Opinion

Does research help to safeguard protected areas?

William F. Laurance
Centre for Tropical Environmental and Sustainability Science and School of Marine and Tropical Biology, James Cook University, Cairns, QLD 4878, Australia

Although many protected areas are foci for scientic research, they also face growing threats from illegal encroachment and overharvesting. Does the presence of eld researchers help to limit such threats? Although evidence is largely anecdotal, researchers do appear to provide some protective effects, both actively (such as by deterring poachers) and passively (such as by beneting local communities economically and thereby generating support for protected areas). However, much remains unknown about the generality and impacts of such benets. A key priority is to develop a better understanding of the advantages and limitations of eld research for aiding protected areas and their biodiversity. Are protected areas protected? In a world beset by environmental challenges, protected areas are seen as a cornerstone of efforts to sustain the biodiversity and natural ecosystem processes of the Earth. The good news is that we have more protected areas than ever: since 1985, the total land area with at least some legal protection has more than tripled, now totaling 13% of the global terrestrial surface [1]. The bad news, however, is that many protected areas are under threat (Figure 1) [25]. Some areas are plagued by illegal encroachment, logging, and burning, whereas wildlife poaching and overharvesting of fuel wood are serious threats for other reserves, especially in developing nations [3]. As land-use and population pressures increase, protected areas are increasingly being surrounded by hostile modied landscapes [3,4]. In many areas, illegal gold mining has expanded apace [5] (Box 1 i). As a consequence of these and other perils, defending the integrity of protected areas and their biodiversity is a growing challenge, in part because many reserves are inadequately resourced and safeguarded [2,3,6,7]. The recent slaughter of elephants in Cameroon (Box 1 ii), murders of numerous park guards (Box 1 iii,iv) and massive human encroachment in some protected areas (Box 1 v) testify to the challenges at hand. Ecotourism is known to promote nature conservation by providing revenues for protected areas [8], especially in areas with large, charismatic wildlife [9] and spectacular
Corresponding author: Laurance, W.F. (bill.laurance@jcu.edu.au). Keywords: biodiversity conservation; illegal mining; poaching; park management; protected areas; scientific research. 0169-5347/$ see front matter 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2013.01.017

scenery. Beyond this, eld researchers might also benet parks and biodiversity, both actively and passively. Here, I make a rst effort to evaluate the impact of researchers on protected areas and their biodiversity, and argue that this is a prime issue for further investigation. Apparent advantages of researcher presence If protected areas benet from a science-safeguarding effect, an ancillary and sometimes hidden benet of research may be promoting nature conservation. What is the evidence? In the most direct sense, several conservation heroes have battled to establish or sustain protected areas (Table 1). Obvious examples include Dian Fossey in Rwanda [10], Daniel Janzen in Costa Rica, Patricia Wright in Madagascar, and Sir Ghillean Prance in Argentina [11]. Scientists employed by conservation organizations have also played key roles. For decades, the Wildlife Conservation Society (WCS), under the leadership of William Conway, emplaced talented scientists in the eld as conservation watchdogs, including Alan Rabinowitz in Belize, George Schaller in the Himalayas, Terese and John Hart in Zaire, and Lee White in Gabon. These dynamic individuals were prime movers in the creation of many new protected areas (J. Terborgh, personal communication). Field researchers can also benet protected areas by actively deterring poachers and encroachers (Table 1, Box 2). The best-documented evidence for this is at Tai Nation te dIvoire, Africa, where active research sites al Park in Co have higher wildlife abundances and less evidence of poaching, compared with areas with little research activity [1215]. Suppression of poaching and illegal logging has also been noted in areas frequented by scientists or bird -Ndoki Reserve in Congo [16], Lope watchers at Nouable Reserve in Gabon (F. Maisels, personal communication), Gunung Palung National Park in Borneo (A.J. Marshall, personal communication) and Soberania National Park in Panama (S.J. Wright, personal communication). Some scientists are audacious. In a central Amazonian reserve where I work, a plucky Brazilian graduate student once faced down a truckload of armed poachers [17], whereas foreign scientists at Gunung Palung spiked trees to deter rampant illegal logging (Table 1). If scientists do often function as de facto park guards, then the benets for biodiversity might be considerable. Several studies suggest that detecting and apprehending poachers in the eld is generally a more effective deterrent than is imposing more severe punishments, such as higher
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(a)

