Contributions to conservation biology and conservation genetics

In the late 1980's I moved away from molluscan systems and devoted more time to the growing field of conservation genetics. Some 25 publications are listed in this general theme, and others are listed in the following themes if they concerned with specific mammals or birds. My early studies, like that describing allozyme variation and differentiation in Africa and Indian rhinoceroses (Publication 102) were frustrated by the difficulties of tissue acquisition. I noted this challenge is a review of the problems of conserving genes and species (Publication 99) and devoted several years to developing noninvasive [non-destructive] genotyping methods to get around it. Publication 119 announced our first successes: in the context of that review article I provided the first evidence that DNA could be amplified from non-human primate hair and from bird feathers. Although published in a relatively obscure journal, this report precedes others that claim precedence for these breakthroughs by more than a year. Three other “firsts” using noninvasive [non-destructive] genotyping methods are noteworthy”:

  • conducted pioneering genetic studies of whole populations of free-ranging mammals and birds, especially chimpanzees, marmosets, lemurs and loggerhead shrikes.
  • provided the first demonstration that animals could be censused [individually counted and sexed genetically] without ever seeing them. Graduate student, Lori Eggert, conducted the first genetic survey of wild African elephants using DNA amplified from dung (Publications 205, 210).
  • provided the first demonstration that genetic erosion in small isolated populations could be monitored. Graduate student Sukamol Srikwan’s work on small mammals trapped on islands in a new reservoir garnered international attention (Publication 192).

Noninvasive genotyping for studies of population structure, mating system, genetic censusing and phylogeography

Our contributions to the introduction of noninvasive genotyping have led to numerous field studies of primates and other vertebrates. Publications 138, 155 and 209 review the rapid adoption of the new methods and their application to a great diversity of species and phenomena. Although many other laboratories have contributed to this revolution I get some pride from the fact that my former graduate student, Philip Morin, was the first to successfully work with both non-human primate hair and bird feathers. He, and graduate student Pascal Gagneux, made numerous significant discoveries about our closest relatives, the chimpanzees. Gagneaux also published a much-cited cautionary analysis on the errors encountered in genotyping from shed hair and other degraded templates (Publication 167). With postdoctoral fellows Nick Mundy and Caroline Nievergelt this approach was extended to populations of marmosets and lemurs and with several graduate students I have been working to resolve the phylogeny of the gibbons. I reviewed the triumphs and tragedies of noninvasive genotyping’s first decade (Publication 209).

Monitoring genetic erosion in fragmented populations by noninvasive genotyping

A set of seven contributions concern the process of genetic erosion. I completed a 6-year study of the effects of rainforest fragmentation on population viability of small mammal populations in Thailand. I regard this contribution as one of my most significant as it involves the successful demonstration of a new method of monitoring genetic erosion noninvasively. The most significant result derives from Sukamol Srikwan's thesis (1997) research and provides the first real-time demonstrations of genetic erosion in fragmented populations of free-ranging animals based on surveys of variation at microsatellite loci (Publication 192).

In southern Thailand, a hydroelectric dam flooded the forested Khlong Saeng valley in 1987 and left 150 rainforest fragments as islands in Chiew Larn reservoir. The area lay in the heart of a 3,500 km2 protected forest and was little disturbed by human activities. We monitored the effects of this habitat fragmentation on the population viability of 12 species of small mammals in these now isolated habitat patches during 1990–1995. Mark-recapture surveys on island and matched mainland sites by graduate students Tony Lynam and Sukamol Srikwan showed that habitat fragmentation led to rapid density decreases or local extirpation of half the species on the smaller islands and to the onset of genetic erosion in surviving populations of the three commonest species. This is one of the first projects to examine both ecological and genetic effects of rainforest fragmentation on mammals in the first decade following habitat alteration. The project has great generality throughout the increasingly fragmented humid tropics as small mammals are indicators of forest ecosystem functioning. The policy implications of our research are that populations in fragmented forests may require both ecological and genetic management if they are to survive and provide ecological services.

The effects of genetic erosion on the viability of small populations following habitat fragmentation are understood in theory but the critical early stages of the process have gone undocumented as the changes are rapid and difficult to monitor. Graduate student, Sukamol Srikwan and I found it is possible to monitor genetic erosion in recently fragmented populations by noninvasive genotyping using hypervariable nuclear microsatellite loci as markers of variability. We studied changes in variability due to genetic drift and inbreeding in populations of three small mammals (forest rat, Maxomys surifer, tree mouse, Chiropodomys gliroides, and tree shrew, Tupaia glis) on island forest fragments in the reservoir in years 5–8 post-fragmentation. Demographic and genetic responses to fragmentation were species-specific, reflecting differences in life history and behavior. Rates of genetic erosion differed in different species but allelic variation was invariably lost faster than heterozygosity. Small, recently isolated populations lose variation faster than allowed for in current conservation practice and genetic erosion may commence before the onset of obvious demographic decline. We are now employing these methods to monitor genetic erosion in isolated populations of elephants, animals that are more typically the focus of conservation efforts.

