1Department of Biology, Colorado State University, 1878

Campus Delivery, Fort Collins, CO 80523, USA2Kellogg Biological Station, Michigan State University,

Hickory Corners, MI 49060, USA3Graduate Degree Program in Ecology, Colorado State

University, Fort Collins, CO 80523, USA

*Correspondence: justin.havird@colostate.edu

(J.C. Havird).

http://dx.doi.org/10.1016/j.tree.2015.11.012

References1. Whiteley, A.R. et al. (2015) Genetic rescue to the rescue.

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2. Frankham, R. (2015) Genetic rescue of small inbred pop-ulations: meta-analysis reveals large and consistent bene-fits of gene flow. Mol. Ecol. 24, 2610–2618

3. Waller, D.M. (2015) Genetic rescue: a safe or risky bet? Mol.Ecol. 24, 2595–2597

4. Tallmon, D.A. et al. (2004) The alluring simplicity and com-plex reality of genetic rescue. Trends Ecol. Evol. 19,489–496

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7. Gemmell, N.J. et al. (2004) Mother's curse: the effect ofmtDNA on individual fitness and population viability. TrendsEcol. Evol. 19, 238–244

8. Reinhardt, K. et al. (2013) Medicine. Mitochondrial replace-ment, evolution, and the clinic. Science 341, 1345–1346

9. Burton, R.S. et al. (2013) Cytonuclear genomic interactionsand hybrid breakdown. Annu. Rev. Ecol. Evol. Syst. 44,281–302

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567–579

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Science & SocietyBanning TrophyHunting WillExacerbateBiodiversity LossEnrico Di Minin,1,2,*Nigel Leader-Williams,3 andCorey J.A. Bradshaw4,5

International pressure to ban trophyhunting is increasing. However, we

argue that trophy hunting can be animportant conservation tool, pro-vided it can be done in a controlledmanner to benefit biodiversity con-servation and local people. Wherepolitical and governance structuresare adequate, trophy hunting canhelp address the ongoing loss ofspecies.

International Outrage over TrophyHunting in AfricaAn American hunter killed a charismaticmale lion (Panthera leo) called Cecil inZimbabwe in July 2015. This sparkedinternational outrage, mainly via a stormof social and other media. Several allegedaspects of the hunt itself, such as baitingclose to national park boundaries, weredone illegally and apparently against thespirit and ethical norms of well-managedtrophy hunts. Online outrage had alsobeen sparked earlier in 2015 by the legalhunt of a Critically Endangered male blackrhino (Diceros bicornis). This hunt wassanctioned by the Namibian Governmentvia an auctioned permit that cost thehunter US$350 000 for the privilege. Thisoutrage arose even though the male wasconsidered ‘surplus’ to the national blackrhino management plan, and the revenuegenerated from the hunt was to be rein-vested into a conservation trust fund to thewider good of conservation in Namibia.These two high-profile hunts and theensuing public backlash against the ethicsand conduct of trophy hunting in generalhave led to proposals to ban the practicethroughout Africa. Furthermore, somecommercial passenger and cargo airlineshave decided to stop, or may soon stop,the transport of trophies of hunted animalsshot legally and sustainably by foreigntourists, irrespective of international con-ventions, such as the Convention on Inter-national Trade in Endangered Species ofWild Fauna and Flora (CITES) and nationallaws that allow trophy hunting.

Trends

Hunting Industry in Sub-SaharanAfricaTrophy hunting strongly contributes to theconservation enterprise in sub-SaharanAfrica, where large areas support importantterrestrial biodiversity that is currently allo-cated to trophy hunting use (Table 1). Whilemost of the hunted individuals (e.g., 96% inSouth Africa in 2012) [1] are often frommore common and less valuable species(Table 1), most of the trophy hunting reve-nue is generated from a few species carry-ing valuable trophies, particularly thecharismatic ‘Big Five’ (lion leopard Pan-thera pardus; elephant Loxodonta africana;buffalo Syncerus caffer; and black or whiterhinoceros Ceratotherium simum) [2]. Outof the US$68 million of gross revenue gen-erated from trophy hunting in South Africain 2012, over US$28 million (at least 41%)was generated from the Big Five alone (i.e.,$5 635 625 from 635 buffaloes; $1 194600 from 33 elephants; $647 500 from37 leopards; $15 270 750 from 617 lions,$300 000 from one black rhinoceros; and$5 355 000 from 63 white rhinoceroses)[1]. Southern African countries and Tanza-nia exported most of the Big Five trophiesbetween 2009 and 2013 (Figure 1). At thesame time, two countries that do not typi-cally attract many tourists (the Central Afri-can Republic, currently undergoing aconflict, and Cameroon, where poachingpressure is high) allowed trophy hunting ofbig cats and elephants, respectively, overthe same period (Figure 1).

