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Genome Resource Banks

Author(s): David E. Wildt, William F. Rall, John K. Critser, Steven L. Monfort and Ulysses S.
Seal
Source: BioScience, Vol. 47, No. 10, AIBS: The First 50 Years (Nov., 1997), pp. 689-698
Published by: Oxford University Press on behalf of the American Institute of Biological Sciences
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Genome Resource Banks
Living collectionsfor biodiversityconservation

David E. Wildt, William F. Rail, John K. Critser, Steven L. Monfort, and Ulysses S. Seal

B iological diversity is the key to (Foose 1987). But achieving this tar-
maintaining life as we know it get for tigers in nature would require
(Wilson 1992). However, rap- Organized banking of a habitat free of human disruption
idly growing human populations biomaterials from that is at least 25,000-50,000 km2
place extraordinary pressures on eco- (Foose 1987), or approximately the
systems, such as large-scale environ- wildlife species could combined areas of Maryland and
mental destruction, habitat conver- New Jersey. The reality for tigers
sion, habitat fragmentation, and provide important and many other species is that there
pollution. One reaction to these prob- is too little contiguous space left to
lems has been the emergence of con- benefits and options to sustain free-living populations. As
servation biology, an assemblage of habitats become smaller and more
scientific disciplines that are focused biotic managers isolated, the species occupying these
on sustaining biodiversity through a habitats also become more vulner-
cooperative synthesis of ideas, infor- terized as "quaint" given the reali- able to inbreeding depression, dis-
mation, and approaches. ties of the current and future world ease epidemics, natural disasters, and
Virtually all conservation biologists (Soule 1992). Some battles for main- social and political change.
agree that habitat preservation is the taining large, protected ecosystems Other approaches for helping to
best way to conserve biodiversity. Set- have already been lost. One species preserve biodiversity have been pro-
ting aside large tracts of land so that that has been adversely affected by posed. Soule (1991) has described a
they are free from human interfer- habitat loss is the tiger (Panthera "biospatial hierarchy" to protect
ence can protect many species, but tigris): Of the eight tiger subspecies biodiversity, beginning at the top
this approach has also been charac- that were recognized as endangered with whole ecosystems (in situ pro-
in 1969 by the IUCN-World Conser- tection) and proceeding down
David E. Wildt (e-mail:dewildt@shentel. vation Union, three (Panthera tigris through communities, species, popu-
net) is programhead and a codirectorof vigata, P. t. sondaica, and P. t. balica) lations (ex situ zoo breeding pro-
NOAHS (New Opportunitiesin Animal are now extinct, and one (P. t. grams), and eventually to cryobanked
HealthSciences),and StevenL. Monfortis biomaterials. In this article, we refer
an endocrinologistand researchveterinar- amoyensis, the South China tiger) is
critically endangered, with fewer to this last strategy as genome re-
ian in the ReproductivePhysiologyPro- source banks (GRBs), which are re-
than 80 individuals remaining in the
gram, at the Conservation& Research positories of systematically collected
Centerat the National Zoological Park, wild (Table 1;Jackson 1993). More-
SmithsonianInstitution,FrontRoyal, VA over, fewer than 400 Siberian tigers germ plasm (gametes), embryos,
22630. WilliamF. Rallis a cryobiologistin (P. t. altaica) exist in isolated pockets blood products, tissue, and DNA for
the EmbryoCryopreservation Unit of the of eastern Russia, northeast China, defined conservation programs.
NationalCenterfor ResearchResourcesat and North Korea (Jackson 1993).
theNationalInstitutesof Health,Bethesda, Fewer than 500 wild Sumatran tigers
MD 20892-5590. JohnK. Critseris scien- Existing genome
(P. t. sumatrae) live on Sumatra, resource banks
tific directorof the CryobiologyResearch
Instituteat theAdvancedFertilityInstitute, largely in five fragmented protected
areas (Tilson and Brady 1992). The concept of GRBs is not new.
Methodist OutpatientCenterNorth, In-
dianapolis,IN 46202. Ulysses S. Seal is Approximately 250 tigers are Already, biomaterials from farmed
chairmanof the ConservationBreeding needed in a population to sustain crop plants and animals are stored
SpecialistGroupof the IUCN-WorldCon- adequate genetic diversity, which is systematically, a development driven
servationUnion's Species SurvivalCom- defined as 90% of the current gene largely by economics and by the de-
mission,AppleValley,MN 55124. variation for the next 100 years sire to ensure secure food sources.

