opinions, perspectives & reviews ISSN 1948-6596 opinion De-extinction in a crisis discipline C. Josh Donlan Advanced Conservation Strategies, Midway, UT 84049 USA & Department of Ecology & Evolutionary Bi- ology, Cornell University, Ithaca, NY 14853 USA. [email protected]

De-extinction, the idea of resurrecting extinct spe- one of hundreds of technological innovations that cies using genetic engineering, has recently caught will happen in the coming decades. Most of them the attention of both the scientific community and will bring new ethical challenges, and de- the wider public (Kumar 2012, Sherkow and extinction may prove to be mild compared to Greely 2013, Zimmer 2013). A diverse group of other disruptive innovations coming our way. The scientists and practitioners, led by long-time envi- pace of de-extinction progress will largely depend ronmental proponent Stewart Brand, has been on the resources its proponents are able to at- busy articulating a framework for de-extinction tract. and exploring a roadmap forward, including iden- Like all intervention-based strategies, there tifying the many challenges that lie ahead. De- will be risks, costs and benefits to de-extinction. In extinction may mean different things to different my view, the potential benefits are profound, people. The Long Now Foundation defines it as while the potential costs and risks are real, but using “genetic technology and DNA from museum not novel. The risks are similar to other restora- specimens or fossils to revive species that have tion-based approaches to biodiversity conserva- gone totally extinct”1. Related discussions are also tion, such as the potential for disease transmis- underway around using genetic engineering to sion and unexpected species interactions (Donlan assist populations in adapting to climate change et al. 2006, Sherkow and Greely 2013). These are and other extinction drivers (Thomas et al. 2013). familiar issues to conservation science, and the De-extinction has sparked a lively debate on biodi- abilities to quantify and successfully mitigate versity conservation strategies, one with plenty of these risks are improving at a steady pace. For detractors who give reasons why it is a bad idea or example, our ability to manage certain invasive that it will never deliver on its promise. species, particularly mammals, has increased dra- There are many unknowns surrounding de- matically over the past two decades. There have extinction. Whether it will happen or not, how- now been over 900 successful invasive vertebrate ever, is likely not to be one of them. It already has, eradications from islands worldwide, including albeit briefly (Folch et al. 2009), and it is likely to from islands larger than 400,000 hectares (Donlan become commonplace—sooner rather than later. 2008, Veitch et al. 2011). Yet there are still obvi- One main reason for this is the rate of technologi- ous limitations in our ability to manage popula- cal innovation, which is currently doubling every tions; those limitations and uncertainty should be decade and accelerating (Kurzwell 2005). Mass a major factor in the initial stages of selecting de- adoption of the radio took 30 years, while the extinction prospects—the current ability to man- World Wide Web required only seven after it was age the taxon. This suggests that vertebrates with introduced in 1991. The power of information slow reproductive rates would make strategic can- technologies is growing even faster, doubling didates. In sum, risk assessment will be a pivotal every year. The cost of sequencing DNA, for exam- factor in the de-extinction process, but the issues ple, is outpacing Moore’s Law2. Using genetic en- involved (e.g. invasiveness, disease transmission, gineering to resurrect extinct species will be just unexpected species interactions) are common

1 http://longnow.org/revive/candidates/revival-criteria/. Last accessed 06 March 2014. 2 Wetterstrand, K.A. (2013) DNA sequencing costs: data from the NHGRI Genome Sequencing Program (GSP). Available at: http:// www.genome.gov/sequencingcosts. Last accessed 06 March 2014.

