Introduction
The African lion,
Panthera leo, has, along side many of the world’s megafauna, become threatened with extinction over the past century (Ripple et al.
2014; Bauer et al.
2015a). Lion populations are estimated to have declined by approximately 43% over the past 21 years (Bauer et al.
2015b) with an estimated 32,000 remaining across Africa, while lion range has declined by 75% over the past 50 years (Riggio et al.
2013). Persecution, loss of prey and loss of habitat are the primary drivers of these declines (Bauer et al.
2015b). Lions are regularly killed in retaliation of livestock depredation, a pressure that is expected to rise with Africa’s growing cattle herds (IUCN
2006; Hazzah et al.
2014). Widespread illegal bushmeat hunting is responsible for decimating prey populations across Africa, thus reducing habitat suitability for lions (Lindsey et al.
2013) as well as impacting lions directly through mortalities as by-catch in wire snares set for prey species (Becker et al.
2013). Unsustainable trophy hunting limits lion populations (Loveridge et al.
2007) and can cause population declines (Packer et al.
2009). In addition to each of these well documented drivers of lion population declines, the targeted poaching of lions for body parts for illegal wildlife trade (IWT) may emerge as yet another significant threat to the viability of lions, as it has for several other big cat species (Environmental Investigations Agency
2017). IWT is the estimated to be the fifth largest illegal industry globally, valued between US$5 and US$20 billion per year (Dudley et al.
2013; Wyler and Sheikh
2008). The trade ranges from small scale hunting in localised areas to commercial, transnational trafficking, both of which have major repercussions for targeted species conservation (Biggs et al.
2016). For example, the targeted poaching of tigers (
Panthera tigris) for bones and skins is one of the most significant threats to tiger population viability (Chapron et al.
2008; Dinerstein et al.
2007; Goodrich et al.
2008), as is the poaching of leopards (
Panthera pardus) for skins (Swanepoel et al.
2016; Raza et al.
2012), the poaching of snow leopards (
Panthera uncia) for skins and bones (Hussain
2003; Li and Lu
2014) and the poaching of jaguars (
Panthera onca) also for skins and more recently also for their teeth (Verheij
2019).
From 2011 to 2018 we studied the population ecology of lions in the Greater Limpopo Lion Conservation Unit (GLLCU) (IUCN
2006), identified as one of eleven ‘lion strongholds’ (Riggio et al.
2013). The GLLCU includes South Africa’s Kruger National Park, Zimbabwe’s Gonarezhou National Park and Mozambique’s Limpopo, Banhine and Zinave National Parks (IUCN
2006). We examined changes in abundance and cause of death for lions from the Mozambican portion of the landscape using primary and auxiliary data obtained from camera-trapping, spoor and call-up surveys, satellite GPS collaring exercises (Everatt et al.
2014,
2015,
2019) and information collated from National Park management. Our aim was to improve knowledge of the conservation status of this sub-population and to identify primary threats. Furthermore, we had
a priori concerns of an apparent emergence in the targeted poaching of lions in the region and sought to quantify the nature and relative extent of this threat.
Discussion
This study presents data indicating the emergence of a further threat to lion conservation - the targeted poaching of lions for body parts. This threat has the potential to have devastating impacts on lion populations mirroring the effects similar pressures have had on wild tiger populations (Chapron et al.
2008; Dinerstein et al.
2007; Goodrich et al.
2008) and may be having on jaguar populations (Verheij
2019).
In our study area, the targeted poaching of lions for body parts has likely contributed unsustainable rates of mortality and has become a direct threat to the viability of lions. These data clearly describe an important yet lesser known, additive threat to the conservation of wild lions and presents a novel contribution to the science of ecological responses of apex predators to changing anthropogenic pressures.
We estimated that the lion population of Limpopo National Park has declined by approximately 66% over 5 years. We acknowledge that due to low responses to call-up surveys the possible influence of stochastic variation cannot be dismissed as explanatory for the differences in the estimates of lion abundance in LNP between 2012 and 2017. However, we believe the additional data collected during the same period from the monitoring of focal study prides including a documented (i) 50% decline in the average minimum pride size, (ii) 89% decline in the minimum number of adult females per pride and (iii) change in the pride’s average sex ratios from 1.8 to 0.3 females per male in addition to the number of lions we documented killed within these pride’s home ranges, all provide additional evidence of a catastrophic decline in the abundance of lions in LNP.