November 1997 689

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Table 1. Estimated numbers of tigers in nature and in zoos. cedures must be modified and opti-
mizedfor eachspecies(Watson1995).
Panthera tigris subspecies Naturea Zoos Nevertheless, AI is simpler than
P. t. altaica 250-400 623b other reproductive techniques. Em-
P. t. sumatrae <500 245b bryo transfer involves the collection
P. t. tigris 3000-5300 297b of embryos from a donor female (ei-
P. t. amoyensis 30-80 50c ther after mating or after AI), fol-
P. t. corbetti 800-1400 68d
lowed by the implantation of the
aJackson 1993 CYinghong 1995 embryos into a surrogate female at
bMueller and Wesul 1995 dTilson et al. 1995 the appropriate stage of her repro-
ductive cycle. The benefit of embryo
Large-scale, organized repositories zoa, bacteria, bacteriophages, cell transfer is, in theory, that a hor-
of germ plasm are more common for lines, hybridomas, fungi, yeasts, re- mone-stimulateddonor will ovulate
plants than for animals, in part be- combinant DNA materials, and vi- many more ova than normal, most
cause it is technically easier to store ruses available for worldwide distri- of which have the potential of be-
plant than animal germ plasm (i.e., bution. coming embryos.These embryoscan
seeds of many plants can simply be be frozen or immediatelytransferred
dried and stored in refrigerators at 4 to one or more surrogates that ges-
Reproductive technologies
?C or -20 ?C; Wildt 1997). Animal associated with GRBs tate the embryos to term, with the
agriculture has, however, benefited offspringhavingthe original donor's
from large-scale sperm and embryo The usefulness of banked germ plasm genotype. For example, a cow usu-
cryostorage for the purpose of im- and embryos from humans, livestock, ally produces only one calf per preg-
proving meat and milk production and laboratory animals depends on nancy. However, a genetically valu-
in domestic livestock. In addition, a assisted reproduction procedures, able female that is given hormones
few programs bank biomaterials which include tools such as artificial can produce many embryos, each of
from animal models used in biomedi- insemination (AI), embryo transfer, which can develop in the reproduc-
cal research to protect the long-term and in vitro (test-tube) fertilization tive tract of a less valuable cow. By
availability of standard genotypes of (IVF). These procedures are some- avoiding pregnancy, the original
mice, rats, hamsters, rabbits, cats, times enhanced by other techniques, donor can be used to produce even
and dogs, ensuring that researchers such as intracytoplasmic sperm in- more embryos to rapidly proliferate
are working with uniform animal jection (ICSI), in which an individual her valuable genes. The significant
models that give repeatable results. sperm cell is microinjected into an challenges to cryo-preserving em-
Transgenic technology (the abil- oocyte to create an embryo. Because bryos include determining both the
ity to incorporate novel genes into a single semen sample often contains embryonicdevelopmentalstage that
injected embryos) has also resulted millions (or billions) of sperm, this is most likely to withstand freezing,
in the production of thousands of sample has almost unlimited fertili- as well as the best cryoprotectants
new animal models. Although this zation potential, assuming that oo- and optimal rates of cooling and
technology has exponentially in- cytes are available and that ICSI is thawingto avoid membranelysis and
creased research opportunities, the successful. embryo death.
byproduct is a proliferation of ani- The ability to artifically insemi- Even more complex is IVF,
mal colonies that require expensive nate a female to produce young was whereby sperm are mixed in a cul-
housing and care. One solution is to demonstrated more than 200 years ture dish with oocytes that are aspi-
cryopreserve sperm and embryos ago by the Italian priest Spallanzani, rated directly from a female's ova-
from genotypes that are not in use using the dog (Asdell 1977). But AI ries using a needle guided by fiber
currently but are potentially valu- is more complicated than merely ran- optic or ultrasonictechniques.Given
able in the future. The Jackson Labo- domly placing sperm into a female. the appropriate culture conditions,
ratory in Bar Harbor, Maine, and the Basic knowledge of reproduction and any embryos that result can then be
National Institutes of Health in timing are essential. One must know, either cultured and transferredto a
Bethesda, Maryland, collect and for example, when a female ovulates recipient host or cryopreserved for
cryostore embryos and, occasionally, and where in the reproductive tract later transfer. The challenges are
sperm from animal models, usually is the most appropriate site to de- similar to embryo transfer except
rodents. Customized collections have posit sperm. Using cryopreserved that additionalknowledgeis required
also been developed for microorgan- sperm adds more challenges. Gametes to safelycollect good-qualityoocytes
isms that are used in the environ- are delicate, water-filled cells, and if and sperm and appropriately pro-
mental, food, and biomedical indus- their structure and function are to cess them to stimulate fertilization
tries to produce products valued at survive cryopreservation, they must and development.
tens of billions of dollars (Cunning- be properly dehydrated and rehydrated In theory, it should also be pos-
ham 1994). The American Type Cul- through the use of cryoprotectants sible to store unfertilized oocytes.
ture Collection (ATCC) in Rockville, (compounds that stabilize cell mem- However, unfertilized oocytes are
Maryland, is the research community's branes) and precise cooling and thaw- much harder to cryopreserve than
leader in cold storage, with more ing rates that minimize ice-induced embryos because the haploid female
than 80,000 cultures of algae, proto- cell lysis. Sperm cryopreservation pro- gamete is highly susceptible to chill-

