An Argument Supporting De-Extinction and a Call for Field Research Charli N

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opinions, perspectives & reviews frontiers of biogeography 8.3, e28431, 2016 opinion An argument supporting de-extinction and a call for field research Charli N. Davis1,2 and Matthew D. Moran1,* 1Department of Biology, Hendrix College, 1600 Washington Ave., Conway, AR 72032 USA 2Current address: Department of Biology, Gilbert Hall, Stanford University, Stanford, CA 94305-5020; *Corresponding author: [email protected]

Abstract. With recent advances in biotechnology, the resurrection of recently extinct species has become a possibility, provoking a debate about the wisdom of what has become known as de-extinction. Regardless of the current feasibility and ethical controversies over de-extinction, ongoing technological advancement is likely to result in resurrected species in the near future. In our opinion, de-extinction will be followed by proposals for reintroduction into the wild. We argue that this development could be valuable for the advancement of ecological understanding and conservation. However, the current con- versations are happening in a vacuum. We therefore call for the initiation of field experiments using physiological and ecological surrogates. This type of research could shed light on the potential impacts of resurrected animals on modern ecosystems. While this research would have challenges, it could provide valuable information on the ecology of the past and better prepare scientists and wildlife managers for de-extinction. Keywords. Conservation, de-extinction, field experiments, re-wilding, reintroduction

Introduction to de-extinction and framing ecosystem processes (McNaughton 1985, Van Au- the issues ken 2000, van Langevelde et al. 2003, Sandom et During the late Quaternary (<50,000 BP) and ex- al. 2014), it is reasonable to infer that many ex- tending into the present, numerous species have tinct megafauna were important in past ecological gone extinct across the globe (Koch and Barnosky processes (Johnson 2009, Gill 2014). In addition to 2006, Julien et al. 2007, Faith and Surovell 2009). Pleistocene megafaunal extinctions, species loss These extinction events have undoubtedly modi- has continued into historical times, with the cur- fied ecological functioning of many ecosystems. rent extinction process affecting almost all taxa, For example, the extinction of Pleistocene including species of all sizes. For example, the pas- megafauna from the Americas and Eurasia ap- senger pigeon (Ectopistes migratorius L.) with its pears to have changed the structure, diversity, immense populations probably would have had and composition of temperate, tropical, and bo- major impacts on forest structure in eastern North real ecosystems (Zimov 2005, Gill et al. 2009, Zi- American and initiated cascading effects through- mov et al. 2012, Doughty et al. 2013). For in- out the food web (Ellsworth and McComb 2003). stance, grasslands are some of the most threat- Similarly, the recent loss of multiple frog species ened ecosystems, in part because of the en- throughout the world is likely having major conse- croachment of woody vegetation, perhaps due to quences for ecosystems (Verburg et al. 2007). the reduction of megafauna browsers and in- While extinction has typically been consid- creases in herbivorous grazing animals (Van Auken ered permanent, recent technological advances in 2000, however see Ratajczak et al. 2012 for the genetic engineering and cloning have made the complexity of woody plant encroachment). Con- return of extinct species a possibility, a process sidering the role of extant large mammals in Afri- referred to as de-extinction (Sherkow and Greely can and Asian grasslands and savannas (Dirzo et 2013, Shapiro 2015). For example, CRISPR al. 2014), including their major influence on distri- (clustered regularly interspaced short palindromic bution and abundance of woody plants and in repeats) technology can be used to modify the frontiers of biogeography 8.3, 2016 — © 2016 the authors; journal compilation © 2016 The International Biogeography Society 1 front. biogeogr. 8.3, e28431, 2016 C. N. Davis & M.D. Moran — De-extinction and field research