Concerns about Trophy HuntingOverall, land allocated to trophy huntinghas the potential to assist countries toachieve biodiversity conservation goals[3]. However, the contribution of huntingto conservation is often contentious forvarious reasons. There can be uncertaintyover the sustainability of offtake rates andtheir potential impact on wildlife popula-tions [4]. This concern arises becausequotas and offtakes are not often basedon scientific assessments. Furthermore,restrictions on the age of hunted

in Ecology & Evolution, February 2016, Vol. 31, No. 2 99

Namibia, however, revenue generatedfrom trophy hunting has encouraged

e o

,

,

h

N

pa g

n

individuals are not often implemented [5].In addition, the contribution of some formsof trophy hunting to conservation is debat-able. This is particularly the case for‘canned lion hunting’, where future targetsare bred and raised in captivity and kept inconfined enclosures until shot, to ensurethat hunters are guaranteed a kill. In SouthAfrica, which is by far the largest exporterof lion trophies across sub-Saharan Africa(Figure 1), 80% of the trophies between2009 and 2013 were from lions raised incaptivity or ranched. The ethics of cannedhunting are dubious, and this abhorrentpractice requires reform before it bringsdown ethically practiced hunting.

The profitability of their respective huntingindustries is hard to compare across sub-Saharan countries [5]. Nevertheless, it isknown that the gross annual revenue gen-erated by the hunting industry comprisestens of millions of US$ in countries such asSouth Africa, Tanzania, and Botswana(Table 1). Despite this, the amount ofaccrued revenue allocated to conserva-tion authorities that could in principle bereinvested in improved managementappears to be limited. In Tanzania, forexample, the accrued revenue allocated

Table 1. Hunting Contribution to Biodiversity Co

Country Area Covered by Game Ranch(% of Total Land Area)a

South Africa 13.1

Tanzania 26.4

Botswana 23.0

Namibia 11.4

Zimbabwe 16.6

Mozambique 10.5

Zambia 21.3

Total –

a[13].bWorld Bank (http://data.worldbank.org/indicator/ER.LcCITES trade database (http://trade.cites.org/).dChacma baboon (Papio ursinus), elephant (Loxodontostrepsiceros), lechwe (Kobus leche), leopard (Panther

eData not adjusted for inflation.f[1].g[6] (data for 2008 for Botswana, Tanzania and MozamhAfrican Indaba (http://www.africanindaba.com/wp-co

100 Trends in Ecology & Evolution, February 2016, Vol. 31

to the Wildlife Division in 2008 amountedto 22% (US$12 353 180) of the grossrevenue generated by hunting in that year[5]. The remainder of the revenue went tothe private sector.

Another limitation is that revenue gener-ated from trophy hunting currently pro-vides few benefits to local communitiessharing habitats with biodiversity [6,7]. In

nservation and National Economies in Sub-Saha

s Terrestrial Protected Areas(% of Total Land Area)b

Top 3 MTrophies

6.2 impala, w

32.2 leopard,

37.2 elephant

43.2 zebra, ch

27.2 elephant

17.6 Nile croc

37.8 lechwe,

– –

D.PTLD.ZS).

africana), hippopotamus (Hippopotamus amphibius), im pardus), Nile crocodile (Crocodylus niloticus), wartho

bique, 2007 for Zimbabwe, and 2002 for Zambia).tent/uploads/2014/03/AfricanIndabaVol3-4.pdf).

local community participation in conser-vation, which in turn has resulted in sub-stantial increases in the abundance ofmany wildlife species and in the totalarea of land falling under communityprotection through conservancies [6]. Itis less clear in other African countrieswhat proportions of hunting-permit rev-enue are directed to community-devel-opment projects, whether they arepayments to community-based orga-nizations, or payments to communitiesfor concession fees, resource fees, orpayments for welfare and education.Finally, legal controls over biological, eth-ical, and financial aspects of the huntingindustry can be more easily circum-vented in many sub-Saharan countries

, No. 2

where management capacity and gover-nance structures are ineffective [8].

Why Blanket Bans CouldExacerbate Biodiversity LossOne currently promoted solution toaddress such concerns is to ban trophyhunting altogether. However, a blanketban on trophy hunting could lead to worseconservation outcomes for three mainreasons. First, financial resources forconservation are limited, particularly indeveloping countries. Hence, bothnonconsumptive and consumptive usesof wildlife are necessary to generateenough funding to support meaningfulconservation success over large areas[9]. While ecotourism can help reducepoverty in communities coexisting withbiodiversity [3], ecotourists generally pre-fer travelling to more accessible areas [10],greatly limiting the opportunities for con-servation in more remote regions. Instead,sustainable hunting can create importantincentives for biodiversity conservation inareas where ecotourism is not economi-cally viable [11]. At a time when greaterproportions of conservation budgets arebeing spent on enforcement, the revenuefrom trophy hunting can empower

ran Countries

st Exportedin 2012c,d

AnnualRevenue(US$ million)e

arthog, kudu 68.0f

hippopotamus, elephant 56.3g

leopard, lechwe 40.0g

acma baboon, leopard 28.5h

leopard, chacma baboon 15.8g

odile, elephant, hippopotamus 5.0g

ippopotamus, leopard 3.6g

217.2

ala (Aepyceros melampus), greater kudu (Tragelaphus (Phacochoerus africanus), zebra (Equus quagga).