690 BioScience Vol. 47 No. 10

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ing injury and cryoprotectant toxic- nature, where its presence helps to for "ideal" matings to fail after ani-
ity (Parks and Ruffing 1996). This protect native habitat. mals have been shipped long distances.
susceptibility is thought to be associ- Therefore, when rare species are bred
ated with the unique characteristics Insurance. Small populations are strictly on the basis of genetics, there
of mature oocytes, namely their large vulnerable to environmental catas- will always be a need for assistance,
size and the presence of a meiotic trophes, political upheavals, and dis- perhaps using cryopreserved germ
spindle and cortical granules in the ease outbreaks. The detrimental ef- plasm or embryos and assisted breed-
ooplasm (Candy et al. 1994). fects on small populations of ing techniques such as AI, embryo
perturbations ranging from oil spills transfer, and IVF.
Application of GRBs to to wars to viral epidemics are well
wildlife species known. For instance, the black- Resolving space problems by reduc-
footed ferret (Mustela nigripes) ing the number of living animals
Given the historical success of stor- nearly became extinct in the Ameri- needed to meet genetic diversity tar-
ing and using biomaterials from live- can West, first due to extermination gets (Ballou 1992). One of the great-
stock and the growing popularity of of its prey (prairie dogs) by ranchers est challenges faced by modern zoos
this approach for management of and then to an epizootic outbreak of is that too little space is available to
laboratory animals and microorgan- canine distemper in the 1980s (Seal maintain too many species, subspe-
isms, it is natural to consider the et al. 1988). In retrospect, a random cies, and populations. Thousands of
potential advantages of cryobiology sampling of germ plasm from the species deserve attention, but zoos
for protecting and conserving wild- wild population before the disease have only enough space to poten-
life. Technological advances once epidemic could have saved more of tially conserve fewer than 1000
used only for humans and domestic the original genetic diversity, which unique taxa by conventional breed-
animals are now finding relevance for is now lost forever. The black-footed ing programs (Conway 1986). GRBs
wild animal species and are increasing ferret is not unique-most of Earth's could make cooperative zoo breed-
the need for the systematic collection biodiversity exists in habitats that ing programs more efficient. For ex-
and storage of biomaterials. Orga- are sensitive to epizootic disease out- ample, as many as 300 animal spaces
nized banking of biomaterials from breaks and drastic shifts in human are needed to retain 90% of the ex-
wildlife species could provide im- social and political structure. Sys- isting diversity in each regional tiger
portant benefits and options to bi- tematic "snapshots" of biomaterials population that is managed by coop-
otic managers. would help to preserve extant, wild erative zoo programs. Using cryo-
genetic diversity in a living archive. preserved sperm and AI, only 160
Easy, inexpensive movement of ge- These biomaterials then could be spaces would be needed because the
netic material among living popula- rederived in emergencies, such as near sperm of selected males would be
tions. One goal of conservation man- extinction. available from liquid nitrogen, rather
agers is to maintain healthy, genetically than from living animals (Johnston
diverse animal and plant populations. Extended generation interval. Ge- and Lacy 1991, 1995). Newly cre-
GRBs can mitigate the effects of un- netic diversity is lost only when ani- ated space could be reallocated to
natural selection pressures, genetic mals are no longer available to re- other species in crisis.
drift, and inbreeding depression by produce (Ballou 1992). As long as
providing a source of germ plasm viable cryopreserved sperm or em- A resource for blood, tissue, and
(i.e., of new genes) that can be in- bryos remain stored, genes do not DNA. Usually the concept of frozen
fused into small or fragmented popu- die with the animal. Banked germ repositories of biomaterials is asso-
lations. For example, rather than plasm can be used long into the future. ciated with germ plasm and embryos.
transporting stress-sensitive wild For example, cattle sperm that have But collecting and storing blood and
animals from one site to another, been cryopreserved for 37 years retain tissues is also important because these
genetic heterogeneity could be main- fertilization capacity (Leibo 1994). materials can be processed into se-
tained by shipping germ plasm or rum, plasma, blood cells, DNA, and
embryos. It may also be technically Increased efficiency of captive breed- tissue and cell cultures. These
feasible to artificially inseminate free- ing. Many rare species in zoos are biomaterials have wide-ranging ap-
living females with sperm from males managed strictly to maximize ge- plications for studying genetic varia-
of other wild, or even captive, popula- netic diversity as part of cooperative tion, phylogeny, paternity, and the
tions. The latter approach has already zoo breeding programs (Hutchins processes underlying diversity, such
been made part of the conservation and Wiese 1991). Curators routinely as gene flow, selection, and mating.
management plan for Sumatran tigers identify desirable animal pairings Molecular techniques have been used
living in highly fragmented Indone- (e.g., Animal A should be mated with to address many practical conserva-
sian habitats (Tilson and Brady Animal B) on the basis of the need to tion issues, including measuring the
1992). Moreover, a GRB could re- retain a target level of genetic diver- extent of hybridization in the endan-
duce or eliminate the need to remove sity for the species. However, these gered Florida panther (Felis concolor
animals from the wild to support individuals will not necessarily be coryi) and assessing the impact of
captive populations. Instead, "sur- sexually compatible. Like people, 200 years of slaughter of humpback
plus" germ plasm would be collected, nonhuman animals have sexual part- whales (Megaptera novaeanglia) on
leaving the entire wild population in ner preferences, and it is not unusual levels of modern genetic diversity