genome of extant species to match the genome of pigeon and Carolina parakeet (Conuropsis carolin- closely related extinct species (Campbell and Hof- ensis L.), may have had cascading effects through reiter 2015). Simpler cloning technology might this system, including drastic alteration of plant also be used to resurrect more recently extinct communities (Ellsworth and McComb 2003). species in which intact genomes survive in tissue De-extinction could also re-establish more samples. Some near successes of de-extinction ancient evolutionary relationships, benefiting nu- include the Pyrenean ibex (Capra pyrenaica pyre- merous organisms. Evidence from living animals ciaca Schinz, which ultimately died, but was the suggest that de-extinction could substantially alter first animal of an extinct subspecies resurrected, ecosystem functioning, perhaps in ways that en- Folch et al. 2009) and the gastric brooding frog hance biodiversity. Extant megafauna, such as (Rheobatrachus spp. Liem) which survived through elephants (Asner et al. 2009), ungulates (Asner et the early larval stages (White 2013). It seems likely al. 2009), large cats (Jorge et al. 2013), canines that further improvements in technology will (Ripple and Beschta 2012), and giant tortoises make de-extinction a reality (Donlan 2014). (Hansen et al. 2010) have profound influences on De-extinction is distinctive from existing modern habitats. Historical reintroductions (e.g., conservation ideas, such as reintroduction and wolves in Yellowstone, bison in the Great Plains) rewilding, and has the potential to change conser- have demonstrated the impact that the reintro- vation strategies dramatically. Reintroduction has duction of large animals can have on ecosystems been a commonly used conservation tool to re- (Knapp et al. 1999, Hill et al. 2008, Ripple and store ecological functioning (Gibbs et al 2008, Rip- Beschta 2012). While the interaction of large ple and Beschta 2012). Rewilding landscapes over mammals in Pleistocene ecosystems were bound a large scale with extant species is a loftier goal to have been complex, we hypothesize that they (Samson et al. 2004). De-extinction is an even would be similar to living species. more radical idea that would bring back extinct Extinct animals may have been important species, which could then be added to existing or seed dispersers for many plants and may be re- re-wilded ecosystems. Indeed, if de-extinction sponsible for living anachronistic plants (Janzen becomes a reality, we believe that the next logical and Martin 1982). Elephants consume large quan- argument among some scientists would be rein- tities of fruit and disperse the seeds over long dis- troduction of these resurrected species into the tances (Dudley 2000, Campos-Arceiz and Blake wild (Shapiro 2015). 2011) in South Asia and Africa. Some plant species rely upon large grazers to remove competitively Potential benefits, risks, and challenges dominant plant species (Olff and Ritchie 1998). It Benefits seems probable that extinct megafauna had simi- De-extinction is likely to happen, assuming tech- lar ecosystem-wide effects. Therefore, it is possi- nological challenges can be overcome. While not ble that de-extinction would provide additional all scientists advocating de-extinction are also in ecosystem services that current biological com- favor of reintroduction, this process is of particu- munities cannot. lar interest to ecologists and conservation biolo- Ironically, resurrecting extinct animals could gists (Donlan 2014). Reintroduction—especially if also improve the chances of preserving the ge- the extinct species represent unique ecological netic legacy of extant animals. For example, a niches not represented by extant species—could cloned mammoth would presumably be created be of particular ecological value. For example, the by altering the genetic code of the Asian elephant deciduous forests of North America are missing a (Elephas maximus L.) to create a cold-adapted large number of recently extinct and ecologically organism (Shapiro 2015). If these animals were unique species that appear to have been impor- then re-introduced to an environment where they tant in structuring this community. The loss of im- can be well-protected, the Asian elephant genome portant seed predators, such as the passenger would also be partially preserved, an important