n.

e

Black rhino (Diceros bicomis)Cri�cally endangeredCITES appendix IPopula�on trend increasing

842

Elephant (Loxodonta africana)VulnerableCITES appendix I and IIPopula�on trend increasing

496400200

Hippo (Hippopotamus amphibius)

VulnerableCITES appendix IIPopula�on trend decreasing

328200100

Figure 1. Number of Trophies Exported from 200Species Subject to Trophy Hunting. Gray-shaded afrom www.iucnredlist.org/technical-documents/spatial-International Trade in Endangered Species of Wild Fauretrieved from the CITES Trade Database (http://tradeterms’ bar. Information about the conservation status, piucnredlist.org and www.cites.org. Numbers next to thebar charts of annual trophies taken per species and p

Leopard (Panthera pardus)Near threatenedCITES appendix IPopula�on trend decreasing

343200100

Lion (Panthera leo)VulnerableCITES appendix IIPopula�on trend decreasing

877600300

White rhino (Ceratotherium simum)

Near threatenedCITES appendix I and IIPopula�on trend increasing

19110050

9 to 2013 (Red Bars) for Six Charismatic Africanreas correspond to the range maps of species obtaineddata. Each species is listed under the Convention ona and Flora (CITES). Net export data for each speciescites.org) by searching for ‘trophies’ under the ‘tradeopulation trend, and CITES listing retrieved from www.external bar in each panel indicate the scale to interpretr country.

Trends i

communities to protect their resources bythe employment of more antipoachingrangers or the construction of disincentiveinfrastructure [12]. If revenue cannot begenerated from trophy hunting, naturalhabitats will be transformed to other formsof land use that provide higher return oninvestments compared with conservation[3], but have negative impacts onbiodiversity.

Second, trophy hunting can have asmaller footprint than ecotourism in termsof carbon emissions, infrastructure devel-opment, and personnel, and can generatemore revenue from a lower volume oftourist hunters. An often-neglected rela-tion exists between ecotourism and avia-tion with regard to energy use andgreenhouse gas emissions. Comparedwith ecotourism, the trophy-huntingindustry relies on fewer tourist hunters,because the income generated per hunteris higher [13]. Additionally, hunters areinterested in maintaining good-qualityhabitat for the simple reason that the qual-ity of the individuals harvested therein isalso high [14]. Finally, hunters are pre-pared to hunt in areas lacking attractivescenery, and require less infrastructure,therefore minimizing habitat degradation.

Third, management for hunting placesemphasis on maintaining large wildlifepopulations for offtake, as opposed toecotourism, where the presence of onlya few individual animals is sufficient tomaximize profits [2]. Both the consump-tive and nonconsumptive uses of biodiver-sity can generate important revenue, soallowing local stakeholders, such as pri-vate landowners and communities, toretain property rights over these speciesis a necessary precursor for them to justifyoffsetting the direct and opportunity costsof conservation. Thus, the economicmodels underlying ecotourism and trophyhunting may lead to diverging manage-ment strategies. Empirical evidenceshows that the strategy of artificially man-aging small populations within electrifiedfences to maximize economic return from

n Ecology & Evolution, February 2016, Vol. 31, No. 2 101

c

s

na

d

ecotourism and minimize managementcosts might be the most appropriate toenhance tourist experiences [2]. By con-trast, wildlife populations potentially havehigher hunting value when their sizes arelarger (i.e., are more viable) and popula-tions are better connected to enhancegene flow, because the latter can affectthe fitness and quality of the individualsharvested.

Concluding RemarksInadequate political, legal, and governancestructures are currently preventing trophyhunting from being an effective tool for cre-ating conservation incentives in sub-Saharan Africa. At the same time, banningtrophy hunting might not be the best solu-tion because biodiversity loss could evenbe worse in its absence. Therefore, wepropose a set of prescriptions that couldenhance the contribution of trophy huntingto conservation and to the equitable shar-ing of the benefits with local people (Box 1).

