Download 150. Woodruff, D.S. Biodiversity: conservation and genetics. In

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).
REVIEW
ARTICLE
A 149
BIODIVERSITY:
CONSERVATION AND GENETICS
DAVID S. WOODRUFF
Department of Biology
University of California, San Diego
La Jolla, California 92093-0116
USA
1. INTRODUCTION
The biodiversity of Thailand is the country's most undervalued and neglected
resource, both biologically and economically.l Yet the nation's plants and animals,
the communities they form, and the ecological services they provide are major assets
that have direct bearing on the quality of life today and in the future. Much of the
Twentieth Century was devoted to building a global consensus on the value of
nature conservation, and even in Thailand where environmental damage has been
enormous, the century closes with increased recognition that nature conservation is
in the national interest. Government condoned environmental destruction and
degradation is increasingly unacceptable to the population at large and major first
steps have been taken to begin to protect what remains of the national heritage.
Although this increased love and appreciation of nature are critical prerequisites for
environmental conservation they are unfortunately insufficient to insure future
generations the wealth and services of nature. Attention in Thailand and elsewhere
must now shift to developing and implementing the science and technology of
biodiversity conservation and community restoration. Environmental management
for human welfare requires more than just a change in societal and political attitudes:
nature, now disturbed, needs our active interventive stewardship. The purpose of
this paper is to draw attention to the hitherto widely ignored genetic aspects of
biodiversity conservation that will require more attention in the next century.
Integrating genetics into biodiversity conservation efforts constitutes one of the great
challenges of the Twenty-first Century -- a fitting focus for the Chulabhorn Research
Institute and this Congress on environment, science and technology.
2. BIODIVERSITY, GENETIC DIVERSITY AND FUTURE LIFE ON EARTH
The biosphere is that portion of the planet where physical conditions permit
life. These conditions, of temperature, oxygen concentrations, etc., occur and
persist only because of the activities of living organisms over the last 3.5 billion
years. This fact, that life sustains itself on an otherwise inhospitable planet,
provides the most important argument for the conservation of nature. The future
habitability of our only home depends on our living in harmony with the planet's
other organisms.
The biological diversity (biodiversity for short) of the planet embraces the
variety and assemblages of organisms at all levels of taxonomic and ecological
complexity. It involves the genetic variants (mutants, strains, races, subspecies)
belonging to the same species as well as the arrays of species and their higher
taxonomic groupings as monerans, protists, plants, fungi and animals. As very few
species can exist alone in nature, biodiversity also embraces the co-evolved
multispecies associations and communities responsible for ecosystem functioning.
Biodiversity thus embraces far more than just the species which are so often the
focus of conservation efforts. Excellent reviews of the status of biodiversity are
provided elsewhere.2-5
I will not belabor the nature and magnitude of the global biodiversity crisis.
Its significance is underscored by the 1992 UN Conference on Environment and
Development - the first true Earth Summit Locally, the situation in Thailand is
worse than in many countries: the largest mammals, birds, reptiles and fish are gone
or endangereds and the country's stocks of ecological capital have been depleted to
the point where human lives are lost and rural communities are becoming
dysfunctional. Natural resource based industries like forestry and tourism have been
seriously mis-managed for private profit rather than sustainability for the public
good. Suffice here to note that species extinctions and community degradation are
not inevitable results of development. In Thailand and elsewhere trends are being
reversed and biodiversity conservation is beginning to receive national political
attention.
AIL'ioughmost discussions of the biodiversity crisis focus on habitats and
species, conservationists are ultimately concerned with the genetic resources
underlying nature. Genetic diversity of individuals, populations and species
provides the raw materials from which our domesticated crops, animals and
microbes can be artificially selected. The clearest arguments for the valuation of
genetic resources come from specific agricultural, pharmaceutical and
biotechnological examples.Zf Less thought has been given, until recently, to the
role of this same genetic diversity in enabling species to persist, to continue to
evolve in nature in response to environmental change. If natural communities with
hundreds of interacting species provide valuable ecological services then the genetic
underpinnings of wild plants and animals are also of concern to biologists and
developers. In the present century biodiversity conservation has been left primarily
to ecologists, in the next century nature will also require genetic management.
Without such intervention species will continue to be lost and communities collapse.