Publications

76. Woodruff, D.S. and O.A. Ryder. Genetic characterization and conservation of endangered species: Arabian oryx and Pere David's Deer. Isozyme Bulletin 19:33. (1986d).
Note: First surveys of allozymic variation in two species (both extirpated in the wild) revealed very little variability in the captive animals. I ran the gels using tissues provided by Oliver Ryder (San Diego Zoo). [No. of citations: 9]

78. Templeton, A.R., H. Hemmer, G. Mace, U.S. Seal, W. Shields and D.S. Woodruff. Local adaptation, coadaptation and population boundaries. In: Genetic Management of Captive Populations. K. Ralls and J. Ballou, eds. Zoo Biology 5(2):115–125. (1986f).
Note: I participated in the Smithsonian Institution workshop that produced this and other multi-authored reviews. [No. of citations: 64]

99. Woodruff, D.S. The problems of conserving genes and species. In: Conservation for the Twenty-first Century. Western, D. and M. Pearl, eds. Oxford University Press, New York, pp. 76–88. (1989b).
Note: This review article was widely used in university seminar courses in the following few years. [No. of citations: 71]

100. Western, D., M.C. Pearl, S.L. Pimm, B. Walker, I. Atkinson and D.S. Woodruff. An agenda for conservation action. In: Conservation for the Twenty-first Century. Western, D. and M. Pearl, eds. Oxford University Press, New York, pp. 304–323. (1989c).
Note: I participated in the conference at Rockefeller University that produced this volume and this synthesis. [No. of citations: 16]

102. Merenlender, A.M., D.S. Woodruff, O.A. Ryder, R. Koch and J. Vahala. Allozyme variation and differentiation in Africa and Indian rhinoceroses. Journal of Heredity 80(5):377–382. (1989e).
Note: First survey of allozymic variation in three endangered rhinoceros species. Our report set a basis for the subsequent studies of wild populations and subspecies boundaries. Graduate student, Adina Merenlender, and I analyzed the samples provided by Ryder (San Diego Zoo), Koch (London Zoo) and Vahala (Dvur Kralove Zoo). [No. of citations: 30]

115. Woodruff, D.S. Genetically based measures of uniqueness. Commentary. In: Preservation and Valuation of Biological Resources. Orians, G.H., et al, eds. University of Washington Press, Seattle, pp. 119–132. (1991b).
Note: Discusses the notion that species can be defined and delimited genetically; a commentary on the accompanying paper by Janis Antonovics. [No. of citations: 4]

118. Woodruff, D.S. Genetics and the conservation of animals in fragmented habitats. In: In Harmony with Nature. Proceedings of the International Conference on Tropical Biodiversity. June 12–16, 1990. Malay Nature Society, Kuala Lumpur, Malaysia. pp. 258–272. (1992k).
Note: Review of the genetic implications of forest fragmentation in Southeast Asia on the survival and continued evolution of animal populations. Invited paper to mark the 50th anniversary of the Malay Nature Society. [No. of ISI citations: 5]

119. Woodruff, D.S. Genetics and demography in the conservation of biodiversity. Journal of the Science Society of Thailand 16(3/4):117–132. (1990i).
Note: In the context of this invited review I published the first evidence that DNA could be amplified from non-human primate hair and from shed bird feathers. Although published in a relatively obscure journal, this report precedes others that have claimed precedence for introducing noninvasive genotyping by a year or more. [No. of citations: 21]

121. Gilpin, M., G.A.E. Gall and D.S. Woodruff. Ecological dynamics and agricultural landscapes. In: Integrating Conservation Biology and Agricultural Production. Agriculture, Ecosystems and Environment 42:27–52. (1992b).
Note: This is a co-authored synthesis of discussions at the international Conservation Biology and Agriculture conference held at Asilomar in May & November 1988. [No. of citations: 13]

122. Woodruff, D.S. and G.A.E. Gall. Genetics and conservation. In: Integrating Conservation Biology and Agricultural Production. Special Issue of Agriculture, Ecosystems and Environment 42:53–73. (1992c).
Note: I chaired the genetics working group at the international Conservation Biology and Agriculture conference at Asilomar in 1988 and prepared this synthesis. [No. of citations: 8]