(b) (c)

(d)

(e)

(f)

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Figure 1. Research activity can reduce a variety of environmental threats in protected areas, such as: (a) illegal logging in Sumatra; (b) wildcat gold mining in Suriname; (c) poached gorilla in Equatorial Guinea; (d) fires near Xingu National Park and associated Kayapo indigenous lands in Brazil; (e) elephant killed by gunshot in Gabon; and (f) apparent poachers detected by an automatic camera in Peninsular Malaysia. Reproduced, with permission, from W.F. Laurance (a,b), J. Fa (c), NASA Modis satellite (d), R. Buij (e), G.R. Clements (f).

nes [1820]. Although the proportion of scientists that engage in active safeguarding is unknown, veteran researcher Jeffrey Sayer suggests that it might be the rule rather than the exception (personal communication). Field researchers can also advance conservation of parks less directly. In the northern Republic of Congo, scientists from the WCS have promoted ecotourism and motivated park guards to redouble their enforcement efforts (J. Sayer, personal communication). Some scientists build local support for protected areas with education programs for nearby communities and by hiring locals as eld assistants or para-taxonomists (S.L. Pimm, M. Peck, and A.J. Marshall, personal communication). In Gabon, the eld assistants that my colleagues and I employ are former hunters with impressive knowledge of local wildlife [21], and several have become keenly interested in nature conservation. Similarly, researchers and ecotourists at Ranomafana National Park in Madagascar are the largest source of income for impoverished nearby villages, providing some US$2 million in revenues and assistance annually that helps to build local support for the park [22]. Scientists are also advancing conservation by helping to empower local residents in a complex and rapidly changing world (Table 1). In Papua New Guinea, eld researchers have helped indigenous communities respond to logging and mining companies seeking access to their lands, so that the communities can judge the promises of nancial gain more realistically (V. Novotny, personal communication). In northwestern Ecuador, researchers are promoting forest conservation by training community para-biologists who collect data on primates and report risks to their
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habitats (M. Peck, personal communication). This effort links local communities to scientists, conservation organizations, and local and national governments (http:// www.primenet.org.uk/). Finally, one cannot ignore the prominent role that scientists have in publicizing parks and their biodiversity. For instance, during the 1970s, researchers at Manu National Park in Peru attracted world-class photojournalists whose lms, documentaries, and books made the park famous and attracted many tourists. Almost every other river in the region has been logged and hunted out, but with boatloads of tourists entering the park each day, no poacher or logger would dare show his face (J. Terborgh, personal communication). The busy tourism industry helps to protect the park directly and also has a strong vested interest, which it freely expresses publicly, in maintaining the integrity of the park. In this manner, science promotes tourism and tourism in turn promotes nature conservation [9,2325]. Limitations of science safeguarding Despite such apparent successes, the science-safeguarding effect seems partial at best. In response to burgeoning Asian demands for ivory and rhino horn, Africa is the midst of an epic elephant [26] and black rhino [27] slaughter by armed poachers, rebels, and even the military that scientists and park managers have largely been unable to stop. At Los Amigos Biological Station in Peru, illegal gold miners threatened to burn down the research station when scientists tried to halt their operations, and then continued mining and clearing forest (N.C.A. Pitman, personal