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goal considering the plight of extant elephants in advance of actual de-extinction, such as working their native range (Wittemyer et al. 2014). under the International Union for Conservation of Nature (IUCN) guidelines or other cooperative Risks agreements. Risks of de-extinction include invasiveness, dis- The social aspects of de-extinction are also ease transmission, and unforeseen species inter- varied and important. These include concerns that actions (Donlan et al. 2006, Sherkow and Greely it will misallocate conservation funds (Mark 2013) 2013, Donlan 2014). These risks are evident with and will relax public sentiment for conservation modern introductions (Pejchar and Mooney (Donlan 2014). Several authors have argued that 2009), so caution and pre-emptive protocols conservation funds will be transferred from tradi- would be prudent to mitigate risk. In case of un- tional conservation programs to riskier de- foreseen problems, response plans also need to extinction programs (Ryder 2002, Redford et al. be developed. However, it is not clear how these 2013). Others have argued that de-extinction ef- risks from resurrected species would be different forts will bring in new sources of money, in par- from traditional reintroduction programs, even ticular from biotechnology companies (Jones though these are widely supported by the scien- 2014). For instance, the Ark Corporation was de- tific community and the public (Donlan 2014). We veloped specifically for de-extinction efforts with support the argument that de-extinction, if ac- money that was unlikely to be utilized for tradi- companied by introduction to the wild, is compa- tional conservation work (Regalado 2013). If ex- rable to reintroductions of extirpated populations tinction was viewed as reversible, would de- (Jørgensen 2013, Jones 2014, Seddon et al. 2014). extinction reduce public interest in conservation? Reintroduction of extirpated populations, with While possibly an issue, conservation support is varying levels of success, have included mammals already in decline, and by all evidence inadequate (e.g., wolves; Ripple and Beshta 2012), reptiles to arrest species extinction (Kareiva and Marvier (e.g., Galapagos tortoises; Gibbs et al 2008), plants 2012). It is also possible that resurrection of ex- (Godefroid et al. 2011), and arthropods (Shepherd tinct species could increase public awareness and and Debinski 2005). These reintroductions also excitement for conservation. involved intense human activity such as captive breeding, efforts to maintain genetic variation, Challenges and intense monitoring after release. These activi- Feasibility is a major challenge to de-extinction ties often succeeded in the goal of reestablish- and effective reintroduction (Jones 2014). Some ment of ecological interactions, often with sub- authors have suggested that cloning or genetic stantial environmental benefit. Perhaps the most engineering will never produce a population large noteworthy was wolf reintroductions in the Yel- enough and with enough genetic diversity to be lowstone Ecosystem, which appear to have had viable (Ehrlich 2014), a problem for many small wide-ranging and profound ecological effects, populations, illustrated by the ongoing genetic many beneficial to biodiversity (Ripple and hurdles with the Florida panther (Puma concolor Beschta 2012). Noteworthy is that most reintro- coryi Bangs; Johnson et al. 2010). An additional duced populations in the U.S. are designated issue is that many species have locally adapted “experimental” for management purposes and populations (Grady et al. 2011), genetic diversity can be removed if necessary (e.g., red wolves in that would almost certainly be impossible to rec- the Great Smokey Mountains; Henry 1998). We reate from the limited samples available from the fully expect and recommend that any reintroduc- Pleistocene remains of extinct animals. However, tion of a resurrected species be treated the same many conservation success stories have shown way, which would presumably lessen environ- that small populations with little genetic diversity mental risk. Since conservation laws vary by coun- can give rise to large and biologically viable popu- try, international cooperation is likely necessary in lations if allowed to expand sufficiently (e.g.,

frontiers of biogeography 8.3, 2016 — © 2016 the authors; journal compilation © 2016 The International Biogeography Society 3 front. biogeogr. 8.3, e28431, 2016 C. N. Davis & M.D. Moran — De-extinction and field research Table 1. Basic ecological questions about Pleistocene ecology that could be studied, methods of study, and selected examples. Questions? Research Method Feasible Example Are current plant communities Controlled introduction of analog Study effect of Asian or African elephants on novel because of Pleistocene species to habitat North American vegetation with semi-wild

Extinction? animals and replicated exclosures How did extinct animals inter- Controlled introduction of analog Replicated large plots with horses with bison act with surviving species? species to habitat where living together, separate, or both absent (2X2 fac- species persist torial design) How did the extinction of Pleis- Controlled introduction of analog Study carbon and nitrogen cycles on habitats tocene animals affect ecosys- species to habitat with analog species compared to replicated tem function? exclosures Effect of high diversity grazing Introduction of analog species Re-creation of Pleistocene grazing/browsing community of the Pleistocene and extant native species in ap- community in the Great Plains of U.S. with all compared to the lower diver- propriate habitat living megafauna plus elephants, horses, sity community of the present camels, and tapirs as analogs. Compare to replicated exclosures How did Pleistocene extinction Laboratory feeding trials with Feeding of fruits to captive elephants (and affect seed dispersal? analog species other analogs); retrieve seeds from dung and test for survival and growth