132. Lynam, A.J., S. Srikwan and D.S. Woodruff. Species persistence and extinction following rainforest fragmentation at Chiew Larn, Surat Thani Province, Thailand. Science Society of Thailand, 18th Congress on Science and Technology of Thailand. October 27–29, Bangkok, Thailand. Abstracts. pp. 570–571. (1992l).
Note: Two dissertations resulted from this 5-year NSF-funded study. The first major paper to emerge from Lynam's PhD thesis is: Lynam, A.J. 1997. Rapid decline and loss of small mammal diversity in monsoon evergreen forest fragments in Thailand. In W.F. Laurance, R.O. Bierregaard, Jr. and C. Moritz (eds.) Tropical Forest Remnants: Ecology, Management and Conservation of Fragmented Communities. Univ. Chicago, Chicago. pp. 222–240. Srikwan's thesis: Srikwan, S. 1998. Genetic erosion in small mammal populations following rain forest fragmentation in Thailand. University of California, San Diego (see also publication 192)

138. Woodruff, D.S. Non–invasive genotyping of primates. Primates 34(3):333–346. (1993d).
Note: First review of my research on chimpanzees and gibbons. The Editor of this journal shared my manuscript with a colleague and delayed the publication of this paper by one issue thus enabling his colleague to get a paper out establishing publication priority with our methods. [No. of citations: 51]

150. Woodruff, D.S. Biodiversity: conservation and genetics. In: Environment, Science and Technology: The Challenge of the 21st Century. Vol. 1, Proceedings of the 2nd Princess Chulabhorn Science Congress. Bangkok, Thailand, November 2–6, 1992. Chulabhorn Research Institute, Bangkok, pp. 589–598. (1999d).
Note: an introduction to current issues in biodiversity conservation based on my lab group’s work in Southeast Asia. [No. of ISI citations: 7]

155. Morin, P.A. and D.S. Woodruff. Non-invasive genotyping for vertebrate conservation. In: Molecular Genetic Approaches in Conservation. Smith, T.B. and R.K. Wayne, eds. Oxford University Press, pp. 298–313. (1996b).
Note: Review of the fruits of the first five years of the application on noninvasive genotyping methods to species of conservation concern. Woodruff and his former graduate student, Phil Morin, reviewed the application of the methods they helped introduce in 1989. [No. of citations: 65]

156. Srikwan, S., D. Field and D.S. Woodruff. Noninvasive genotyping of free–ranging rodents with heterologous PCR primer pairs for hypervariable nuclear microsatellite loci. Journal of the Science Society of Thailand 22:267–274. (1996c).
Note: Graduate students Sukamol Srikwan and Dawn Field and I describe methods for the development of heterologous primer pairs for microsatellite loci that were used in Srikwan's thesis research on genetic erosion. [No. of ISI citations: 1]

167. Gagneux, P., C. Boesch and D.S. Woodruff. Microsatellite scoring errors associated with non-invasive genotyping based on nuclear DNA amplified from shed hair. Molecular Ecology 6:861–868. (1997f).
Note: Very important analysis of the false homozygote problem associated with the, by then, widely used noninvasive genotyping method based on shed hair. Gagneux was technically Boesch's graduate student at Basel but in reality worked in my laboratory for 5 years. [No. of citations: 237]

192. Srikwan, S. and D.S. Woodruff. Genetic erosion in isolated small-mammal populations following rainforest fragmentation. In: Genetics, Demography and Viability of Fragmented Populations. Young, A. and G. Clarke, eds. Cambridge University Press, pp. 149–172. (2001a).
Note: This chapter describes the key result of the genetic studies associated with the Khlong Saeng Biodiversity Project. Using noninvasive genotyping methods and panels of microsatellite loci, my graduate student Sukamol Srikwan found evidence for genetic erosion in populations of rodents and tree shrews in their first 20 generations post-fragmentation. This research demonstrates for the first time that genetic variability can now be monitored effectively and will hopefully lead to more attention being paid to the genetic aspects of population viability in species of conservation concern.
See also: Srikwan, S. 1998. Genetic erosion in small mammal populations following rain forest fragmentation in Thailand. PhD thesis, University of California, San Diego. [No. of citations of this paper: 39; of the book: 172]

194. Woodruff, D.S. Populations, species and conservation genetics. In: Encyclopedia of Biodiversity. Vol. 4. Levin, S., ed. Academic Press, San Diego, pp. 811–829. (2000d).

200. Woodruff, D.S. Declines of biomes and biotas and the future of evolution. Proceedings of the National Academy of Sciences, USA 98:5471–5476. (2001d).
Note: This review was prepared after I chaired a panel discussion at the NAS colloquium on the future of evolution. I argued that the ultimate test of evolutionary biology as a science is not whether it solves the riddles of the past but rather whether it enables us to manage the future of the biosphere. Unfortunately, our inability to make clearer predictions about the future of evolution has serious consequences for both biodiversity and humanity. In this essay I outlined the predictable changes in the biosphere and the individual species that make it up and the actions we might take to mitigate the undesirable effects of the on-going mass extinction. I argued that bioneering, the interventionist genetic and ecological management of species, communities, and ecosystems in a postnatural world, is poised to become a growth industry. It is not the control of nature that we should seek but rather a deeper appreciation of the natural dynamics of these complex systems and a willingness to work with rather than against these dynamics. [No. of citations: 73]

