Biodiversity in China: Lost in the Masses?

Burton K. Lim is Assistant Curator of Mammalogy in the Department

of Natural History at the Royal Ontario Museum in Toronto,

Canada. His research interests focus on the biodiversity and

evolution of mammals with a particular emphasis on systematics

and biogeography of bats. He received a Ph.D. in the Ecology and

Evolutionary Biology program from the University of Toronto.

Judith Eger is Senior Curator of mammals in the Royal Ontario

Museum’s Department of Natural History. Her research interests

include systematics and biogeography of bats of Madagascar and

Asia. Her current research, focusing on tube-nosed bats of Southeast

Asia, has taken her on eight expeditions to Vietnam and China.

A. Townsend Peterson is University Distinguished Professor in the

Department of Ecology and Evolutionary Biology and the Biodiversity

Research Center at the University of Kansas in Lawrence, Kansas.

He specializes in the geography, ecology, and history of species’

distributions. He received his Ph.D. from the University of Chicago.

Dale H. Clayton is an evolutionary parasitologist interested in

coevolutionary interactions between birds and their ectoparasites.

He received his Ph.D. at the University of Chicago, followed by a

postdoc and five year lectureship at Oxford University in England. He

moved to the University of Utah in 1996, where he is now a Professor.

Sarah E. Bush is a Postdoctoral Researcher at the University of

Kansas, Museum of Natural History and Biodiversity Research

Center. She specializes in the evolutionary ecology of host-parasite

interactions. She received her Ph.D. from the University of Utah.

Rafe M. Brown is Assistant Professor in the Department of Ecology

and Evolution, University of Kansas, and Curator in Charge of the

Herpetology Division of the University of Kansas’ Natural History Museum

and Biodiversity Institute. He specializes in the study of processes of

evolutionary diversification in island archipelagoes with an emphasis on

systematic herpetology and biodiversity conservation in Southeast Asia.

BY BURTON K. LIM, JUDITH L. EGER , A. TOWNSEND PETERSON, MARK B. ROBBINS, DALE H. CLAYTON, SARAH E. BUSH, & RAFE M. BROWN

INTRODUCTION

History of Biotic Surveys in China

China’s biological diversity is immense,1 with two great biogeographic realms – tropical Indomalaya and temperate Palaearctic – that meet in the southern half of the country.2 The juxtaposition of these two realms brings together very different groups of organisms, as well as endemic forms unique to the area. Consequently, the assemblage of species in this zone is amazingly diverse.

Not counting the traditional knowledge of plants and animals used by people over the millennia, scientific classification and documentation of life forms in China did not begin seriously until the early nineteenth century, when natural historians collected specimens and sent them to museums in Europe for identification following the then-new standardized Linnaean binomial nomenclature system. For example, the giant panda (Ailuropoda melanoleuca) was originally described in 1869 by Père Armand David, a Jesuit missionary priest from France who deposited his collections in the Paris Museum. Western scientists dominated the study of Chinese biodiversity into the early twentieth century.3

As political circumstances changed, however, access to China by foreign scientists was quelled.4 It was not until the early 1950s, after the newly formed People’s Republic of China established the Chinese Academy of Sciences (also known as Academia Sinica), that Chinese biologists began to fill this scientific void. The Institute of Zoology was created within the Chinese Academy of Sciences and faunal surveys were initiated in several regions throughout the country.5 Even so, systematic studies in China were difficult because most taxonomic descriptions and distributional data were in foreign languages, and specimens necessary

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for comparisons were deposited in other countries. Efforts to develop a cadre of Chinese biologists knowledgeable in the sciences of their country were further hindered by the policies of Mao Zedong in the late 1950s that strove to conquer nature and to exploit land for human use.6 Some efforts were made toward foreign collaboration (e.g., with former Soviet bloc nations), but even these steps ended with the ill-fated Cultural Revolution (1966-1976) when social liberties, including scholarly activities, were curtailed severely.