Box 1. Prescriptions to Make Trophy Hunting M

1. Net Conservation Benefit1.1 Mandatory levies imposed on safari operators by gfor conservation and management.1.2 Ecolabeling certification schemes adopted for tropbiodiversity conservation and respect animal welfare

2. Biological Sustainability2.1 Mandatory population viability analyses to ensure2.2 Ban posthunt sales of any portion of the quarry

3. Socio-Economic-Cultural Benefit3.1 Promote and fund trophy-hunting enterprises run3.2 Create trusts to facilitate equitable benefit sharineconomic sustainability.

4. Adaptive Management: Planning, Monitoring,4.1 Mandatory scientific sampling of hunted animals,stomach contents, full morphometrics, disease scree4.2 Mandatory 5-year reviews of all individuals hunted

to government legislators to extend permits.

5. Accountable and Effective Governance5.1 Full disclosure to the public of all data collected (inproponents held by government legislators only.5.2 Independent government observers placed randohappen.5.3 Trophies are confiscated and permits are revoke

6. Animal welfare6.1 Backup professional shooters and trackers prese

102 Trends in Ecology & Evolution, February 2016, Vol. 31

To make these prescriptions more relevantfor decision-makers, we have summarizedthem according to the guiding principles ontrophy hunting promoted by the Interna-tional Union for the Conservation of Nature[15]. In particular, we make suggestions onhow net biodiversity benefits and stake-holder returns can be achieved simulta-neously, and highlight how the huntingindustry and governance structures canbe made more transparent to avoid unethi-cal or illegal practices. Finally, we provideadditional guidelines to account for animalwelfare concerns. Promoting these andother prescriptions could enhance the roleof trophy hunting in addressing the ongoingloss of species.

AcknowledgmentsWe thank M. Festa-Bianchet and an anonymous

reviewer for comments that helped improve the man-

uscript. E.D.M. acknowledges ERC-StG

Grant 260393 (GEDA) and the Academy of

Finland Centre of Excellence Programme

ore Effective for Conservation

overnments that are invested directly into trust funds

hies originating from areas that contribute to broaderoncerns.

that harvests cause no net population decline.hot, to avoid illegal wildlife trade.

(or leased) by local communities.g within local communities and promote long-term

and Reportingincluding tissue for genetics, teeth for age analysis,ing, and so on.nd detailed population management plans submitted

cluding levied amounts), although personal details of

mly and without forewarning on safari hunts as they

when illegal practices are disclosed.

nt for all hunts to minimize welfare concerns

, No. 2

2012–2017 (Grant 250444) for support. Unless spec-

ified otherwise, photographs in Figure 1 by E.D.M.

1Department of Biosciences, University of Helsinki,

FI-00014, Helsinki, Finland2School of Life Sciences, University of KwaZulu-Natal,

Private Bag X 54001, Durban 4000, South Africa3Department of Geography, University of Cambridge,

Downing Place, Cambridge, CB2 3EN, UK4The Environment Institute and School of Biological

Sciences, The University of Adelaide, Adelaide, SA 5005,

Australia5Laboratoire Écologie, Systématique et Évolution – UMR

CNRS 8079, Université Paris-Sud, Bat 362, F-91405,

Orsay Cedex, France

*Correspondence: enrico.di.minin@helsinki.fi (E. Di Minin).

http://dx.doi.org/10.1016/j.tree.2015.12.006

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4. Bradshaw, C.J.A. et al. (2006) Incorporating known sour-ces of uncertainty to determine precautionary harvests ofsaltwater crocodiles. Ecol. Appl. 16, 1436–1448

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6. Booth, V.R. (2010) The Contribution of Hunting Tourism:How Significant is this to National Economies, CIC Techni-cal Series Publication, FAO

7. NACSO (2014) The State of Community Conservationin Namibia – A Review Of Communal Conservancies,Community Forests and Other CBNRM Initiatives,NACSO

8. Leader-Williams, N. et al. (2009) The influence of corruptionon the conduct of recreational hunting. In RecreationalHunting, Conservation and Rural Livelihoods: Scienceand Practice (7) (Dickson, B. et al., eds), In pp. 296–316,Blackwell Publishing

9. Naidoo, R. et al. (2015) Complementary benefits of tourismand hunting to communal conservancies in Namibia. Con-serv. Biol. Published online October 13, 2015. http://dx.doi.org/10.1111/cobi.12643

10. Balmford, A. et al. (2015) Walk on the wild side: estimatingthe global magnitude of visits to protected areas. PLOSBiol. 13, e1002074

11. Lindsey, P.A. et al. (2006) Potential of trophy hunting tocreate incentives for wildlife conservation in Africa wherealternative wildlife-based land uses may not be viable. Anim.Conserv. 9, 283–291

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14. Ramanzin, M. and Sturaro, E. (2014) Habitat quality influ-ences relative antler size and hunters’ selectivity in roe deer.Eur. J. Wildl. Res. 60, 1–10

15. IUCN (2012) Guiding Principles on Trophy Hunting as a Toolfor Creating Conservation Incentives, IUCN