November 1997 691

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blood samples had been periodically
collected and cryopreservedfor over
Collections a decade, scientists had the raw ma-
terials to determinethe time between
Museums Zoos and Genome the emergence of this morbillivirus
botanical Resource and the onset of lion morbidity and
gardens Banks mortality.
Economic opportunities for improv-
ing the agriculturaleconomy and the
quality of life, especially when wild
4 species hybridize with domesticated
livestock. For example, in Southeast
Asia wild cattle occasionally leave
their dense forest habitat and mate
Objectsand Living Biological with common domestic cattle to pro-
nonliving organisms materials duce hybridcalves (Vietmeyer1983).
organisms The resulting hybrid vigor makes
wild cattle species attractive for
Past/Present Present Present/Future boosting the quality of local meat-
...... III
producing stocks. A GRBwould not
/
........... .. ...
-qq

only protect the biodiversity of na-


tive wild cattle stocks through the
Figure 1. Various collections of biological materials. Whereas traditional museums,
zoos, and botanical gardens collect materials from the past and present, genome long-termpreservationof sperm,but
resource banks (GRBs) offer enormous opportunities for the future. also enhance animal agriculture
throughthe shareduse of germplasm
with local cattle producers.
Thus, the benefits of GRBs for
wild animals arise largely from the
need to effectively manage small
populations in natureor in captivity.
Scientists routinely survey and col-
lect animalsand plantsas studyspeci-
mens. Cryobankedgerm plasm, em-
bryos, tissue, blood, and DNA would
be another type of collection, but
one with considerably more conser-
vation potential than provided by
the conventional collections of ob-
jects, plants, and animals found in
traditional museums, botanical gar-
dens, and zoos (Figure 1).

Germ plasm cryopreservation


for wildlife
Severallaboratorieshave proven the
biological viability of cryopreserved
sperm or embryos for species as di-
Figure 2. Eld's deer fawns produced by artificial insemination with frozen-thawed verse as the bighorn sheep (Ovis
sperm from genetically valuable sires. The Eld's deer is an endangered species that canadensis), the chimpanzee (Pan
is indigenous to Southeast Asia.
troglodytes), and the giant panda
(Ailuropoda melanoleuca; Wildt et
(O'Brien1994a, 1994b). All of these over time can be screenedto identify al. 1993). We have taken this ap-
analyses requiredthe collection and the onset and cause of a particular proachfurtherby demonstratingthat
storage of blood products and tis- epidemic in natural or captive popu- cryopreservedsperm can be used to
sues. These biomaterialsare also im- lations. One illustration is the recent help managesmall populations. One
portant for practical health and sur- epizootic outbreakof canine distem- example is the Eld's deer (Cervus
vival issues. For instance, blood per that was fatal to as many as 30% eldi), which is endangeredthrough-
samples are a resource for develop- of the lions (Panthera leo) in the out its natural range in Southeast
ing indices of clinical well-being. Serengeti ecosystem in Tanzania Asia (Figure 2). Specialists in as-
Biomaterialsthat are cryopreserved (Roelke-Parkeret al. 1996). Because sisted reproduction,cryobiology, en-