northern elephant seal; Mirounga angustirostris efforts progress, a realistic educational system Gill; Bonnell and Selander 1974). It has also been must be enacted to accompany it. Educational argued that there is no remaining habitat for ex- programs in schools and outreach by public and tinct species (Pimm 2013). While habitat loss has private conservation organizations, similar to reduced many habitats to non-viable ecosystems, what is done with traditional conservation efforts, many areas still remain. Temperate North Amer- would need to be implemented. ica, where large areas of relatively intact habitat remain and many native species survive, would be Preparing for the future a good candidate for reintroduction of resurrected Current research on several species, including species. The High Plains in particular (especially mammoths (Shapiro 2015), the passenger pigeon parts of eastern New Mexico, Colorado, and Wyo- (Hung et al. 2013), and the gastric brooding frog ming) contain many large ranches with unplowed, (White 2013), is increasing the likelihood of at native grasslands, several of which contain a least some resurrected species in the near future, nearly full complement of modern flora and and that arguments for reintroduction will follow. fauna—even healthy numbers of large animals Since we predict that de-extinction will become a such as elk, pronghorn, and mountain lion reality, we wish to make a call to action to per- (Wilkenson and Turner 2013). While small animals form field research. We hope that this type of re- would be difficult to contain, if de-extinction and search will pre-emptively answer questions, such reintroduction includes large mammals, some of as potential species interactions of resurrected these areas could conceivably be fenced similar to species, the nature of old evolutionary relation- some African parks (e.g., Lake Nakuru National ships, and past and future ecosystem functioning Park; Mwangi and Western 1997) to prevent dam- (Table 1). This type of research could also mitigate age to surrounding private lands and communi- potential risks. ties. It has been hypothesized that many current There will also undoubtedly be cultural limi- ecosystems are novel, because of the extinction of tations to de-extinction, including substantial con- megafauna (Gill et al. 2009). Several paleoecolo- cern from government agencies and the general gists have suggested that the extinction of Pleisto- public (Shapiro 2015). Therefore, as de-extinction cene megafauna changed North America from a