Opinion
Box 1. Website articles referred to in this paper
(i) Butler, R. (2012) Environmental impact of mining in the rainforest. Mongabay.com 27 July 2012 (http://rainforests. mongabay.com/0808.htm) (ii) Grossman, S. (2012) Hundreds of elephants slaughtered in Cameroon as ivory demand skyrockets. Time Newsfeed 16 March 2012 (http://newsfeed.time.com/2012/03/16/hundreds-ofelephants-slaughtered-in-cameroon-as-ivory-demand-skyrockets/) (iii) Hance, J. (2010) Poachers kidnap and murder ranger in India. Mongabay.com 14 June 2010 (http://news.mongabay.com/ 2010/0614-hance_ranger.html) (iv) Anon. (2012) Rebels kill 3 rangers in Congos Virunga National Park. Mongabay.com 27 October 2012 (http://news.mongabay. com/2012/1027-virunga-attack.html) (v) Hance, J. (2012) Over 100,000 farmers squatting in Sumatran park to grow coffee. Mongabay.com 6 November 2012 (http://news. mongabay.com/2012/1106-hance-squatters-bukit-barisan.html) (vi) Holbrook, J.B. and Frodeman, R. (2012) Science: for sciences or societys sake? Science Progress 1 March 2012 (http:// scienceprogress.org/2012/03/owning-the-national-sciencefoundation%E2%80%99s-broader-impacts-criterion/) (vii) WWF (2012) Timeline of recent instances of poaching and illegal wildlife trade in Central Africa (http://www.google. com.au/url?sa=t&rct=j&q=&esr c=s&source=web&cd= 6&ved=0CFIQFjAF&url=http%3A%2F%2Fwww.divshare. com%2Fdirect%2F19315157-0f8.pdf&ei=y3CtUOz4Asjvm AXlooCgBg&usg=AFQjCNFvKu1db5l3Hb_mrFFhuf2AFz7qCQ) (viii) WWF (2012) Cameroon arrests one of Central Africas most notorious wildlife poachers. 5 October 2012 (http://wwf.panda. org/?206372/Cameroon-arrests-one-of-Central-Africasmost-notorious-poachers)

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communication). An assessment of 109 protected areas across Africa concluded that research and tourism were less important than was effective enforcement by park guards and the involvement of local or international conservation groups in promoting ape conservation [28]. One must conclude that, although scientists often have positive effects in promoting local conservation, there clearly is scope for increasing these benets. A further point of concern about science safeguarding is that, in attempting to promote nature conservation, crusading researchers might inadvertently upset local sensitivities. For instance, my efforts to encourage tropical biologists to adopt a forest [11] prompted worries that some scientists might not be familiar enough with local social, cultural, and political contexts to advance conservation effectively [29]. Such issues are debated frequently in academic circles and are strongly inuenced by ones training and world view (e.g., [3032]). Finally, under certain circumstances, eld research might be harmful for nature conservation. It has been suggested, for instance, that radiotelemetry studies contributed to local extinctions of African wild dogs [33] and tigers [34], putatively by stressing the dogs and making the tigers more vulnerable to hunters. More generally, mark recapture studies and biological collecting, if not conducted carefully, have the potential to harm fauna and ora

Table 1. Examples of how researchers have contributed to the establishment and safeguarding of protected areas
Protected area and region Volcanoes National Park, Rwanda Parks in northern Congo-Brazzaville and Central Africa Republic Gabon Gunung Palung National Park, Indonesian Borneo Kenyir Wildlife Corridor, Peninsular Malaysia Lazovsky Nature Reserve and Zov Tigra National Park, Russian Siberia Biological Dynamics of Forest Fragments Project, Brazilian Amazonia Brownsberg National Park, Suriname Ranomafana National Park, Madagascar Description Dian Fossey fought to protect mountain gorillas from poaching WCS scientists promoted research and ecotourism to reduce wildlife overhunting (Figure 1c,e, main text) WCS scientists played a key role in convincing the government to establish a national protected area network With central government backing, foreign scientists drove off poachers and spiked trees in an effort to stop massive illegal logging (Figure 1a, main text) in the park Scientists report poachers caught on camera traps (Figure 1f, main text) to enforcement authorities and have lobbied to freeze development along a highway bisecting the wildlife corridor Researchers use hidden camera traps to identify poachers targeting rare Amur tigers and to focus efforts of antipoaching patrols Researchers chased off poachers and opposed government efforts to allow colonization of the study area Scientists decry illegal gold mining (Figure 1b, main text) in the park and lobby the Government to increase enforcement efforts Patricia Wrights discovery of the golden bamboo lemur in 1986 led to the establishment of the park, and visiting researchers and ecotourists now provide key income for local communities Less wildlife poaching in areas with researcher presence Serengeti Wildlife Research Centre has provided an active researcher presence for over 50 years Long-term researchers encouraged the Kayapo to reject contracts with mahogany loggers and have funded aerial patrols to detect encroachment along reserve boundaries (Figure 1d, main text) Hunted mammals have increased near popular bird-watching routes, evidently because of reduced poaching in the area Information source [10] Jeffrey Sayer Lee White and Michael Fay Chuck Cannon and Andrew Marshall http://myrimba.org
a