Reforms began in the late 1970s, ushering in new policies of openness that produced international collaborations, such as the Wolong Panda Project involving the World Wildlife Fund and the Environment Protection Bureau of China. However, the struggle between preserving nature and developing the Chinese economy has constrained the extent of these efforts. With greater freedom of academic pursuits and a resurgence of scientific cooperation, newer areas of study (e.g., conservation biology, population ecology, molecular biology) have flourished, but at the expense of traditional biological research fields, including field inventories and systematic studies, which are needed for a better understanding of biodiversity as a sustainable natural resource.

The Importance of Biodiversity

The number of species of organisms presently described worldwide is slightly less than two million, but estimates of actual numbers of species range to an order of magnitude higher, from 5-30 million,7 indicating how little is known about the biological world. Within well-known and carefully-studied groups, such as mammals, knowledge of global species diversity has increased substantially (from 4629 to 5416 species, an increase of 17 percent) in the last decade.8 This increase indicates that much remains to be learned even about well-known groups.

The discovery of rubber, pharmaceuticals, and other key chemical compounds in plants highlights the industrial and medical benefits that detailed biodiversity studies can offer to humankind. Such knowledge should heighten awareness of the potential scientific discoveries being lost to species extinctions caused by habitat degradation and destruction. An excellent current example is the Three Gorges Dam on the Yangtze River, which pits the benefits of electricity and flood control against the plight of human displacement and loss of wildlife habitat. In 2007, the baiji, or Yangtze River dolphin (Lipotes vexillifer), was reported as

likely extinct after intensive surveys did not detect a single sighting during six weeks of visual and acoustic monitoring.9 The primary cause of its extinction clearly was unselective, large-scale fishing; however, even if a few individuals went undetected in the last surveys, their prospects of surviving in the changing and deteriorating ecosystem downstream of the dam are dim. Other threatened large animals endemic to the Yangtze River include the Chinese paddlefish (Psephurus gladius) and a subspecies of the finless porpoise (Neophocaena phocaenoides asiaeorientalis). Undoubtedly, many smaller and less notable species are equally affected by the altered environment in the water and the extensive flooding of more than one million km2 (360,000 mi2) of land.

Conservation efforts typically focus on large charismatic megafauna, while small organisms like insects and parasites that live on (or in) other organisms are largely ignored. Despite the fact that parasites represent as much as half of the world’s biodiversity,10 their status is not accurately reflected in conservation ranking systems. Only one species of parasitic louse is listed as threatened by the International Union for the Conservation of Nature, and no flea, mite, tick, acanthocephalan, cestode, or parasitic nematode species is listed.11 Despite the lack of official acknowledgement, parasites have suffered and continue to suffer co-extinction with their hosts.12 Besides simply conserving parasites because they are part of global biodiversity, parasites should be conserved for other reasons. Impacts of parasites on host populations are complex and are only beginning to be understood. Although parasites often negatively impact host populations, they may play important roles in the evolution and maintenance of host diversity.13, 14, 15

Thus, extinction of parasites in an ecosystem may be detrimental to host populations in unpredictable ways. Parasite communities can also provide valuable information about how hosts interact with each other and how they use the environment over spatial and temporal scales.11 Parasites even play a beneficial role in human medicine—for example, leeches are used to thin blood near reattached fingers and relieve veins congested due to plastic surgery. The anticoagulant agents from these and other hematophagous parasites are being synthesized for future management of thromboembolic diseases.16

The earlier naturalists seem to have been on the right track over two centuries ago by focusing energy on documenting and studying biodiversity. Today, however,

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many scientists have detoured, with other research areas taking precedence in spite of the central importance of basic biodiversity documentation. Particular urgency includes the study of biodiversity in southern China, as this region has the highest species richness in the country; however, southern China has seen the least biological exploration due to its relative remoteness. Furthermore, this region is experiencing increasing population pressure, land use conversion of natural habitats to agriculture and urban expansion, and broad-scale industrial contamination. Here, we describe a multidisciplinary, collaborative research project focused on Chinese biodiversity, and discuss its relevance to people and the environment as a natural resource.