692 BioScienceVol. 47 No. 10

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docrinology, animal husbandry,vet- Figure 3. Cheetah cub
erinary medicine, and behavior col- produced by artificial
laboratedto develop conditions that inseminationat the Rio
allow AI to succeed. So far, 15 fawns Grande Zoo in Albu-
have been born from AI using querque,New Mexico,,
with frozen-thawed
cryopreservedspermfromgenetically spermthatwascollected
valuablemales (Figure2; Monfort et from a wild, free-rang-
al. 1993), and half of them have been ing cheetahin Namibia
translocatedto the SingaporeZoo to and then transported
begin a captive breeding and educa- transcontinentally.
tion programin a region that is close
to their original habitat. even among closely .- !
The cheetah provides another ex- related species (Wildt ii-, . |l
ample of the use of assisted repro- et al. 1992). The de-
duction to manage a small popula- tailed mechanisms
tion. For centuries, this species has of reproduction are
reproduced poorly in zoos. More known for fewer
than a decade of reproductive, ge- than 100 species,
netic, and medical studies in the field many of them live-
and in zoos were needed to obtain stock and laboratory
the essential physiological data to animals. Intensive
consistently produce cheetah cubs study of the repro-
by AI (Howard et al. 1992). Nine ductive biology of
cheetah litters have been born from wild animals, espe-
artificially inseminated females, in- cially those that are
cluding two recent births in North unrelated to labora-
America sired with sperm from wild- tory and livestock
caught males of Namibia; the sperm animals, is needed to .^. .
had been cryopreserved and shipped generate appropri-
transcontinentally(Figure3). Although ate basic knowledge :-
the sperm donors were released and so that AI, embryo
later found killed, their genes remain transfer, and IVF
available in frozen sperm that is now can be used, when necessary, to help Again, basic technological research
known to be capable of producing manage endangered populations. is needed to provide the answers. For
offspring. The ability to effectively All aspects of reproductive biol- example, magnetic resonance imaging
cryopreserve sperm from this species ogy require attention, especially the (a technique that is commonly used in
eliminates the need to ever remove sensitivity of gametes and embryos the assessment of human health) has
another cheetah from the wild to of different taxa to the stresses of recently revealed a major obstacle to
support zoo breeding programs. freezing and thawing. In some cases, the cryopreservation of fish em-
Meanwhile, the GRB provides a re- only minor refinements will be bryos-namely, a multinucleated
serve of disease-free gametes that needed to ensure that a cryopreserved layer of nonyolky cytoplasm (the yolk
could help to restore the cheetah sample is viable on thawing. How- syncytial layer) that prevents ad-
population in Namibia in the event ever, many scientific advances and equate movement of cryoprotectant
that a local catastrophe severely de- new techniques will be required to compounds into and out of the em-
pletes the population. overcome inevitable problems. For bryo (Hagedorn et al. 1996).
The Eld's deer and cheetah ex- example, it is necessary to develop
amples are the first indications that the ability to cryopreserve oocytes. Practicalimplementationof
reproductive technology can assist And because most gamete biologists GRBs for conservation
in the practical management of en- are mammal-centric, sophisticated
dangered species. Until recently, cryopreservation studies need to be Collecting and storing biomaterials
wildlife was rarely propagated suc- extended to the gametes and em- from diverse species is one challenge,
cessfully by AI, embryo transfer, or bryos from taxa whose reproductive but their judicious use is quite an-
IVF. Progress has been slow because biology has been largely ignored, in- other. The most serious potential
reproductive techniques that were cluding birds, reptiles, amphibians, pitfall is the development of spuri-
developed for cattle or humans can- fishes, and invertebrates. Many spe- ous, disorganized collections that
not be readily applied to animals as cies will present formidable chal- have no particular conservation pur-
different as gorillas (Gorilla gorilla), lenges. For example, AI with frozen- pose and are unlinked to nature.
orinoco crocodiles (Crocodylus in- thawed sperm is relatively common Repositories should also not become
termedius), and Puerto Rican parrots in the breeding and management of static warehouses of biodiversity or,
(Amazona vittata). Biological mecha- fish (Harvey 1993), but fish embryos worse, "gene morgues" that are com-
nisms regulating reproductive fitness have never been cryopreserved suc- posed of dead or nonviable materials
amongtaxaarediverse,varyinggreatly cessfully, despite vigorous attempts. (Goodman 1990).

November 1997 693

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One goal of the planning process
Resources Conservation is to determine the type and amount
and funding justification of biomaterials to collect, store, and
use to achieve genetic management
targets. For example, how many
Technical issues related Knowledge of life sperm must be collected from a given
to collection, storage, / historyand male of a given genetic value that is
use, monitoring, naturalreproduction
living in a given population? Com-
and ownership puter simulations allow many of these
issues to be addressed, using infor-
mation about the reproductive biol-
Type and amount Knowledge of
of biomaterials "assisted reproduction" ogy of the species combined with
to store specific conservation goals. Such
analyses show that even the inter-
mittent, occasional use of frozen
sperm can greatly enhance a manager's
Accessibility of Demographic ability to achieve genetic goals
donors for banking Successful distribution (Johnston and Lacy 1995, Wildt and
Genome Resource of "donors"and Seal 1994). These analyses further re-
Banking "recipients" veal the need for three banks for
in situ and ex situ each species, one designated an "in
perpetuity" repository (for use only
Figure 4. Factors that need to be considered in developing a GRB for an animal when the species approaches extinc-
taxon or species, with an emphasis on reproductivebiomaterials. tion), another for routinely manag-
ing living animals, both in situ and
ex situ, and yet another containing
How can GRBs be implemented Seal 1995). A GRB "Action Plan" biomaterials available for research
for conservation? The Conservation concept has been formulated to steer (i.e., nonpropagation purposes).
Breeding Specialist Group (CBSG) stakeholders through the many pit- The action plan also deals with
of the IUCN-World Conservation falls associated with cryobanking ac- the technical aspects of collection,
Union's Species Survival Commis- tivities. Specific guidelines have been storage and use, research needs, fund-
sion has addressed this question as a developed on writing an action plan ing of the GRB, and proprietary is-
part of its overall mission. CBSG, (CBSG 1992). Furthermore, a proto- sues. In the case of ownership of rare
with a worldwide network of 700 type GRB action plan has been de- biomaterials, participants from the
members, serves as a neutral catalyst veloped for the tiger (Wildt et al. CBSG workshops have agreed that
and facilitator for conservation plan- 1995), a species chosen because of nations have sole responsibility for
ning for animals, plants, and habi- its precarious status in nature and its determining the ownership and value
tats (and maintains a Web site at charisma (which will attract atten- of their genetic resources within in-
www.cbsg.org). CBSG has helped in tion to the process) and because an ternational and legal limits. First, a
developing GRB processes in two enormous amount of information is country always has the option of
ways. First, it facilitates workshops available on the biology and assisted declining to provide samples to any
in biologically rich regions through- reproduction of the tiger, which GRB program. Second, biomaterials
out the world whose participants pri- would allow a GRB to be effective. should ideally be donated to GRB
oritize those species deserving conser- This exercise has been useful be- programs, thereby separating the re-
vation attention and then recommend cause it has allowed biologists to source from commercial interests.
detailed strategies to ensure their re- identify and address the many com- There is reluctance to commercialize
covery (Ellis and Seal 1995, Westley plexities that are inherent to devel- genetic materials, the fear being that
and Vredenburg 1997). Thus, CBSG oping and implementing a practical adding a price to a sperm sample or
helps to objectively identify species repository for any given species. a vial of DNA will provoke nefarious
that could benefit from a host of con- The action plan is a written docu- trade in endangered species prod-
servation approaches, including reposi- ment containing explicit information ucts. Third, some proportion of ev-
tories of cryopreserved biomaterials. (Figure 4) that justifies the bank on ery collection should be placed in a
CBSGworkshop participants have rec- the basis of both in situ and ex situ central GRB within the region in
ommended GRBs for conservation conservation. It also provides rel- which it is collected, and it should be
of the cheetah and lion in Namibia evant information on species biology managed by an appropriate species
and the giant panda in China. (life history and natural reproduction), specialist group or management com-
Second, CBSG has provoked in- on animal numbers in the wild and in mittee. Fourth, ownership of germ
ternational awareness and debate captivity, and on the accessibility of plasm and embryos should remain
about the usefulness of organized these animals for donating to the GRB with the owner of the donor animal
biological repositories as part of con- (there is no point to developing a re- (i.e., the nation, institution, or indi-
servation planning and action pository if managers are reluctant to vidual), unless transferred to a spe-
(Bartels and Wildt 1994, Wildt and allow sampling of biomaterials). cies coordinator or a management