The targeted poaching of lions accounted for 35% of known human caused mortalities across the landscape and 61% of lion mortalities in and immediately adjoining Limpopo National Park, far surpassing the combined effects of retaliatory killings of lions following livestock conflict events and deaths associated with by-catch from bushmeat poaching. We did not find a correlation between the targeted poaching of lions for body parts and retaliatory killings where body parts were harvested, suggesting body parts are taken opportunistically during the later. However, a new or rising demand for lion body parts could exacerbate motives to kill lions in the vicinity of communities and livestock, irrespective of livestock losses or a perceived threat of losses. Incentivizing the killing of lions by a demand for body parts could seriously undermine conflict mitigation efforts.
The impacts of these deaths on the lion population would extend beyond a simple decrease in abundance depending on the demographics of the lions killed. For instance, we recorded that in at least one case, and likely two cases, the entire pride of lions was killed, and six adult females were killed from the three focal study prides. The loss of adult pride members can disrupt pride structure and social cohesion, negatively impacting territorial defence and cub recruitment reducing population’s ability to withstand possible population disturbances (Loveridge et al.
2007,
2016). The loss of an entire pride or the loss of several or all of the breeding females from a pride can therefore have disproportionate impact on the viability of the sub-population compared to the loss of young dispersing males or females. As cooperative breeders, the reproductive success of a pride increases when three to ten lionesses are present, while female survival is reduced within prides containing only one to two lionesses (Packer et al.
1988). By the end of 2018 two of our three focal study prides had lost all of their adult lionesses. During 2017 and 2018 we documented the last surviving adult lioness from either of the three focal prides twice attempt to raise cubs. Both attempts were unsuccessful. The death of adult pride males also can have cascading effects by resulting in a more rapid turnover of pride males and consequent infanticide of cubs (Whitman et al.
2004), with greater detrimental effects to the population.
The cause of the increase in targeted poaching of lions for body parts is still poorly understood. A local demand for traditional medicinal or ceremonial use of lion parts has likely been present in the area for some time. Skin, meat and possibly fat were the only body parts known to be harvested from lions killed from 2011 to 2013, (Fig.
4). These particular killings were non-targeted poaching incidents (Fig.
2) and therefore the harvesting of body parts may have been opportunistic. Fat has been documented as the most prevalent lion derivative in some known
muti markets in southern Africa (Williams et al.
2015). The harvesting of heads or faces and paws was first recorded with the emergence of targeted poaching of lions in 2014 and all subsequent targeted poaching victims have had these body parts removed. The same body parts were also harvested from several retaliatory killings, post 2014. This increase in the removal of heads or faces and paws from lions in and around Limpopo National Park, along with the confiscations of lions’ teeth and claws at the Mozambique airport indicates a recent demand specifically for lion canine teeth and claws.
While the findings we present here are among the few quantitative descriptions of targeted poaching of lions for body parts, they do confer with the previous finding of Hazzah and Gudka (
2010) who documented a trade in lion parts sold as trinkets to tourists in Kenya. There, predominantly Chinese tourists were fuelling a demand for lion teeth and claws, supplied with lions often killed in conflict situations by Masai herdsmen, while other body parts such as pieces of skin, were sought for local demand. The situation we present from Mozambique may have similarities to the situation documented in Kenya, however the main source of the demand is still speculative. During 2017 there has also been reported increases in the poaching of lions for teeth and claws in the Niassa reserve in northern Mozambique (C. Beggs Niassa Lion Project
pers coms) and captive lions in the Limpopo province of South Africa (K. Marnewick Endangered Wildlife Trust
pers coms) as well as cases where lions killed for conflict in the Caprivi region of Namibia now also had teeth and claws removed (L. Hansen Kwando Carnivore Project
pers coms).