THE STUDY

Multinational Collaboration

Even with more than 100 combined years of field experience among the coauthors of this paper, logistics still constitute one of the most difficult parts of biotic survey expeditions, particularly when it involves scientists from North America working in a country where Chinese is the primary language of discourse. The assistance of a Chinese doctoral student and collaborating institutions in China was instrumental to the success of this project.

Initial points of collaboration were established in 2000, with the Northeast Forestry University in Harbin, Heilongjiang Province. Two preliminary field-trips, which focused on birds and mammals, were funded by the University of Kansas and the Royal Ontario Museum. These early trips allowed us to assess the feasibility of a larger-scale and longer-term project: the first trip in 2001 covered three sites in Heilongjiang Province in the far northeast, followed in 2002 with a trip to two sites in Hunan Province insouth-central China17 (Figure 1). Next, we travelled to Yunnan Province in the south to discuss and eventually sign a collaborative agreement with the Kunming Branch of the China CITES (Convention on International Trade in Endangered Species) Administrative Office, the authority responsible for managing importation and exportation of wild fauna and flora.

The success of the initial “proof of concept” trips and the contacts established with Chinese institutions and officials prompted us to submit a proposal to the Biotic Surveys and Inventories Program of the U.S. National Science Foundation to study the terrestrial vertebrates and

associated parasites in southern China. The University of Kansas was the lead institution, with the collaboration of the Royal Ontario Museum and the University of Utah. Researchers at an additional 14 institutions in the United States, Canada, and Russia have supported the project by assisting with identification and curation of several major parasite groups. The field teams have included eight graduate students from six countries, including the United States, China, Mexico, Ecuador, Indonesia, and Romania. Upon approval of funding, we embarked on a series of surveys across southeastern China, particularly Guangxi Zhuang Autonomous Region (2004–2005) and Guizhou Province (2006–2007; Figure 1).

Field Methodology

The field crews consisted of pairs of experts in parasitology and each of the three terrestrial vertebrate groups (birds, mammals, and reptiles and amphibians). For poorly known regions, the most scientifically sound method for documenting biodiversity is capture and removal of series of individuals of each species as voucher specimens for study, description, and deposition in museum collections. This technique ensures scientific veracity, with the potential for confirmation of identifications and documentation of species present at a particular place in time using standardized methods, the first step in assessing and creating an inventory of biodiversity. This approach also enables future biodiversity studies, which would entail the same methodology repeated at regular time intervals to gauge if changes have occurred.

The specialists in each of the three vertebrate groups employ different sampling procedures. Birds are typically caught during the day with “mist nets,” which are made of fine nylon mesh. Bats are caught in mist nets at night, but are also caught using a device called a harp trap, which has fishing lines strung vertically between horizontal poles; the thin lines stop bats in flight harmlessly and cause them to fall into a confined holding bag. Other small mammals (i.e., rodents and shrews) are captured in box-like live traps. For amphibians and reptiles, buckets are placed in the ground, with plastic sheeting stretched between them to direct animals into the pitfalls, and herpetologists must also actively pursue and catch their study organisms by hand, often at night. As such, a vertebrate survey camp consists of many specialists all doing very different jobs, but working together towards the goal of documenting the biodiversity of the site under study.

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The parasitologists’ work begins once the vertebrate specimens reach the camp, where rudimentary laboratory facilities are established. The vertebrate hosts are first examined externally for ectoparasites, including lice, ticks, fleas, flies, and mites. Then each host is dissected to check internally for endoparasites, including acanthocephalans, trematodes, nematodes, and cestodes. Moreover, specialized samples are also taken to search for additional kinds of parasites: blood smears for malaria-like hematozoa, tissue samples for viruses, and feces for coccidia. Although these collection methods sample only a portion of the parasite species diversity at the site, they offer a first broad survey of the major parasite groups in the region.