694 BioScience Vol. 47 No. 10

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committee (the preferred options). studies: Technology can be used with vive cryopreservation, with normal
Decisions about apportionment of some reliability in these species to follicle growth and ovulation occur-
offspring resulting from the use of positively effect management of small ring after transplantation, often to a
these biomaterials should be made populations. One confounding fac- host whose immune responses are
by the owners of the donor and re- tor will continue to be species-spe- suppressed to keep her from reject-
cipient at the time when the sperm, cific differences that almost always ing the foreign ovary tissue. Oocytes
ova, or embryos are used. Finally, will require studies to understand released from such frozen-thawed
right and title to all other biomaterials the reproductive biology of both material are viable; live births have
(the tissues, blood products, DNA, males and females and how their resulted in mice and sheep after au-
and other bodily fluids or excretions) germ plasm and embryos respond to tologous transplants of ovarian grafts
should be assigned by the owner of cryopreservation (Wildt et al. 1992). stored at -196 ?C (Gosden et al.
the donor to a regional coordinator or Sperm and embryos that appear vi- 1994, Gunasena et al. 1997, Harp et
species specialist group that can ap- able after thawing but somehow later al. 1994). A second promising ap-
portion these materials to those spe- fail to result in offspring are another proach that may simplify applying
cialists who are best able to generate dilemma. Is the problem sublethal germ plasm cryopreservation to di-
the knowledge that will contribute cellular injury? Or is it, rather, fail- verse species is the ability to isolate
to conservation and protection. ure to create a suitable in utero envi- and cryopreserve embryonic and
ronment in the host female? spermatogonial stem cells (Avarbock
Cryoconservation: high Reproductive scientists have also et al. 1996, Campbell et al. 1996).
priorities for the future speculated about the potential of Recently, such techniques have per-
using a common species to enhance mitted cryopreserved rat testes cells
Wide-ranging dialogues, facilitated propagation of a rare species. The to continue spermatogenesis when
by organizations such as CBSG, best example is interspecies or inter- thawed and transplanted into im-
about the ramifications of GRBs and generic embryo transfer, in which muno-incompetent mice (Clouthier
how the process could proceed are a the embryos of an endangered spe- et al. 1996).
positive first step. For a wildlife GRB cies are gestated in the uterus of a The bottom line is that basic and
to be an effective conservation tool, different species. There have been a applied research in conservation bi-
there must be an organizational con- few isolated successes with this tech- ology must be strongly advocated at
figuration that involves all stake- nique. Offspring have been born from all levels, including through federal
holders, strong science, a written gaur (Bos gaurus) embryos that agencies such as the National Sci-
strategy, and global cooperation. were transferred to domestic cattle ence Foundation and the proposed
Specific, high-priority needs include: (Stover and Evans 1984); from bongo National Institute for the Environ-
(Tragelaphus euryceros, an African ment (NIE). If established, the NIE
* More knowledge and support. bovid) embryos transferred to eland would fund taxonomic and biogeo-
Mastery of the modern use of (Taurotragus oryx, another African graphic surveys, studies of the roots
cryopreserved sperm and embryos in bovid; Dresser et al. 1985); and from of extinction, and the upkeep of ex
cattle breeding was built on three zebra (Equus burchelli) and Prze- situ and in situ genetic resources,
decades of research involving hun- walski's horse (Equus przewalskii) including germ plasm repositories
dreds of animal scientists, thousands embryos transferred to domestic (Blockstein 1990, Hubbell 1993).
of experimental cattle, and millions mares (Summers et al. 1987). But the * Cooperation and training. A high
of dollars of federal, state, and in- lack of similar success stories for the priority for successful GRBs is the
dustrial funding. The burst of growth past ten years suggests that biologi- development of cooperative linkage
in strategies to combat human infer- cal compatibility between the tro- at the level of global, regional, na-
tility can also be traced to a biomedi- phoblast (the progenitor of the pla- tional, and local communities. GRBs
cal community that was both entre- centa) of the embryo and the uterine must contribute positively to the glo-
preneurial and responsive to a human endometrium will prevent interspe- bal conservation of a taxon. Estab-
health need. Hundreds of fertility cies embryo transfer from becoming lishing a tiger GRB for the captive
clinics emerged that generated mas- routine, at least using current tech- population in North America, for
sive amounts of new data; the in- nology. By contrast, intraspecies instance, does little to address the
evitable result has been that many embryo transfer does have potential, need to conserve the species in its
children are born from assisted re- so long as information is available range countries. Therefore, the tiger
production. Thus, for both cattle and about the time of ovulation and about GRB Action Plan is only one compo-
humans, the success of using cryo- ways to synchronize the donor and nent of a comprehensive conserva-
preserved germ plasm was predicated surrogate so that the uterus of the tion plan developed by all regions
on enormous financial support for recipient accepts the donor's em- that are interested in preserving the
basic and applied research. bryos. Basic research will be key to species. Western countries also have
Similar resources must be applied characterizing these mechanisms for most of the reproductive and bank-
to high-priority wildlife species. Sev- every species of high interest. ing specialists, whereas developing
eral conservation models already Promising new approaches for countries hold most of the world's
mentioned (e.g., Eld's deer and chee- assisted reproduction also need to be biological richness. Cooperative GRB
tahs) have proven the value of explored. For example, whole ova- programs provide an opportunity for
multidisciplinary and integrative rian sections have been found to sur- technology transfer that will enable