Our findings indicate an apparent preference for teeth and claws, which confer with the Williams et al. (
2017b) continental meta-analysis of trade in lion parts. Williams et al. (
2017b) concluded that the domestic trade in teeth and claws was high across the continent and likely poses a greater threat to wild lions than an international demand, though the impact of which was generally unknown. However, our findings have indicated a possible international demand from Vietnam impacting this wild population and calls for further detailed investigation. The sudden emergence of this preference around 2014 in the study area may also warrant further examination of IWT and legal trade trends at both a domestic and international level and related socio-economic variables of Mozambique around this time. The role and widespread use of the Internet, and in particular social media, is reported to be further facilitating IWT (Lavorgna
2014) whereby a demand for, or use of, a specific species and / or body part may be shared instantly across a large platform signalling a sudden preference.
The legal export of lion parts from captive lion breeders in South Africa may also fuel an illegal trade in lion body parts to be used within Traditional Chinese Medicine markets or curios (Williams et al.
2017a). While direct evidence linking the legal trade in captive sourced lion parts from South Africa to the targeted poaching of wild lion populations has to date been scant (Williams et al.
2015), there is reasonable concern of a link (CITES
2016; Parliamentary hearings). Lion teeth and claws have the highest monetary value in South Africa’s legal market (Williams et al.
2019). In all of the lion poaching incidences we documented where only teeth and claws were taken, the poachers involved were working on foot and under at least a nominal threat of being arrested. In such a situation it is likely that poacher’s selection for teeth and claws over removing full skeletons is a way of optimizing their return while reducing the costs. It is also possible that established rhino and elephant poaching syndicates and traders already operating in the region have simply added lion parts to their list of illegal wildlife products. This hypothesis is supported by interactions we documented between lion and elephant poaching which included the use of poached elephants as bait to kill lions and a seized shipment containing a mix of elephant ivory with numerous lion teeth and claws destined for Vietnam.
Conclusion
The illegal wildlife trade poses an unprecedented threat to global wildlife (Rosen and Smith
2010) and poaching is a major threat to many of the world’s large carnivores (Ripple et al.
2014). The loss of apex predators can have cascading impacts through lower trophic levels leading to ecological state shifts and ecological collapse (Estes et al.
2011). The loss of charismatic megafauna from protected areas can also result in substantial loss of potential revenue from tourism (Naidoo et al.
2016).
We acknowledge that this study is reporting on small data sets, however we believe they are worthy of reporting and consideration in light of this threat’s sudden emergence in the system, the potential impact it may have had on an already limited lion population (Everatt et al.
2014,
2019), and the devastating impact it could have on other lion populations across Africa.
We strongly recommend that African governments, protected area managers, conservation organizations, researchers and the global conservation community be vigilant of and quick acting towards addressing this emergent and serious threat to wild African lions, and other big cats. Stakeholders should adopt holistic and collaborative approaches to preventing and halting the poaching of and trade in the body parts of imperilled cats.
Acknowledgements
This work was supported by Grants received by KTE from the Wildlife Conservation Network’s Lion Recovery Fund [Grant Number MZ-ACE-01]; National Geographic Big Cats Initiative [Grant Number 916]; Natural Sciences and Engineering Research Council of Canada [Grant Number PGSDZ-487542-2016]; the US Fish and Wildlife Service [Grant Number F17AP00822]; the Wilderness Foundation [Grant Number 01-2015,01-2016]; the Ratel Trust [Grant Numbers 05-2016,01-2018]; Panthera Kaplan Graduate Award [Grant Number 10-2014]; Nelson Mandela University Post Graduate Research Scholarship [Numbers NMU PGRS 2014,2015,2016,2017], University of Pretoria Post Graduate Scholarship [Numbers UPPGS 2012,2013] Elephant’s Alive, Biologist Without Borders (Grant No: 2016-01), Wilderness Trust (Grant No. 2014), SATIB Trust and the Wilderness Foundation (Grant No. 2016). We thank the Administração Nacional das Áreas de Conservação, Mozambique and South African National Parks for granting us annual research permits as well as the management of Kruger National Park, Limpopo National Park, Banhine National Park and Karangani Nature Reserve for granting us access to each protected area to conduct research. We would also like to thank the many field rangers in each of the parks and reserves where we have been working who have both assisted with research and who work tirelessly towards the protection of threatened wildlife. We would also like to thank several anonymous reviewers.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.