frontiers of biogeography 6.1, 2014 — © 2014 the authors; journal compilation © 2014 The International Biogeography Society 25 C. Josh Donlan — De-extinction in a crisis discipline across many biodiversity conservation interven- from more “important” activities. Will the ability tions. to bring back extinct species wipe away people’s Another common criticism of de-extinction concern about protecting species alive today? This is that it would divert attention and resources possibility assumes that conserving species is a away from other biodiversity issues and the major priority for many—although much evidence strategies to address them, such as endangered suggests otherwise (Brook et al. 2003, Sorice et al. species conservation and land-use change 2013). Could de-extinction act as a perverse incen- (Scientific American Editors 2013, Mark 2013). tive and political tool to promote activities that Will de-extinction become the next new “fad” in harm species and the environment? At a mini- biodiversity conservation and shift precious re- mum, the answer is probably yes. But environ- sources away from other strategies (sensu Red- mental policy and conservation strategies are no ford et al. 2013)? This argument can be made for stranger to perverse incentives. The US Endan- any conservation strategy: carbon markets dis- gered Species Act, for example, is fraught with tracting from ecosystem-based approaches, pay- them (Donlan et al. 2013). In many countries, ment for ecosystem services programs distracting strong policies already exist to prevent extinction; from species-based conservation, and working yet species continue to decline. It seems unlikely landscapes distracting from protected-area net- that the ability to de-extinct certain species would works (Redford and Adams 2009, Soulé 2013). drastically change the moral landscape around There is little evidence to support any of these endangered species conservation. Another sce- claims, partly because conservation practitioners nario is also worth considering: rather than acting are notoriously bad at tracking spending and out- as a perverse incentive, could de-extinction be comes (Ferraro and Pattanayak 2006, Halpern et used as a strategic policy tool to promote and trig- al. 2006). Similar to research efforts (Brodie 2009), ger conservation actions? If the passenger pigeon how conservation funding is allocated is influ- were resurrected, would there not be a legal case enced by many factors, including those that have for its protection and the designation of critical less to do with science or strategy (e.g. a family habitat under the Endangered Species Act? Moral foundation’s personal interest). Conservation dol- hazard is no stranger to the field of biodiversity lars are often not fungible, and novel initiatives conservation. can generate new funding sources. If successful, While the risks of de-extinction are not de-extinction will become a relatively specialized new, the challenges are substantial. The labora- tool under the larger umbrella of species’ reintro- tory challenges will enjoy the momentum and re- ductions. Thus, one would hope de-extinction will sources of the biomedical and agricultural sectors. become more complementary than competitive Bringing de-extinction into the “wild” will be less within the larger portfolio of conservation strate- fortunate. We are currently better at manipulat- gies. In my view, a significant diversion of re- ing genomes than we are at rewilding landscapes. sources is unlikely because conservation strategies This will have to change if the benefits of de- are not mutually exclusive—a point conservation extinction are to be fully realized. Moving from a scientists tend to overlook. De-extinction work on few individuals to a functioning, viable population the Woolly mammoth, anti-poaching programs for will probably be the limiting step—presenting a forest elephants, and market-based solutions for monumental challenge for conservation biologists. illegal wildlife trade can and should occur concur- Species reintroductions commonly fail, particu- rently. And the funding for those initiatives is larly for captive-born individuals (Jule et al. 2008). likely to come from different sources—from dif- Allee effects—demographic dynamics of small ferent players with different interests across the populations—are more complex than previously diverse