates are achieving protected status.
The trade in butterflies exemplifies the problems (Table 11.3). Much of the trade is legal and in Papua New Guinea and elsewhere in the world, ‘butterfly ranching’ provides valuable income to indigenous communities. However, as always, there is also a large illegal trade of specimens collected from the wild. As with a lot of the wildlife trade, a great deal of it takes place in Asia. At one stage, Taiwan was known as the ‘butterfly kingdom’, because it bought and sold so many butterflies: as many as 30 million butterflies per year were being exported. Most of these butterflies were sold to Japan, but Europe and USA were also important markets. In recent years, the Taiwanese market has declined but elsewhere in Asia, particularly Malaysia, there is a big problem with the illegal export of rare and endangered butterfly species. Although the rarest butterfly species are protected by CITES legislation and therefore specimens require both export and import certificates, it is not difficult to find them for sale on the internet. For example, in 2016, a pair of Queen Alexandra's birdwing butterflies Ornithoptera alexandrae (which are found only in Papua New Guinea), were being offered for sale from Russia for US$ 5000. Whether the specimens and the permits they allegedly had were genuine is another matter, but this gives an indication of the money involved. For unscrupulous individuals, the ‘dark web’ offers an even larger hunting ground.
Table 11.3 The market for Lepidoptera.
| Volume | Value | Quality | Main Market |
| High | Low | Low | Commercial Asian mass market for decorations. The body is often discarded. |
| Low | High | High | Museums and specialist collectors in Europe, USA, and Asia. Details of time, place, and date of collection required. |
| Very low | Very high | High | Artistic and curio market in Europe, USA, and Asia. Rare species are prepared for artistic display. |
Control of the illegal trade in butterflies and other invertebrates largely depends on policing auction houses and internet sites for evidence of illegal activity, intercepting specimens in transit, ensuring that import and export certificates are genuine, and correct identification of specimens – and this usually requires traditional morphology‐based taxonomy (Table 11.3).
In the UK, the Wildlife and Countryside Act, 1981, names 14 species of insect and 13 species of other invertebrate. Under this act, it is illegal to capture, kill, or sell named species, except under licence. Possession of any of them, alive or dead, is considered illegal, unless they were acquired before the Act came into force or under licence. Examples include the mole cricket Gryllotalpa gryllotalpa, the large Blue Butterfly, Maculinea arion, the swallowtail Butterfly, Papilio machaon, the medicinal leech, Hirudo medicinalis, and apus, Triops cancriformis.
11.14 Future Directions
The cost of molecular biological techniques is likely to decrease in future years whilst their speed will increase because of the expanding demand for cheap, quick, and sensitive methodologies. Consequently, the use of molecular methods for the identification of both species and individual animals is likely to become more widespread as their use becomes financially acceptable. For example, Beltramo et al. (2017) describe the use of a DNA biochip kit (Meat Low Cost and Density Array kit (Chipron GmbH, Germany)) capable of detecting the presence of 24 domestic animal species at the same time. This kit works by sequencing the 16S rRNA mitochondrial gene and could be adapted to screen for the presence of a wide range of animals. Certainly, increasing use could be made of genetic markers to identify illegal trade in organisms such as abalone, scallops, and lobsters.
An alternative approach would be to develop more dipstick style tests, such as the one available for bear bile. These types of test are widely used in human medicine as ‘point of care’ tests, so the technology is available. One could also test for the presence of two or more species by incorporating two or more antibodies and two or more ‘test lines’.
Stable isotope analytical techniques hold great promise for determining the geographical origin of all sorts of biological material, from bones to illegal drugs. Once reliable databases become available, these techniques will undoubtedly be used more frequently. Similarly, stable isotopes could be used to establish whether an organism was collected from the wild rather than being raised in captivity or cultivated. This is particularly relevant for distinguishing meat derived from game animals raised in captivity on game farms from that from animals that were poached in the wild. Similarly, in the exotic pet trade, it could differentiate between captive born and animals caught in the wild.
The use of Fourier‐transform infrared spectroscopy (FTIR), stable isotopes, and other analytical techniques, such as e‐noses, is likely to increase. For example, e‐nose technology could prove useful for detecting the presence of abalone and other shellfish, as well as rhino horn and ivory. Hand‐held e‐nose devices, possibly linked to mobile phone apps, would be particularly useful in field situations and at customs points in airports, etc. Total reflection X ray fluorescence (TXRF) is an effective means of determining the levels of trace elements (e.g. carbon, nitrogen, oxygen, iron, zinc), as well as potential toxins such as mercury and lead (Ribeiro et al. 2014). TXRF could be particularly useful for marine organisms, such as abalone and shellfish.