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developing countries to become self- gether voluntarily to conserve rare and cryopreservation. For wild popu-
sufficient in all available conserva- native plants and to conduct research lations, GRB activities could be co-
tion strategies, including genome and education (CPC 1991). The ordinated through IUCN-World
banking. Because GRBs depend on Center's national collection of nearly Conservation Union taxon specialist
cooperation of scientists from many 3.5 million seeds (of which one-third groups that have a mandate to de-
different disciplines (e.g., cryobiol- are cryopreserved) includes 494 taxa, velop species or taxon action plans
ogy, gamete biology, embryology, of which 216 are federally listed as for both wild and captive popula-
veterinary medicine, population bi- endangered or threatened. tions. Superimposing gene banking
ology, molecular genetics, captive This plant model could be useful on the process would be a natural
breeding, and field biology), train- in developing similar cooperative way to strengthen the chain linking
ing could span many of the life sci- arrangements among wildlife manag- science and conservation.
ences. The result would be conserva- ers and universities, commercial bull * Safety. Standards for safe and ef-
tion programs and repositories in (cattle) studs, or even human fertility fective monitoring, quality control,
the range countries of the species, clinics that routinely cryopreserve and long-term accessions support are
with trained specialists regulating biomaterials. Universities offer a par- essential. Protocols already in place
protection of, and access to, native ticularly rich source of ideas and tal- for securing agricultural germ plasm
resources. ents. Many university investigators and microorganisms will be useful
* Birthing GRBs. Quantitative mea- struggle to find money for their bio- prototypes. For example, the ATCC's
sures must be used to select species logical studies and are constantly ex situ management of microorgan-
for banking. The workshop processes looking for new funding sources. If isms is a remarkable model of safe
developed by CBSG assists in mak- genome resource banking can be storage and tracking on a huge scale
ing first-cut prioritizations of taxa made attractive to donors from the for many different organisms.
deserving attention (Ellis and Seal public, private, and corporate sec- Samples are stored in 57 liquid nitro-
1995). It then becomes the responsi- tors, then the academic community gen refrigerators with a capacity of
bility of those who manage indi- (the natural collectors of all kinds of more than two million vials each, in
vidual habitats or species (both in biomaterials) would be highly moti- 37 ultra-low temperature refrigera-
situ and ex situ) to determine if, and vated to become involved. CBSG has tors (that hold more than 150,000
when, genome banking would be a found worldwide interest among all vials at -70 ?C), or in four 4 ?C cold
useful adjunct to other conservation of these groups. Perhaps a first step rooms (900 square feet each), all of
initiatives. is a global electronic GRB network which are continuously monitored
Once the decision is made to imple- for coordinating interests and re- electronically for temperaturechanges.
ment a GRB, then the next challenge sources. A professional society con- GRB operating procedures must com-
becomes genome banking infrastruc- cerned with conserving living genetic ply with the highest quality control
ture. If resources were limitless, for- resources from wildlife, crops, and standards and have at least two stor-
mal regional GRB edifices-com- livestock could also be created. The age locations to minimize loss in case
plexes that house many curators benefits would go far beyond simply of catastrophe. Quarantine programs
caring for vast amounts of living exchanging technical information, as will be mandatory to avoid intro-
biomaterials from diverse biota- widely divergent stakeholders inter- ducing disease to wild or domestic
could be developed. But such an ap- ested in technology, agriculture, wild- stocks. More research will be needed
proach is naive in this era of con- life, animals, plants, and biopolitics on enhanced methods of pathogen
stricted budgets and organizational would be given the opportunity to detection and germ plasm treatment
downsizing. Moreover, a centralized better understand one another's to reduce the risk of disease transfer.
GRB approach has not worked par- needs, while identifying common * Databases. Any rare biomaterial
ticularly well for others, as those strategies to protect all valuable ge- from a living animal or plant is only
who struggle to financially maintain netic resources. as useful as the information avail-
centers that preserve orthodox seeds GRBs could also be developed able about that particular specimen-
from valuable food plants will tes- under the umbrella of the intensive that is, without high-quality data on
tify. We believe that the best strategy species management strategies that its type, quality, source, owner, and
for now is to exploit already avail- now prevail in zoos. There are more ancestry, the biomaterial can be
able infrastructure. Museums could than 80 species survival plans in worthless. The lives of zoo animals
add collections of frozen, living speci- North America, in which zoos work representing many wildlife species
mens, thereby adhering to (and, in- together to maintain maximum ge- are now monitored in relational da-
deed, ingeniously amplifying) their netic heterogeneity in a given species tabases (Ballou 1991, Ballou and
archival and conservation mission. (Hutchins and Wiese 1991). These Lacy 1995), and similar programs
Crop seed banks and botanical gar- efforts are occasionally linked to the are needed to track an animal's germ
dens could expand activities to in- range countries of species origin, with plasm, embryos, blood products, tis-
clude more plant diversity. One ex- support provided to local zoos or sue, and DNA. The International
cellent example is the Center for Plant field researchers. For example, the Species Information System (ISIS),
Conservation (CPC), which is head- North American Cheetah Survival an international nonprofit organiza-
quartered at the Missouri Botanical Plan has financially supported edu- tion based in Minneapolis, monitors
Garden. CPC is a consortium of 28 cational outreach and research in the origin, provenance, pedigree,
gardens and arboreta working to- Namibia, including sperm collection birth and death dates, sex, translo-