202. Woodruff, D.S. Molecular genetic comparison of African and extinct Indian cheetah. In: The End of the Trail. The Cheetah in India by Divyabhanusinh. 2nd edition. Oxford University Press, New Dehli, India, p. 191. (2002a).
Note: My collaborator Divya is the world authority on Asian cheetah. He published this letter from me describing our work-in-progress in the second edition of his book. Based on genotyping three Indian cheetah shot in 1925, our results suggest the Asian cats were very similar to those found today in Namibia. A manuscript co-authored with Eggert and Divya is in preparation. [No. of ISI citations: 4]

204. Woodruff, D.S. Evolution of living fossils – paradox of the Coelacanth. [Keynote Lecture]. In: Aquamarine Proceedings Symposium. The Coelacanth, Fathom the Mystery. Aquamarine, Fukushima, pp. 5–7. (2002c).
Note: Based on my genetic work on the recent radiation of six species of Nautilus, I discuss the prospects for the discovery of still more species of coelacanth.

206. Srikwan, S., K. Hufford, L.S. Eggert and D.S. Woodruff. Variable microsatellite markers for genotyping tree shrews, Tupaia, and their potential use in genetic studies of fragmented populations. ScienceAsia 28:93–97. (2002e).
Note: A methods paper providing genetic markers for gene mapping and for studies of genetic erosion in tree shrews. Graduate student Srikwan used these methods to obtain her key results, published in Publication 191. She was assisted in the optimization of the PCR conditions by two fellow graduate students. [No. of citations: 7]

209. Woodruff, D.S. Non-invasive genotyping and field studies of free-ranging non-human primates. In: Kinship and Behavior in Primates. Chapais, B. and C. Berman, eds. Oxford University Press, Oxford, pp.46–68. (2003c).
Note: In 1989, when we introduced noninvasive genotyping, it represented a revolutionary solution to the dilemma that arose when the effects on behavioral studies of shooting, trapping and bleeding, or biopsy darting wild animals became unacceptable. Having contributed to the development of the now widely used methods I review the significant lessons learned during the course of the first 10 years, the dramatically improved genotyping techniques, and the prospects for the 2nd decade. [No. of citations: 12]

216. Woodruff, D.S. Genetics and the future of biodiversity. [Keynote talk] Proceedings of the 9th BRT Annual Conference. Pp. 20–29. (2006b)
Note: see also Theme 9 below.

C7. Pangan, K. E. & Woodruff, D.S. Conservation of captive populations: a demographic analysis of the Zoological Society of San Diego mammal collection, 1980–2004.
Note: this manuscript together with the next two has been re-written and the three together have been combined with a fourth on the interpretation of the results; this longer paper (C10) with three appendices is currently under review.

C8. Pangan, K. E. & Woodruff, D.S. Conservation of captive populations: a demographic analysis of the Zoological Society of San Diego bird collection, 1980–2004.

C9. Pangan, K. E. & Woodruff, D.S. Conservation of captive populations: a demographic analysis of the Zoological Society of San Diego reptile and amphibian collection, 1980–2004.

C10. Pangan, K. E. & Woodruff, D.S. Sustainability of captive populations: demographic analysis of the San Diego Zoo collection, 1980–2004, and the institutional transition from exhibition to conservation. Note: combining the data in the above three manuscripts with a longer analysis and discussion, manuscript C10 is currently under review.

When Chiew Larn Reservoir was flooded in 1987–1988, 90 small islands formed on hilltops in the Khlong Saeng valley, between Khao Sok National Park (south) and Khlong Saeng Wildlife Sanctuary (north). Up to 12 species of small mammals were trapped on the resulting islands of rain forest and their populations began to show the predicted effects of genetic erosion. A tree shrew population (right) began to lose significant microsatellite heterozygosity in the eight years post-fragmentation. This was the first demonstration that genetic erosion could be monitored non-destructively (Publication 192).

Within five years of the flooding of the Khlong Saeng valley all 12 species of small mammals had been extirpated from this 1 hectare island in Chiew Larn Reservoir. Over 32,000 trap-nights of live-trapping on matched island and mainland control sites enabled us to document patterns of species extirpation and genetic erosion in surviving populations following range fragmentation and isolation (see Publications 118, 132, 150, 192, 204 and 206).

Dr. Sukamol Srikwan used noninvasive microsatellite genotyping of a forest rat, a tree mouse and a tree shrew to provide the first demonstration that genetic erosion occurred rapidly and could be detected and monitored in recently fragmented populations of free-ranging mammals on large and small islands in Chiew Larn Reservoir (Publications 156, 192, 206).