Genetic engineering will have to add population and species-level conservation to its
traditional concerns.? The urgent challenge is now to develop the science of
conservation genetics together with the appropriate technology to prevent the
irreplaceable loss of more species, communities and ecological services. Failure to
accept stewardship of the genetic resources underpinning biodiversity wi11leave
humans on a duller and more dangerous planet
3.
CONSERVATION OF GENETIC DIVERSITY
Extinction, as Lande!" has noted, is fundamentally a demographic process
influenced by genetic and environmental factors. Before discussing these genetic
factors it is important to reiterate his opinion that for wild populations in natural or
seminatural environments, demography is likely to be of more immediate importance
than genetics in determining population viability. Genetic factors do not figure
among the four major courses of extinction (the Evil. Quartet): overkill, habitat
destruction and fragmentation, impact of introduced species, and secondary or
cascade effects. I I Thus, although genetic factors are major determinants of a
population's long-term viability, conservationists can do more for a threatened
population in the short-term by managing its ecology. Ecological management is
the cheapest and most effective way of conserving genetic diversity.
Having noted the interdependence of ecology and genetics in determining a
population's viability let us now examine two aspects of the conservation of genetic
diversity that require scientific research and technology development. The first
involves the mitigation of the effects of genetic erosion in small populations. The
second concerns the recognition and genetic management of evolutionarily
significant units (species, races, etc.).
Genetic Erosion.
I follow OuborgI2 in defining genetic erosion as the decrease in
heterozygosity and the loss of alleles from a population due to random genetic drift
and inbreeding. These inexorable processes that rob small isolated populations of
their viability are insignificant in larger populations and in populations connected
with one another as a metapopulation by frequent gene flow. Genetic drift (chance
loss of alleles during meiosis) leads to decreased heterozygosity and reduced genetic
diversity without regard for whether the alleles lost are beneficial or deleterious.
Inbreeding (mating of related individuals) also leads to a decrease in the frequency of
heterozygotes.
It may also lead to an increase of genetic disease as recessive
deleterious alleles are exposed in homozygous form. Such alleles. the genetic load
of all species, are routinely purged by natural selection in large outbred populations
and are rarely noticed. However, when historically outbred populations crash
following range destruction and fragmentation, the frequencies of deleterious alleles
can increase by drift and inbreeding faster than they can be culled. Genetic erosion
thus leads to reduced individual and population viability.
In theory, the rate of genetic erosion is simply related to effective population
size (Ne) such that the change in frequency of heterozygotes is 1/(2NeJ. An effective
population of 10 will therefore lose heterozygotes five times faster than an effective
population of 100. Note that in this formulation we are using the effective
population size (NeJ not the CCii5US population size (N). Ne is almost always less
than N as a variety of life history factors will reduce the number of genetically
effective or different individuals in a given population.
The predictions of
population genetic theory are that small populations lose genetic variations faster
than large populations and have lower levels of variation (heterozygote frequency
and allelic diversity). Genetic erosion in small recently fragmented populations may
thus contribute to their extinction.
The potentially deleterious consequences of genetic erosion are predicted by
the widely accepted axiom that genetic variability is positively correlated with
individual and population fitness. A central premise of evolutionary theory holds
that genetic variability (especially additive genetic variation) is a prerequisite for
adaptation by evolution. Without the variability to work on natural selection can do
little to improve a population's chances of surviving significant environmental
change. It follows that small, isolated populations have higher probabilities of
extinction than large widespread populations. Although this argument is supported
by theory and many observations it is not without its critics and conservationists
should be aware of these controversies.U
Some species with long histories of
inbreeding show little sign of genetic erosion and, in other species, individual fitness
does not appear to be related to genetic variability. In still other cases demographic
bottlenecks have actually increased the additive genetic variation in a population and
thus countered the predicted effects of genetic erosion.l+ It is important to
remember that there have been very few studies of genetic erosion in nature. Until
more research is undertaken and the apparent paradoxes resolved, genetic erosion
must be regarded as a potential but still unproven general enhancing factor in the
extinction process.