696 BioScience Vol. 47 No. 10

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All use subject to JSTOR Terms and Conditions
cation information, and biomedical storing biomaterials from high-pri- Valley (MN): IUCN-World Conservation
Union Species Survival Commission's Con-
data for more than 250,000 living ority taxa provides insurance and servation Breeding Specialist Group.
and 750,000 deceased animal speci- increases future opportunities. Who Blockstein D. 1990. Committee formed to
mens representing 6500 taxa at 495 knows the future value of these snap- create 'NIH for the environment.' Diver-
institutions in 54 countries (Flesness shots of biodiversity? What is cer- sity 6: 44.
et al. 1984).1 Because of its vast ex- tain is that failure to collect, to store, Campbell KHS, McWhir J, Ritchie WA,
Wilmut I. 1996. Sheep cloned by nuclear
perience with tracking whole ani- and to make this material accessible transfer from a cultured cell line. Nature
mals and their pedigrees (i.e., by will contribute to a growing loss in 380: 64-66.
maintaining records on dead speci- genetic diversity and fewer discre- Candy CJ, Wood MJ, Whittingham DG,
mens), ISIS is the logical choice to tionary options for the future. For Merriman JA, Choudhury N. 1994.
develop software that will monitor these reasons alone, it is worth de- Cryopreservation of immature mouse oo-
stored biomaterials and meaningful cytes. Human Reproduction 9: 1738-
veloping more grassroots programs 1742.
data that are related to their collec- in systematic sampling, storage, and [CBSG] Conservation Breeding Specialist
tion (e.g., the history and pedigree of use of germ plasm and biomaterials, Group. 1992. Guidelines for preparing a
the donor and the quantity and qual- especially for high-priority taxa. genome resource bank for wildlife conser-
vation. CBSG News 3: 29-31.
ity of the specimen). ISIS is currently [CPC] Center for Plant Conservation. 1991.
focusing on creating application soft- Acknowledgments Genetic sampling guidelines for conserva-
ware that allows relevant informa- tion collections of endangered plants.
tion on each biological specimen to The authors thank Jonathan Ballou, Pages 227-238 in Falk A, Holsinger KE,
be shared across continents, regions, Robert Lacy, Leslie A. Johnston, Ann eds. Genetics and conservation of rare
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mobot.org/CPC/welcome.html.
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Cunningham IS. 1994. National Academy of
ham, the Oklahoma City Zoo; Mitch Sciences releases long-awaited landmark
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