Individuals kept as voucher specimens to represent the biodiversity at each study site are assigned preliminary identifications, but many problematic vertebrate taxa

require further study in the lab for verification of identifications. Parasites are sorted into major taxonomic groups in the field, but genuine identification takes place in the laboratory, under the eye of trained specialists. For all specimens, basic information is recorded carefully in field notebooks including collection site, habitat, body measurements, and reproductive condition of the vertebrates along with any associated parasites. Vertebrate specimens are typically prepared as traditional dried museum study skins, skeletons, or whole bodies fixed in formalin and preserved in ethanol, depending on the taxonomic group. These diverse preparations are intended to provide the widest range of research options, including examination of external characters, skeletal anatomy, and soft tissue structure. All specimens also have tissue samples frozen in liquid nitrogen for genetic study, which is one of the

Figure 1- Map of China with Guizhou Province (yellow), Guangxi Zhuang Autonomous Region (red), Hunan Province (green), and Heilongjiang Province (or-

ange). Study sites are (1) Diding Headwater Forest Nature Preserve, (2) Shiwandashan National Nature Reserve, (3a) Kuankuoshui Nature Reserve, (3b) Dashahe

Nature Reserve, and (4) Shuipu Village in the vicinity of Maolan National Nature Reserve.

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fastest growing areas of research in biology. Parasites are preserved in vials of ethanol, or formalin, fixed on slides, or frozen in the field. Back in the lab, most parasites go through a series of additional processes so that they can be properly identified, curated, and prepared for molecular studies in the future.

Study Areas

Each expedition lasted approximately one month, with actual field collecting lasting 19-26 days. The first two study areas were in Guangxi Zhuang Autonomous Region, in southern China along the Vietnam border (Figure 1).18 Diding Headwater Forest Nature Preserve (also known as Jin Xin County Provincial Nature Reserve) was surveyed from 18 September to 9 October 2004, and Shiwandashan National Nature Preserve was surveyed from 14 April to 8 May 2005. At both sites, the general habitat was subtropical moist broadleaf forest on low mountains.19 The last two study areas were in neighboring Guizhou Province.20 In 2006, we were at Kuankuoshui Nature Reserve (Figure 2) from 14-26 April, and Dashahe Nature Reserve from 29 April to 4 May. Both sites are in the northern part of the province, in subtropical moist broadleaf and mixed forest on moderately high karstic mountains. In 2007, we worked in the southern part of Guizhou, near the border with Guangxi, based near Maolan National Nature Reserve in subtropical moist broadleaf forest on low karstic mountains from 26 March to 16 April. All study areas were in secondary forest in relatively close proximity

to agricultural fields and human settlements.

Curation and Study of the Material

Although the expeditions are an intense month of field work, they are only the first step in the research process in the documentation of biodiversity in China. Protocols vary among the different groups of organisms, but the curation process, which starts in the field with specimen preparation and data collection, continues over years in museum and university laboratories. Each specimen type is subject to its own curation process: dried study skins are fumigated, skeletons are cleaned of flesh by dermestid beetles and the bones numbered and catalogued, and frozen tissue samples are arranged in boxes for easy retrieval from ultracold freezers. Only at this time can final identifications be made, although some groups (particularly parasites) can require years of study to arrive at a complete understanding of the specimens and their taxonomic relationships. Further study may involve detailed dissections to understand morphology, analysis of DNA nucleotide sequences, or geographic analyses of patterns of distribution.

SURVEY RESULTS

The biotic surveys developed in this project covered four regions of southern China, and involved about three person-years of field studies. The laboratory side of this research is ongoing, and in some cases will take years before identifications and descriptions of the material collected are finalized. However, an initial summary is possible.