[17]
c

[22]

Nouable-Ndoki, Republic of Congo Serengeti National Park and nearby protected areas, Tanzania Kayapo Indigenous Reserve, Brazilian Amazonia Soberania National Park, Panama
a

[16] Jeffrey Sayer [46]

S. Joseph Wright

Hance, J. (2012) Development halted in crucial wildlife corridor in Malaysia. Mongabay.com 7 November 2012 (http://news.mongabay.com/2012/1107-hance-kenyircorridor.html).

Zoological Society of London (2012) Forest eyes are watching you. 7 November 2012 (http://www.zsl.org/conservation/news/forest-eyes-are-watchingyou,1020,NS.html).

Anon. (2008) Scientists call for mining ban, new protected areas in Suriname. Mongabay.com 21 June 2008 (http://news.mongabay.com/2008/0618-suriname_ mining.html).

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Box 2. Conservation in the trenches
For every high-profile scientist crusading for biodiversity, scores more are working behind the scenes to promote nature conservation. One example is Zacharie NZooh from Cameroon (Figure I). A plant ecologist by training, Zacharie was recruited by WWF-Cameroon in 2002 to conduct biodiversity surveys in the Sangha Tri-National Conservation Complex in the northwestern Congo Basin. Since then, he has hiked thousands of kilometers and developed an unparalleled knowledge of the flora, fauna, and people of the area. He has also become highly engaged in protecting the area, especially from illegal poaching and gold mining (J. Sayer, personal communication).

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In 2011, one of the eco-guards that Zacharie advised was killed and another wounded by poachers (Box 1 vii). Since then, Zacharie has persuaded the Cameroon Army to deploy contingents from its Rapid Intervention Battalion, who have beefed up park protection. Guided by Zacharie, they have so far confiscated 16 Kalashnikov rifles and arrested several poachers. Cameroon law-enforcement authorities have also begun targeting white-collar poachers, who are the political and business elites who bankroll the poachers and handle the products of their illicit trade. As a result, some major players in the illegal bushmeat business are now behind bars (Box 1 vii,viii).

(a)

(b)

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Figure I. Zacharie NZooh (a) in Cameroon and one of the species he is fighting to protect (b). Reproduced, with permission from M. Dandjouma (a) and F. Carre (b).

[3537], and would be a special concern for rare or locally endemic species or insular populations in parks. In addition, certain disturbance-sensitive wildlife might avoid areas with high researcher or tourist activity [3842], such as the vicinity of research centers, trails, and long-term eld sites. A camera-trapping study in Sumatra, for instance, suggested that larger mammals, such as barking deer, sambar, and Sumatran rhinoceros, tend to avoid areas frequented by eld researchers, whereas sun bears become more nocturnal [38]. Many temperate species, including moose, bobcats, wolves,