Such scientific uncertainties are typical in conservation biology and no
excuse for inaction. The possibility that genetic erosion is already threatening
fragmented populations of Thailand's endangered species is too serious to wait for
the resolution of the general issues.6,I5-I6 As noted at the outset, managers can take
immediate action to relieve the pressures on a population's genetic diversity by
confronting the Evil Quartet, by securing the population ecologically. With time,
they can begin to monitor population's genetic viability and counter loss of variation
with natural or artificial gene flow. Thais should not lose the opportunity to save
what is left of their genetic resources by waiting for the development of a better
theoretical understanding of the role of genetic erosion in human induced
extinctions. Although I have here followed convention in arguing that genetic
erosion works primarily by reducing individual fitness it is possible that it could act
in other ways. For example, if loss of genetic variation makes individuals more
susceptible to environmental variance then genetic erosion will be far more important
during this time of major global climatic change than it has been in the past
Evolutionarily Significant Units.
If populations and metapopulations are the units of ecology, subspecies and
species the units of systematists, and races and varieties the units of agriculturalists,
what units should conservation biologists focus their attention on. The answer, I
believe, does not matter, as long as the units selected involve individuals with a
common recent genetic history. Our goal should be to conserve natural
evolutionarily significant units (ESUs) regardless of how they originated or their
current taxonomic status. Our goal should be to conserve evolutionary potential, a
process requiring genetic diversity, rather than very narrowly defmed types or kinds
of organisms.8,17
Notwithstanding the need to focus on processes (ecosystem functioning and
evolutionarily significant units) it is clear that for the foreseeable future most
biodiversity conservation efforts will concentrate on species - the fundamental units
of nature. The power of the species-level focus is well illustrated by regional
Species Survival Plans, national Endangered Species Acts and the international
Convention on International Trade in Endangered Species. Species inventories are
used to identify biodiversity "hot-spots" and species distributions are mapped to
identify "gaps" in the protected area systems.
Species level conservation plans have both strengths and weaknesses. As
Thailand is beginning to place more emphasis on species management it is important
to review the weaknesses of this approach. First, the theoretical underpinnings of
the species concept are still under active development Experts still disagree on just
how species originate and how they should be defined.If Numerous species
concepts are debated among evolutionary biologists and even the currently most
popular biological, cohesion and phylogenetic species concepts may be hard to apply
to real world situations. Conservation biologists cannot wait for the resolution of
these issues; their energies and the enabling legislation behind their efforts must be
unfettered by such scientific debates. Second, the use of the species level approach
requires' conservationists to make choices among the many species requiring
attention. For pragmatic reasons we must allow that all species are not created equal
and carefully select those whose management might conserve whole ecosystems.
Such choices are very difficult and different groups around the world are
experimenting with programs targeting different types of species including
ecologically
pivotal keystone
species, umbrella species with Iarge area
requirements, charismatic megavertebrate flagship andfocal species, and species
that are especially vulnerable to human activitles.t? Other groups are trying to
identify and conserve ecologically sensitive management indicator species. Almost
everywhere evolutionary relics (living fossils) and local endemics are afforded
special consideration.
Rarity per se may not be a sufflcient criterion to merit
interventive management.w With limited resources conservationists in Thailand
must now try to objectively establish their priorities for effective biodiversity
conservation in the next century. Genetic data, as discussed below, comes into play
once the hard choices have been made.
Evolutionarily significant units, once selected for conservation management,
require prompt genetic assessment. Whatever their current taxonomic designation
(species, subspecies, unnamed but isolated geographic race) it is important to verify
their genetic integrity and innate variability. The consequences of failing to carry out
a full genetic study at this stage can be expensive, embarrassing and lead to loss of
genetic resources and extinction. Consider the following examples:
•
outbreeding depression led to the failure of a reintroduction program involving
ibex, Capra ibex, in Czechoslovakia. The program involved genetically distant
Turkish and Nubian subspecies; their hybrids were so poorly adapted that the
entire population went extinct 8
•
outbreeding depression led to reproductive waste (unnecessary deaths) in a
spider monkey, Ateles sp., breeding colony when different chromosomal types
were inadvertently mixed} 7
•
failure to recognize the natural pattern of genetic variation in an endangered
Sonoran topminnow, Poeciliopsis occidentalis, in Arizona and Mexico led to a
restocking plan with a l,righprobability of failure.l?
The prime purpose of genetic screening early in any taxon-based conservation effort
is therefore to preclude the inadvertent mixing of well-differentiated groups within a
single management program. This is especially important when the program
involves both in situ and ex situ efforts and reintroductions and translocations are
contemplated. Comprehensive genetic screening will also provide baseline data on
innate genetic variation and its partitioning within and between populations
(population structure).