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grazer/browser dominated ecosystem to one con- clines in mosses and shrubs. Also interesting was trolled by fire, which may have had important an apparent change in ecosystem processes that consequences for plant species diversity (Johnson models indicate could modify greenhouse gas 2009). For example, grazing can reduce the fre- emissions by reducing methane release (Zimov et quency and intensity of fire, allowing woody al. 2012). A similar park, Askania-Nova in the plants to become established, which then influ- Ukraine, has a mixture of native and introduced ences the abundance of browsing animals ulti- surrogates living in a natural environment, but a mately controlling woody plant encroachment literature review finds very little research, with (van Langevelde et al. 2003, Sankaran et al. 2008). the exception of studies on Przewalski’s horse be- Although studying the effects of de-extinction is havior (Equus ferus przewalskii Poliakov; Zharkikh seemingly paradoxical—since we do not have any et al. 2009). The current conflict in the area, how- formerly extinct animals to study—there are rea- ever, makes ecological research difficult. Perform- sonable alternatives. The most obvious solution ing similar experiments in other locations (with would be the use of extant ecological and evolu- more political stability) and habitats where extinc- tionary analogs (Donlan 2005, Donlan et al. 2006). tions occurred would expand our knowledge of Recent preliminary experiments from our potential effects of de-extinction. laboratory have shown that some North American Such experiments, although logistically chal- plant species survive and grow better after pass- lenging would be reasonably practical. One field ing through the digestive system of elephants, experiment we propose is the interaction of bison, compared to native seed dispersers (Boone et al. pronghorn, horses, and elephants on the Great 2015). This study suggests that important ecologi- Plains of the United States. Bison (Bison bison L.) cal relationships could be re-established through and pronghorn (Antilocarpa Americana Ord) are de-extinction. Living elephants are considered native, while the horse (Equus ferus caballus) and physiologically and ecologically similar to extinct elephants (Loxodonta or Elephas) would be appro- elephants from Eurasia and the Americas (Kalb et priate analogs for the extinct North American al. 1996, Dudley 2000; but see Green et al. 2005), horses (Equus spp.) and Mastodons (Mammut and these could be utilized to perform additional spp. Blumenbach), respectively. Fossil evidence more complex field experiments. Captive ele- suggests that bison, pronghorn, horses, and elephants could be introduced into field sites to phants were some of the most abundant mam- study grazing, browsing, trophic cascades, and mals during the Pleistocene (Guthrie 1968, disturbance impacts on plant and animal commu- Spencer et al. 2003). This quartet is ecologically nities, similar to research that has been per- similar to the Serengeti-Mara group consisting of formed by the reintroduction of other large mam- zebra, wildebeest, gazelle (two species), and Afri- mals, such as bison (Knapp et al. 1999, Moran can elephant. This combination of grazers (zebra: 2014) and wolves (Ripple and Beschta 2012). low-quality grass, wildebeest: high-quality grass), Reintroduction of large mammal analogs browsers (gazelles), and ecosystem engineer- has been initiated by scientists in Asia with the browsers (elephant) has a profound effect on eco- establishment of the “Pleistocene Park” along the system functioning (McNaughton 1985). Bison, Kolyma River in northeastern Siberia (Zimov pronghorn, and horses are widely available in the 2005). They have reintroduced Yakutian horses western U.S. For example, the National Bison As- (Equus ferus caballus L.), Muskox (Ovibos mo- sociation organizes the trading of bison among schatus Zimmermann), and Wisent (Bison bonasus ranchers, and conservation groups often sell ex- L.). Acquiring animals for the project has been cess animals (Robert Hamilton, Tallgrass Prairie challenging and not without set-backs, so results Preserve Director, personal communication). are preliminary. However, the researchers have There is also a surprisingly large number of captive already shown substantial changes in plant com- elephants in zoos, circuses, and sanctuaries in munities, including an increase in grasses and de- North America (several hundred animals; Mason

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et al. 2009). With the increasing concern for ele- cational efforts are at promoting positive action phant welfare in captivity, returning them to a for conservation, with evidence suggesting that wild or semi-wild environment could find public the zoo experience does little to improve knowl- support. Although not directly related to conser- edge or motivate people to act on behalf of con- vation, the ethics of keeping highly intelligent and servation (Kellert and Dunlap 1989, Mazur and social animals, such as elephants, in captivity is Clark 2001, Kuhar et al. 2010). Thus, it has been very suspect. Providing a place in the wild for hypothesized that a more in situ approach to con- them to live more natural lives, especially if they servation focusing on ecological processes and cannot be returned to a true wild state in their realistic human-animal relationships would be native range, would be more ethically defensible more effective in conservation (Hutchins and Con- than the current model of captivity. way 1995, Mazur and Clark 2001). Engaging in There would no doubt be difficulties in in- breeding and introducing resurrected species troducing elephants to wild habitats. Modern could be an advancement for the future of zoos. Asian and African elephants are tropical animals, For example, the Northern white rhinoceros not tolerant of cold weather, and they have com- (Ceratotherium simum cottoni Lydekker) is almost plex social structure not easy to replicate in cap- certain to go extinct soon since natural reproduc- tive populations. Therefore, they would most tion of the remaining individuals is unlikely likely have to be introduced in a semi-wild condi- (Swaisgood et al. 2006). Technology developed tion where they have access to shelter during the through de-extinction studies could be applied to colder months of the year, but would be able to this living species which currently exists only in interact with the native ecosystem the rest of captivity. time. Unbeknownst to many ecologists, there are While the above experiments would help two facilities in the United States that house ele- elucidate some possible effects of de-extinction, phants in this way: The Elephant Sanctuary in Ten- there are several caveats. Unlike large mammals, nessee and the Performing Animal Welfare Soci- it is much more difficult to design experiments to ety in California. Both of these facilities allow ele- determine the effects of small species reintroduc- phants to roam over relatively large areas of natu- tion, because their analogs would presumably be ral and semi-natural habitats, while the facilities more mobile and more difficult to contain in a provide shelter when necessary. Experiments us- controlled study (but see Heske et al. 1994 for an ing this type of partially wild situation would be an example of small rodent exclosures). Apex preda- excellent prelude to resurrected animals that tors present other unique challenges, including would be physiologically adapted to the North large habitat area requirements, low fecundity, American climate. and high risk of human conflict. Furthermore, the Experimental reintroductions would not population regulation of analog species would have to be limited to the four species described have to be performed by humans, unless all spe- above. Another formerly common Pleistocene cies interactions could be established within the mammal group in North America was the study system. camelids. Extant species of camels from South America or Asia could be experimentally intro- Conclusion duced to North American habitats as an additional Our basic argument therefore is to do the field browser (Donlan et al. 2006). Other examples of research. Debates about the morality and ethics potential surrogate species include modern tapirs, of de-extinction are of great importance, and it is peccaries, and a variety of predators. imperative that we proceed with caution, but de- De-extinction efforts could be paired with extinction is likely to occur in the near future re- conservation organizations such as zoos to propel gardless, assuming technological obstacles are conservation forward to save species that still sur- overcome (Donlan 2014). Once extinct animals are vive. Currently, it is unclear how effective zoo edu- resurrected, proposals for reintroduction are likely