black bears, and bald eagles, also retreat or alter their behavior in response to human activity [3941], even to quiet hiking and nature observation [42]. An additional concern is that humans can inadvertently transmit infectious diseases to wildlife, including primates [43], bats [44], and amphibians [45]. For such reasons, I hypothesize that the impact of research on park and biodiversity values might be nonlinear, being most positive at intermediate values (Figure 2). Concluding remarks It is remarkable that the effects of eld research on the conservation values of protected areas have yet to be assessed systematically. To what degree does research benet or harm park values? Can research activity be optimized in space and time to maximize its benets for conservation? Are heavily studied areas, such as the vicinities of popular research centers, biased biologically because their faunal communities have been altered by researcher activity? These are but a sampling of important questions that could and should be addressed (Box 3). Understanding such relations is important. For instance, if eld research generally benets park values, then ndings from a recent survey of biodiversity trends in tropical forest protected areas [3] might be overly optimistic. In this study, my colleagues and I assessed trajectories of biodiversity change in 60 relatively well-studied protected areas across the tropics. Half of these reserves showed evidence of declining reserve health, but our conclusion might be even starker if the sites we studied,

Benet for biodiversity

Researcher or ecotourist acvity

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Figure 2. Hypothetical relation between research activity and its benefits for protected areas and their biodiversity. Photograph reproduced, with permission, from W.F. Laurance.

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Box 3. Studying science-safeguarding effects
A variety of approaches could be used to assess the impact of researchers on protected-area values, including:  Testing whether indices of research activity, such as the number of publications, correlate with indices of biodiversity health or threats across different parks.  Assessing how researcher activity affects park values, such as wildlife abundances and the activity of poachers or encroachers (e.g., [1214]), at different sites within a single park.  Experimentally manipulating researcher activity at different places or times, to determine whether and how this affects wildlife responses and park encroachment.  Using questionnaires to evaluate the effects of field research on conservation values of parks, by surveying a large, representative sample of scientists.

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Such research raises ancillary questions for conservation practice and training, including:  Should researchers be encouraged to study in locations that suffer from greater threats [3], even if this might entail more personal risk, to maximize the benefits for conservation (Figure I)?  Does protecting a park merely displace its threats to nearby unprotected areas (e.g., [47,48])?  Which personal or professional attributes make researchers most engaged and effective as conservation leaders? Such information (e.g., [11,49]) could help inform the numerous graduate programs in conservation leadership currently being offered by universities.

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Figure I. Some protected areas are at serious risk. This bullet-ridden road sign, from the Waimiri Atroari Indigenous Reserve in central Amazonia, says Dont run over the animals. Reproduced, with permission, from W.F. Laurance.

by virtue of being well studied, were buffered from some key environmental threats. Although some scientists are highly engaged in park conservation, there clearly is scope for others to increase their role as protectors and advocates. One leading conservation researcher asserts that It is high time that this came to be a standard obligation for scientists (T.E. Lovejoy, personal communication). Such activities can also benet the scientists themselves. For example, the US National Science Foundation increasingly emphasizes broader criteria, such as public outreach and greater societal benets, in evaluating research proposals (Box 1 vi), and many philanthropic foundations place great weight on conservation activities when awarding grants and environmental prizes to scientists. Although many questions remain, I believe that available evidence suggests that eld research does broadly benet biodiversity and park values. If this is the case, then this information needs to be conveyed to funders and decision-makers. Maintaining a long-term research presence could be one of the more effective ways to help safeguard imperiled protected areas. Parks with exceptional biodiversity values might merit more research funding on this basis alone. In an era of increasing nancial austerity, we must carefully weigh the potential

implications of reducing research in our embattled protected areas.

Acknowledgments
I thank John Terborgh, Jeff Sayer, Fiona Maisels, Stuart Pimm, Patricia Wright, Mika Peck, Nandini Velho, Nigel Pitman, Chuck Cannon, Andrew Marshall, Carlos Peres, Joe Wright, Stephen Blake, Susan Laurance, David Lindenmayer, David Edwards, John Fa, Corey Bradshaw, Vojtech Novotny, and Rhett Butler for many useful thoughts. John Terborgh, Tom Lovejoy, Ghillean Prance, David Edwards, Reuben Clements, and two anonymous referees commented on the manuscript.

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