Traditional taxonomy is often misleading when it comes to defining
evolutionarily significant units for conservation management. Most vertebrates and
flowering plants received their taxonomic names long before the development of the
biological species concept. Even conspicuous, well-known species may require reassessment The magnitude of the genetic difference between the two subspecies of
orangutan, Pongo pygmaeus+ and between the West African and the other
subspecies of chimpanzee, Pan troglodytest) suggests that they require separate
management. Large genetic distances (proportional to evolutionary divergence from
a common ancestor) must be taken into account for effective conservation
management
Genetic relationships between individuals, populations, subspecies and
species can be established by a number of laboratory methods. Karyotypes,
allozymes, mitochondrial DNA RFLP (restriction fragment length polymorphism)
patterns, mitochondrial and nuclear gene sequences have all been used effectively.
With sufficient tissue, time, expertise and money the genetic parameters of interest to
conservationists can all be estimated. That this was not done routinely in the past
reflects a failure of managers to appreciate the risks involved in ignoring genetics
and a real shortage of sufficiently motivated geneticists. Another problem is more
insidious and reflects the inadequacies of the infant science of conservation genetics.
Often laboratory studies provided managers with uninterpretable data or added
unacceptable complexities to on-going programs. In this regard it is worth noting
that genetic distance data alone may not answer the key question about an ESU's
homogeneity. The event of speciation is not simply related to genetic distance:
although large distances may indicate significant genetic differentiation accompanied
by speciation, small distances do not necessarily indicate that populations are
con specific, Interpretation of genetic data for management purposes typically
requires a simultaneous assessment of other patterns of variation (morphology,
distribution, ecology and behavior). Morphology, the criterion used traditionally to
define species is often unreliable, but coupled with genetic patterns permits the
recognition of ESUs in some of the taxonomically most challenging syngameons.t
I have argued that species generally provide the best focus for taxon-oriented
conservation but subspecific variants and unnamed isolated populations (restricted to
islands, mountain tops, river basins, etc.) may be equally meritorious.
Again,
taxonomic status of the target population is less important than the ecosystem and the
number of other species that will benefit indirectly from the conservation program.
What is important, is that target taxon be genetically defined and representative of
some natural ESU. Subsequent management of the ESU would then seek to
maintain or restore the genetic variability of the original population(s). Care would
also be taken to avoid "enlarging" the ESU by hybridization with individuals from
another species or subspecies. Failure to manage genetic integrity along these lines
resulted in the contamination of one line of endangered Przwalski's horse with
domestic horse genes and may have contributed to the extinction of the dusky
seaside sparrow. 22 In a last ditch attempt to save the latter species from the east
coast of Florida, the last birds were crossed with a subspecies from the west coast of
Florida rather than the more closely related Atlantic coast subspecies from further
north. Had genetic relationships among the taxa been established earlier this mistake
could have been avoided.
In managing threatened ESUs the creation of "generic" populations _
mixtures of previously isolated and well-differentiated subspecies, for example _
should be avoided. It is justified only when there are no alternatives as hybrid or
generic taxa are clearly preferable to the groups extinction. Such artificial hybrid
taxa and their natural equivalents can not be excluded from conservation
consideration simply because they lack racial "purity". Such a notion is obsolete and
runs counter to our present appreciation of the importance of conserving as much
genetic diversity as possible.
It is not the purpose of this paper to discuss the theory and methods of
managing genetic diversity once it is identified and characterized.
For recent
discussions of population viability analysis and metapopulation analysis and the
technologies of captive propagation the reader is referred elsewhere.23-29 Suffice it
to note that the conservation of genetic diversity requires a multidisciplinary
synthetic approach combining the best basic science with the pragmatism of the
traditional nature manager.
4.
RESEARCH INVOLVING THAI ANIMALS
I now offer a few examples from my own research to illustrate the
importance of considering genetic factors in biodiversity conservation.
The
examples were chosen to illustrate three common problems that managers will have
to deal with in the next century: proper identification of ESUs, selection of
appropriate individuals for reintroduction programs, and assessing levels of
variation remaining in remnant populations. In some cases the research was based
on proven methods, in others it is frankly experimental. In all cases it involved
collaboration between Thai scientists and managers and members of my laboratory
group in the U.S. In each case the expertise and technology has or will be
transferred to laboratories in Thailand.