environmental sector. appreciated (Hughes 2013, Luque et al. 2013). And A moral hazard argument accompanies the for many species for which de-extinction may be concern of de-extinction acting as a distraction highly desirable, the threats that were responsible frontiers of biogeography 6.1, 2014 — © 2014 the authors; journal compilation © 2014 The International Biogeography Society 26 C. Josh Donlan — De-extinction in a crisis discipline for their extinction still remain (e.g. habitat de- corner of the globe, and technology evolves at an struction and land-use change). Those remaining exponential rate. Yet the majority of those in the threats will limit the utility of de-extinction to a biodiversity conservation sector seem to ignore subset of extinct species, which calls on conserva- public opinion, which is increasingly indifferent to tion biologists to develop a decision framework to environmental issues (Kareiva and Marvier 2012). guide efforts and priorities. Given the asymmetry Public and subsequently political support for bio- in resources between inside and outside the labo- diversity conservation is declining. Biodiversity ratory, the “skin-out” challenges and the innova- conservation does not need silver bullets; rather, tions needed to overcome them may decide the it needs strategies that garner the support and on-the-ground outcomes of de-extinction. interest of average citizens. De-extinction may be The de-extinction debate is part of larger one of them: half of Americans believe “scientists discussion around the role of synthetic biology in will bring back an extinct animal by cloning it” by biodiversity conservation (Redford et al. 2013). 2050 (Pew Research Center 2013). Synthetic biology and related fields are already Will de-extinction revolutionize biodiversity delivering benefits to biodiversity conservation conservation? Unlikely. But let’s be honest: our (Ben-Nun et al. 2011, Anthes 2013). The potential current strategies are not sparking revolutions implications are as profound for extant species as either. Rather, they are underperforming—all of for extinct ones (Redford et al. 2013, Thomas et al. them. Biodiversity conservation needs all the help 2013). Yet, synthetic biology has gone largely un- and strategies it can muster. Decades ago, Stewart noticed by conservation scientists, and misinfor- Brand penned an epigram on his Whole Earth mation and subjectivity appear to be clouding the Catalog: “We are gods and might as well get good value proposition of synthetic biology to biodiver- at it”—excellent advice for conservationists in the sity conservation. coming decades. I suspect that de-extinction may be serving as more salt on open wounds. Biodiversity conser- References vation is increasingly viewed as a discipline in cri- Anthes, E. (2013) Frankenstein's cat: cuddling up to biotech's sis (Rosner 2013). Over the past decade, new in- brave new beasts. Scientific American, New York. tervention-based and human-centered strategies Ben-Nun, I.F., Montague, S.C., Houck, et al. (2011) Induced pluripotent stem cells from highly endangered spe- have been proposed and are gaining support. cies. Nature Methods, 8, 829–831. Some of those approaches are being viewed as Brodie, J. (2009) Is research effort allocated efficiently for incompatible with historical strategies for biodi- conservation? Felidae as a global case study. Biodiver- sity and Conservation, 18, 2927–2939. versity conservation. At one extreme is the view Brook, A., Zint, M. & De Young, R. (2003) Landowners' re- that “wilderness”, as we once perceived it, no sponses to an endangered species act listing and im- longer exists and successful conservation strate- plications for encouraging conservation. Conservation Biology, 17, 1638–1649. gies will rely heavily on management actions, and Donlan, C.J. (2008) Rewilding the islands. In: State of the wild will often explicitly integrate human needs (Lalasz 2008–2009: a global portrait of wildlife, wildlands, et al. 2011). At the other extreme is the view that and oceans (ed. by E. Fearn and K. Redford), pp. 226– 233. Wildlife Conservation Society & Island Press, such an approach runs counter to conservation Washington D.C. biology, is fundamentally flawed, and is akin to Donlan, C.J., Gartner, T., Male, T. & Li, Y. (2013) Species con- “gardening” (Soulé 2013). With conservation biol- servation incentives. Environmental