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to follow. If this proposal occurs, then the impor- Donlan, C.J., Berger, J., Bock, C.E., et al. (2006) Pleistocene ‐ tant goals are to assure that we get the most eco- rewilding: an optimistic agenda for twenty first cen- tury conservation. The American Naturalist, 168, 660– logical and scientific benefits from the process, 681. while minimizing risk. Debates about the ecologi- Doughty, C.E., Wolf, A. & Malhi, Y. (2013) The legacy of the cal impacts are currently being undertaken with- Pleistocene megafauna extinctions on nutrient avail- ability in Amazonia. Nature Geoscience, 6, 761–764. out enough data, yet the research that would an- Dudley, J.P. (2000) Seed dispersal by elephants in semiarid swer these questions is possible, despite being woodland habitats of Hwange National Park, Zim- logistically challenging. By bringing together ecolo- babwe. Biotropica, 32, 556–561. Ehrlich, P.R. (2014) The case against de-extinction: it’s a fasci- gists, social scientists, and conservation minded nating but dumb idea. Yale Environment 360 Report- organizations, it might be possible to address ing, Analysis, Opinion & Debate. Digital resource these ecological questions and proceed with de- available at http://e360.yale.edu/feature/ the_case_against_de- extinction using good science. Not only will this extinction_its_a_fascinating_but_dumb_idea/2726/. research guide us toward responsible de- Ellsworth, J.W. & McComb, B.C. (2003) Potential effects of extinction actions, it will also provide exciting in- passenger pigeon flocks on the structure and composition of presettlement forests of eastern North formation on past ecological and evolutionary his- America. Conservation Biology, 17, 1548–1558. tory of our planet. Faith, J.T. & Surovell, T.A. (2009) Synchronous extinction of North America's Pleistocene mammals. Proceedings of the National Academy of Sciences Acknowledgments USA, 106, 2064–2065. Thanks to R. Dirzo, H. Mooney, D. Gordon, and P. Folch, J., Cocero, M.J., Chesné, P., et al. (2009) First birth of an animal from an extinct subspecies (Capra Seddon who provided valuable comments to an pyrenaica pyrenaica) by cloning. Theriogenology, 71, earlier draft of this manuscript. Several anony- 1026–1034. mous reviewers provided valuable comments and Gibbs, J.P., Marquez, C. & Sterling, E.J. (2008) The role of greatly improved the paper. This work was sup- endangered species reintroduction in ecosystem restoration: tortoise–cactus interactions on Española ported in part by the J. Keith Sutton Research Island, Galápagos. Restoration Ecology, 16, 88–93. Award to C. N. Davis. Gill, J.L. (2014) Ecological impacts of the late Quaternary megaherbivore extinctions. New Phytologist, 201, 1163–1169. 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