Proper Identification of Evolutionarily Significant Units.
Three studies of freshwater molluscs and their parasites illustrate the
importance of proper identification of evolutionarily significant units even though the
animals themselves are not the subject of conservation efforts. First, allozyme
variation was used to show that 21 nominal species of Thai clams, Corbicula, are
actually all members of the same conchologically variable species, C.fluminea.30
This means that an effort to save the clams previously referred to C. erosa and found
only in Glaeng district, Rayong province, would betaxonomically unjustified,
More generally, the taxonomic revision of the clams indicates that attempts to
conserve the traditional "species" for their own sake would have been misguided.
Second, a similar allozyme study of a small snail in the Mekong and Mun rivers
revealed that "Neotricula aperta" is actually comprised of at least four separate
sibling species.t! Misidentification of ESUs in this case has important biomedical
implications as one or more members of the species group is the intermediate host of
the human blood fluke, Schistosoma mekongi, The third example involves this
snail-transmitted parasite which had been confused with the species S. japonicum
from Japan, China and the Philippines. Allozyme variation shows clearly that the
Thai schistosome is a different species and that it is more closely related to S.
malayensis than the widespread S. Iaponicum.n
These three examples show how
both taxonomic lumping and splitting can affect the definition of ESUs for
conservation purposes. Each case involved an animal that was relatively wellknown in Thailand (as a food source, disease vector, or pathogen) but the use of
traditional non-genetic taxonomy would have resulted in the adoption of
inappropriate units for conservation management.
Selection of Appropriately Matched Individuals for Reintroduction.
Translocation and reintroduction are increasingly important conservation
management tools. Two on-going projects illustrate the need to consider genetic
factors in planning such actions. The first case involves the threatened Eld' s browantlered deer, Cervus eldi, and the Royal Forest Department's propagation project at
Phu Khieo Wildlife Sanctuary in northeast Thailand. This is within the traditional
range of the Southeast Asian subspecies, C. e. siamensis, which has been extirpated
in Thailand. Deer moved to Phu Khieo include Laotian C. e. siamensis, and
individuals of C. e. thamin, a subspecies centered in Myanmar that may survive in
the ranges of western Thailand. Two questions arise: are the Burmese and Siamese
subspecies genetically compatible and is it alright to release the western subspecies
into the former range of the eastern subspecies? A very preliminary genetic
comparison in my laboratory suggests that the two subspecies are more different
than expected: 13 differences including 2 transversions were detected among 167
base-pairs of the mitochondrial cytochrome b gene sequence studied (Carlos Garza,
pers. comm.). If this result were confirmed and extended then it would seem
genetically inadvisable to mix the subspecies. Similarly, it may be preferable to
reintroduce Laotian deer to Phu Khieo rather than Burmese as long as the former are
available.
The second case involves the genetic management of captive gibbons,
Hylobates. The Thai Zoological Organization has long had a serious problem with
abandoned pet gibbons; in the mid-1980's up to 20 per month would be abandoned
at or turned over to the Dusit Zoo, Bangkok. CITES restrictions prevented these
animals from being placed in captive breeding programs outside Thailand and the
Thai zoos were ill-equipped to house, let alone breed, these threatened apes. One
long-term solution under discussion by officials of the Zoological Organization, the
Royal Forestry Department, concerned NGO's and primatologists would involve
rehabilitating and reintroducing selected individuals to sanctuaries within their
former range. One problem with this laudable idea is that the animals themselves are
of unknown geographic origin and there is some concern about inadvertently mixing
gibbons of diverse origin. White-handed gibbons, H. lar, for example, range over
1500 km from north to south in Thailand and several geographically defined but
morphologically indistinguishable subspecies have been named - the effects of
releasing northern gibbons into south Thailand and vice versa, and the viability of
intersubspecific hybrids are unknown. The solution to this problem is to learn the
geographic patterns of genetic variation in this species and use these data to establish
the probable region of origin of all candidates for reintroduction. Our first attempt to
do this failed; the 252 base-pair segment of the cytochrome b gene used was simply
not informative enough.V A second attempt with a more variable gene sequence is
now underway and promises to permit the sorting of captive far gibbons into
appropriate genetic groups.
Assessing Levels of Genetic Variation in Isolated Populations.
Managers need to be able to assess the extent and rate of genetic erosion in
recently fragmented and isolated populations.