Among mammals, our surveys have documented 63 small mammal species, including 42 species of bats (Figure 3), nine species of rats and mice (Figure 4), two species of squirrels, and six species of insectivores (shrews and their close relatives). Diversity was distinct among the four survey areas; more than half of the species (52 percent) were documented at only a single site, and only one (Pearson’s horseshoe bat, Rhinolophus pearsonii) was recorded at all four sites. The two areas that were most similar in terms of mammal fauna (Diding and Shiwandashan) were roughly 200 km apart, but shared only about a third (31 percent) of their mammal species. Possible explanations for this heterogeneity could include differences in methodology, although the same twomammalogists worked all four of the southern expeditions using standardized techniques; seasonal variation

Figure 2- Kuankuoshui Nature Reserve in northern Guizhou Province was

surveyed in April 2006. The general habitat is mixed forest on karst moun-

tains beginning at an elevation of 1,500 meters. In the valley from left to

right are the Park headquarters and village, planted stands of coniferous

trees, man-made lake, and tea plantations, photo by Matthew C. Brandley.

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[although the two areas surveyed in Spring, Shiwandashan and northern Guizhou, had the lowest similarity (12 percent)]; or actual differences in mammal faunas between areas caused by ecological or biogeographic factors.

Among birds (Figures 5 and 6), we documented 145 species at the two sites in Guangxi and 153 species at the three sites in Guizhou, including a number of species that are nationally or globally threatened. 58 species were shared between the two Guangxi sites, whereas only 35 species were shared among the three Guizhou sites. Differences in species totals and relative abundance among sites can be explained by elevation, vegetation, season, effort, and the size of each reserve.

Among amphibians, we documented the occurrence of 36 species, including 16 frogs of the family Ranidae (true frogs), eight species of the family Rhacophoridae (old world tree frogs; Figure 7), six Megophryidae (leaf-mimic litter frogs), three Microhylidae (chorus frogs), three Bufonidae (toads), and a single species of Hylidae (New World tree frogs). Among reptiles, we recorded 32 species, including 11 nonvenomous species of snakes of the family Colubridae, four venomous snake species of Viperidae (pit vipers: Figure

8), three venomous Elapidae (cobras and coral snakes), a single species of Homolopsinae (estuarine mud snakes), and a single blind snake of the family Typholpidae. We also recorded two species of turtle, nine lizards of the family Scincidae (skinks), four Agamidae (angle-head lizards; Figure 9), and a single grass lizard (Lacertidae). More than 60 percent of the amphibian and reptile fauna was recorded at only a single site; only a few species of common frogs were recorded at all four sites—and most of these represent complexes of cryptic species that will soon be recognized as distinct species.

Parasitologists on these biotic surveys have examined over 2100 individual vertebrates, representing more than 350 species of birds, mammals, reptiles, and amphibians. Birds represent the greatest proportion of vertebrates examined with just over 1300 individuals from 200 species. The parasites from the vertebrate hosts are even more diverse than the hosts themselves. Represented parasites include parasitic fleas, flies, lice, ticks, mites (Figure 10), pseudoscorpions, leeches, acanthocephalans, nematodes, cestodes, trematodes, coccidia and hematozoans (Figure 11), as well as avian influenza viruses. All parasites were stabilized

Figures 3, 4, 5 & 6 (clockwise from top left)- One of nine species of tube-nosed bats (Murina aurata) documented during our biotic survey of south-

ern China, photo by Burton K. Lim © Royal Ontario Museum; Chestnut white-bellied rat (Niviventer fulvescens) from Kuankuoshui Nature Re-

serve, photo by Judith L. Eger © Royal Ontario Museum; Chestnut-winged Cuckoo (Clamator coromandus); Paradise-Flycatcher (Terpsiphone paradise).