Policy and Law, ogy founded on the basis of preservation, some 43, 162–166. Donlan, C. J., Berger, J., Bock, C. E. et al. (2006) Pleistocene within it are wary of approaches that are not rewilding: an optimistic agenda for 21st century con- strongly aligned with the ideas of John Muir. As servation. The American Naturalist, 168, 660–681. this debate takes up increasingly more ink in aca- Ferraro, P.J. & Pattanayak, S.H. (2006) Money for nothing? A call for empirical evaluation of biodiversity conserva- demic journals, new insights from palaeoecology tion investments. PLoS Biology, 4, e105. challenge our views of what is natural, economic Folch, J., Cocero, M.J., Chesné, P., et al. (2009) First birth of development continues to influence almost every an animal from an extinct subspecies (Capra frontiers of biogeography 6.1, 2014 — © 2014 the authors; journal compilation © 2014 The International Biogeography Society 27 C. Josh Donlan — De-extinction in a crisis discipline

pyrenaica pyrenaica) by cloning. Theriogenology, 71, Redford, K.H., Padoch, C. & Sunderland, T. (2013) Fads, fund- 1026–1034. ing, and forgetting in three decades of conservation. Halpern, B.S., Pyke, C.R., Fox, H.E., Chris Haney, J., Schlaepfer, Conservation Biology, 27, 437–438. M.A. & Zaradic, P. (2006) Gaps and mismatches be- Rosner, H. (2013) Is conservation extinct? A new look at pre- tween global conservation priorities and spending. serving biodiversity. Ensia, July 2013. Available at: Conservation Biology, 20, 56–64. http://ensia.com/features/is-conservation-extinct/ Hughes, W. (2013) Numbers count: caste-specific component (last accessed 06 March 2014). Allee effects and their interactions. Journal of Animal Scientific American Editors (2013) Why efforts to bring extinct Ecology, 82, 923–926. species back from the dead miss the point. Available Jule, K.R., Leaver, L.A. & Lea, S.E.G. (2008) The effects of cap- at: http://www.scientificamerican.com/article.cfm? tive experience on reintroduction survival in carni- id=why-efforts-bring-extinct-species-back-from-dead- vores: a review and analysis. Biological Conservation, miss-point (last accessed 06 March 2014). 141, 355–363. Sherkow, J.S. & Greely, H.T. (2013) What if extinction is not Kareiva, P. & Marvier, M. (2012) What is conservation sci- forever? Science, 340, 32–33. ence? Bioscience, 62, 962–969. Sorice, M, Oh, C., Gartner, T., Sniekus, M., Johnson, R. & Kumar, S. (2012) Extinction need not be forever. Nature, 492, Donlan, C.J. (2013) Increasing participation in incen- 9. tive programs for biodiversity conservation. Ecological Kurzwell, R. (2005) The singularity is near. When humans Applications, 12, 1146–1155. transcend biology. Penguin Books, New York. Soulé, M. (2013) The “New Conservation”. Conservation Biol- Lalasz, R., Kareiva, P. & Marvier, M. (2011) Conservation in ogy, 27, 895–897. the anthropocene: beyond solitude and fragility. Thomas, M.A., Roemer, G.W., Donlan, C.J., Matocq, M., Dick- Breakthrough Journal, issue 2. Available at http:// son, B.G & Malaney, J. (2013) Gene tweaking for con- thebreakthrough.org/index.php/journal/past-issues/ servation. Nature, 501, 485–486. issue-2/conservation-in-the-anthropocene/ (last ac- Veitch, C. ., Clout, M.N. & Towns, D.R., eds. (2011). Island cessed 06 March 2014). invasives: eradication and management. IUCN, Gland, Luque, G.M., Giraud, T. & Courchamp, F. (2013) Allee effects Switzerland in ants. Journal of Animal Ecology, 82, 956–965. Zimmer, C. (2013) Bringing them back to life. National Geo- Mark J. (2013) Back from the dead. Earth Island Journal, 28, graphic, April 2013. Available at http:// 30–37. ngm.nationalgeographic.com/2013/04/species- Pew Research Center (2013) Living to 120 and beyond: revival/zimmer-text (last accessed 06 March 2014). American’s views on aging, medical advances and radical life extension. Pew Research Center, Washing- Submitted: 9 September 2013 ton D.C. Redford, K.H. & Adams, W. (2009) Payment for ecosystem Accepted: 20 January 2014 services and the challenge of saving nature. Conserva- Edited by Matthew Heard tion Biology, 23,785–787. Redford, K.H., Adams, W. & Mace, G.M. (2013) Synthetic biology and conservation of nature: wicked problems and wicked solutions. PLoS Biology, 11, e1001530.

frontiers of biogeography 6.1, 2014 — © 2014 the authors; journal compilation © 2014 The International Biogeography Society 28