This has not been attempted in
Thailand or elsewhere to any significant extent because of technical obstacles.
Animals had to be darted or captured and bled, and the tissue sample had to be
frozen immediately and transported to the laboratory on dry ice or liquid nitrogen.
For most free-ranging mammals and birds in remote areas this is too difficult to
contemplate. We have overcome these problems by developing a non-invasive
genotyping method which uses hair, feathers and even feces as the DNA source.34
We are now demonstrating the method's utility for assessing levels of genetic
variation in recently fragmented populations of small mammals in Khlong Saeng
Wildlife Sanctuary. At the same time we are testing theoretical predictions about
rates of genetic erosion by monitoring these populations for their first 10 years postisolation. The particular populations under investigation became isolated on small
islands in Chiew Lam Reservoir wben the River was dammed in 1987. The ongoing extinction processes in these forest fragments are described elsewhere. 15.35-6
It is premature to describe our genetic results and their significance.
5. CONCLUSION
The above research projects are suggestive of the urgent and enormous
challenge confronting scientists and managers in Thailand. To an outsider like
myself it is clear that in the last decade, despite horrific setbacks, there is a net
improvement in national efforts to conserve biodiversity. Increased interest among
students and academics, increased public perception of the importance of
biodiversity, increased interagency cooperation on conservation projects, improved
legal framework supporting conservation efforts, improved implementation of
government policies (a narrowing of the gap between words and deeds), increased
public intolerance for government condoned destruction of natural resources
including biodiversity are-among the highly encouraging signs that Thailand will
take the necessary steps to conserve her natural heritage, The research priorities and
infrastructure needs to meet this challenge are clearly defined in recent reports of the
Science Society of Thailand and the Royal Forest Departrnenut-t? what remains to
be seen is how fast these recommendations will be addressed and implemented.
Thailand is very fortunate in having a Royal Family whose members play
major roles in national conservation efforts. Their leadership has enabled numerous
foreign scientists like myself to make small contributions to such important national
efforts. Meeting the environmental challenges of the Twenty-first Century, as
Professor Dr. HRH Princess Chulabhorn correctly noted requires the cooperative
efforts of numerous specialists; it has been a privilege to collaborate with my Thai
colleagues in their critical endeavor.
Environmental conservation and nature
protection are global problems and together we must seek both local and global
solutions.
ACKNOWLEDGEMENTS
My collaborative research in Thailand would not have been possible without
permission of the National Research Council and the collaboration and support of
numerous colleagues including: Warren Brockelman, Alongkorn Mahannop, Chira
Meckvichai, Jarujin Nabhitabhata, the late Seub Nakhasathien, Schwarm Tunhikorn,
Suchart Upatham and Sawai Wanghongsa.This work was supported by grants from
U.S.A.I.D., U.S.N.S.F. and the University of California.
REFERENCES
1.
Science Society of Thailand (1991) Biodiversity in Thailand. Research
Priorities for Sustainable Development. Chulalongkorn University,
Bangkok.
24 p.
2.
McNeely, J.A., Miller, K.R., Reid, W.V., Mittermeier, R.A. and Werner,
T.B. (1990) Conserving the World's Biological Diversity. IUCN, WRI,
CI, WWF-US, The World Bank, Gland, Switzerland. 193 p.
3.
Wilson, E.O. (1992)
Cambridge. 424 p.
4.
Solbrig, O.T., ed. (1991) From Genes to Ecosystems:
Agenda for Biodiversity. Int'I. Union BioI. Sci., Cambridge.
The Diversity of Life. Harvard University Press,
A Research
5.
World Conservation Monitoring Centre (1992) Global Biodiversity: Status
of the Earth's Living Resources. Chapman & Hall, London. xx + 594 pp.
6.
Woodruff, D.S. (1991) Nat. Hist. Bull. Siam Soc. 38:163-177.
7.
Oldfield, M.L. (1989) The Value of Conserving Genetic Resources.
Sinauer Assoc., Sunderland,
Massachusetts. xvii + 379 p.
c,
8.
Woodruff, D.S. (1990) in The Preservation -and Valuation of Biological
Resources
(G.H. Orians et aI., eds.) pp. 119-132, University of
Washington Press, Seattle.
9.
Woodruff, D.S. and G.A.E. Gall (1992) Agri. Ecosystems Environ.
42:53-73.