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in the field and will undergo, or have already undergone, additional laboratory procedures to preserve them as archival-quality specimens. These parasites have been distributed to a network of parasitologists that specialize on each of the different parasite groups. Over time, these parasites will be identified and many new species and several new genera will be described. Already, a new genus of fly has been described (see below) and descriptions of a new genus of mite and a new genus of nematode are underway (H. Proctor pers. comm., V. Tkach pers. comm.).

INCREASING BIODIVERSITY

Noteworthy highlights of our biotic surveys include the discovery of species new to science. Some of these previously unknown species have avoided detection because of relative rarity, such as a horseshoe bat that we recently described in collaboration with Chinese and Mexican colleagues (Figure 12).21 Others are difficult to identify with traditional morphological techniques, but prove quite distinct when studied in terms of molecular genetics. DNA barcoding (www.barcodinglife.org), based on the use of short, standardized molecular gene segments to identify species, confirmed the diversity of known mammal species initially reported in our surveys, and also aided in discovery of four new species among the tube-nosed bats (Figure 13). This example of cryptic species indicates an underestimation of biodiversity in some widely distributed taxa.

Similarly, among the new species of amphibians and reptiles collected, perhaps the most striking of discoveries are large numbers of morphologically indistinguishable sympatric cryptic new species of stream frogs. DNA sequence data, together with a comprehensive survey of

morphology, indicate that these and many other Chinese and Indochinese populations represent an enormous complex of often-sympatric cryptic species that have escaped the attention of herpetologists since the first species in this group were described more than 100 year ago.22 We have found similar patterns in most species of common tree frogs and paddy frogs, suggesting that southern China and northern Indochina may actually have few “widespread” frog species, but rather huge complexes of closely related species. This biotic survey has, conservatively, documented over 500 associations between host and parasite species. Most of these are new host records and many will also represent new parasite species and genera. One exciting example is a new genus and species of parasitic batfly, Maabella stomalata (Figure 14), from a subfamily of flies with fewerthan 20 known species.23 The females of this unusual fly are obligate parasites of horseshoe bats (Rhinolophus spp.) After attaching on the wing of the bat, the parasite is enveloped by the skinand tissue of the host, and then loses its wings and legs before reproducing.

We also documented numerous distributional range extensions, including the first occurrences of several vertebrate species in China. Among mammals, eight of the 63 species encountered were new country records, and 12 more were new provincial records. About 116 species of small mammals (bats, rats, and shrews only) are expected for Guangxi and Guizhou provinces, based on the best available summaries.5, 24, 25 As such, our small mammal surveys documented 54 percent of the expected species of small mammals, and added another 17 percent to the list. Our surveys did not encounter a larger proportion of the species likely present because we only worked at four primary sites in the region, and potentially also owing to extensive land-use transformation over recent years that may have affected the native species diversity. For birds, 17 of the species recorded at the Guizhou sites were new for the province. Four frog species and two snake species were new records for China. There were eight frogs, three snakes, and two lizards that were new provincial records.

DISSEMINATION OF INFORMATION

One basic tenet of this project is that all biodiversity information will be promptly and openly available to scientists around the world. As such, we have made every reasonable effort to curate and cataloge specimen material, and to organize the associated data in standard formats

Figure 7- Tree frog (Philautus odontotarsus). Photo by C.J. Hayden.

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that permit efficient access by other scientists. A continuously-updated summary of project survey results is posted at http://darwin.biology.utah.edu/china/Index.htm, including links to project personnel, preliminary results, publications, and photographs.

Data for vertebrate specimens are freely available and searchable online after cataloging and uploading to internet databases following the DiGIR (Distributed Generic Information Retrieval) protocol: birds (www.ornisnet.org), mammals (www.manisnet.org), and amphibians and reptiles (www.herpnet.org). Information on parasites can be requested from the parasitologists based at the University of Utah, and will eventually be posted online in DiGIR-enabled databases as with the vertebrate data.