10.
Lande, R. (1988) Science 241:1455-1460.
11.
Diamond, J. (1989) in Conservation for the Twenty-first Century. (D.
Western & M. Pearl, eds.) pp. 37-41, Oxford University Press, New York.
12.
Oubourg, N.J. (1993) On the relative contribution of genetic erosion to the
chance of population extinction. PhD thesis, Utrecht University. 151 p.
13.
Barrett, S.C.H. and Kohn, J.R. (1991) in Genetics and Conservation of
Rare Plants (D.A. Falk & K.E. Holsinger, eds.), Oxford Univ., New York.
pp.3-30.
14.
Carson, H.L. (1990) Trends Ecol. Evol. 5:228-230.
15.
Woodruff, D.S. (1992) in Proc. Int'I, Confr, Tropical Biodiversity. "In
Harmony With Nature." pp. 258-272, Malay. Nature Soc., Kuala Lumpur.
16.
Woodruff, D.S. (1993) J. Sci. Soc. Thailand, in press.
17.
Woodruff, D.S. (1989) in Conservation for the Twenty-first Century. (D.
Western & M. Pearl, eds.) pp. 76-88, Oxford University Press, New York.
18.
Waples, R.S. (1991) Definition of "Species" Under the Endangered
Species Act: Application to Pacific Salmon. NOAA Tech. Memorandum
NMFS FINWC-194. 29 pp.
19.
Noss, R.F. (1991) in Balancing on the Brink of Extinction.
The
Endangered Species Act and Lessons for the Future. (lK.A. Kohn, ed.)
pp. 227-246, Island Press, Washington, D.C.
20.
Mace, G.M. and Lande, R. (1991) Conserv. Bioi. 5:148-157.
21.
Morin, P.A., J. Moore and D.S. Woodruff
London, B249:293-297.
(1992)
Proc. Roy. Soc.
22.
Avise, J.C. and Nelson, W.S. (1989) Science 243:646-648.
23.
Fiedler, P.L. and S. Jain, eds. (1991) Conservation Biology: The Theory
and Practice of Nature Conservation, Preservation and Management.
Chapman & Hall, New York. 507 p.
24.
Falk, D.A. and Holsinger, K.E., eds. (1991) Genetics and Conservation of
Rare Plants. Oxford University, New York. ~83 p.
25.
Gilpin, M.E. and Hanski, I. (1991) Metapopulation Dynamics. Academic
Press, London, 336 p.
26.
Hedrick, P.W. and Miller, M. (1992) in Conservation of Biodiversity for
Sustainable Development (0.T. Sandlund, K. Hindar & A.D.H. Brown,
eds.) pp.70-87. Scandinavian Univ. Press, Oslo.
27.
Boyce, M.S. (1992) Annu. Rev. Ecol. Syst. 23:481-506.
28.
Moore, H.D.M., Holt, M.V. and Mace, G.M. (1992) Biotechnology and
the Conservation of Genetic Diversity. Zool. Soc. London, Oxford
University Press. 256 p.
29.
Ballou, J., M. Gilpin and T. Foose, eds. Population Management for
Survival and Recovery, Univ. of Chicago Press, in press.
30.
Kijviriya, V., E.S. Upatham, V. Viyanant and D.S. Woodruff
Amer. Malacol. Bull. 8:97-106.
(1991)
31.
Staub, K.C., D.S. Woodruff, E.S. Upatham and V. Viyanant
Amer. Malacol. Bull. 7:93-103.
(1990)
32.
Woodruff, D.S., A.M. Merenlender, E.S. Upatham and V. Viyanant
(1987) Am. J. Trop. Med. Hyg. 36:345-354.
33.
Garza, J.C. and D.S. Woodruff (1993) Molec. Phylogen. Evol. 2(1):
34.
Woodruff, D.S. (1993) Non-invasive genotyping of primates. Primates, in
,press.
35.
Lynam, A.J. (1992)
Abstracts. p. 289.
2nd Princess Chulabhorn Science Congress.
36.
Lynam, A.J., Srikwan, S. and Woodruff, D.S. (1992) 18th Congress on
Science and Technology of Thailand Abstracts. pp.570-571.
37.
Santisuk, T., et al. (1991) Plants for Our Future: Botanical Research and
Conservation Needs in Thailand. Royal Forest Dept, Bangkok. 48 p.