Currently, nine scientific papers have been published or are accepted for publication as a result of this project, and at least 17 more are now submitted or in preparation, and numerous presentations have been made at conferences and symposia. Perhaps most importantly, specimens resulting from project efforts have been loaned to many researchers at other institutions for further study.

Capacity Building

Assistance and cooperation with Chinese institutions involved in biodiversity work has been initiated in a variety of ways. We have deposited reference collections representative of local faunas for teaching and research at the Beijing Institute of Zoology, Northeast Forestry University, Guangxi Provincial Nature Museum, and Maolan National

Nature Reserve. Presentations summarizing our work have been given to students and faculty at the Northeast Forestry University and Guizhou Normal University. A collaborative visit to Canada was organized in 2006 for six officials of the Guizhou Provincial Forestry Bureau to observe Canadian approaches to management of protected area systems, including meetings at the Royal Ontario Museum, Point Pelee National Park, Algonquin Provincial Park, and Parks Canada. Finally, we have established contacts with several Chinese researchers and institutions to study biodiversity and publish joint research papers.21

Implications of Biodiversity

Beyond expanding knowledge in the academic and scientific world, our biotic surveys have basic implications and importance for China in a number of different ways. From a human health perspective, emerging infectious diseases have a profound impact not only on medical issues but also on economic issues. For example, the rapid spread of Severe Acute Respiratory Syndrome (SARS) in 2003 infected thousands of people worldwide and caused hundreds of deaths, with substantial socioeconomic ramifications. Researchers speculated that transmission of the SARS Coronavirus (SARS-CoV) most likely began in the markets of southeastern China, where many live animals were kept in close confinement under dubious hygienic conditions.

The masked palm civet (Paguma larvata) was originally suspected as the reservoir host of the virus, but further study identified it as only an intermediary amplification host for transmission because of its presence in animal markets. A

Figures 8 & 9 (left to right)- Chinese habu (Protobothrops mucrosquamatus); Mountain horned dragon lizard (Acanthosaura lepidogaster). Photos by Juan Guayasamin.

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subsequent broader survey of mammal groups suggested instead that horseshoe bats (Rhinolophus spp.) were the natural reservoir of a SARS-like coronavirus (SL-CoV).26, 27

However, horseshoe bats are small insect-feeders and not the typical large fruit-eating bats that would be found in markets, so no easy mode of transmission to humans is apparent, which may explain why the virus had not “emerged” before. Furthermore, these coronaviruses are genetically similar (92 percent) to those causing SARS, but sufficiently different in an important receptor binding site, indicating that SL-CoV in bats did not cause the SARS epidemic in 2003 directly.26 Nonetheless, considerably study is still required because the etiology of the SARS-CoV remains poorly known, as does our understanding of its distribution and transmission. Likewise, Rhinolophus is one of the most speciose genera of mammals,8 but its species diversity, distribution, and evolutionary relationships are also poorly known21, 28 highlighting the fundamental importance of biotic surveys to understanding emerging infectious diseases.

The emergence of a particularly pathogenic strain (H5N1) of avian influenza in China in the late 1990s provides a further illustration of the importance of biodiversity surveys. Although this flu strain has already spread broadly across Eurasia and Africa,29 its host ecology remains poorly understood. Specifically, a current dogma in the influenza field is that aquatic birds represent the primary

reservoir of these viruses,30 but the evidence behind this assumption is not strong. In fact, one initial result of our work has been the documentation of influenza infections much more broadly than might be expected in landbirds. This work (presently under consideration for publication) will constitute—we believe—the first element in a transformation in understanding of influenza ecology.

Chytridiomycosis is an emerging infectious amphibian disease caused by the chytrid fungus (Batrachochytrium dendrobatidis). This fungus has been associated with amphibian population declines and extinctions in diverse habitats on several continents.31, 32, 33, 34, 35 Although large-scale chytrid-associated declines have not as yet been reported for China, we consider it inevitable that the fungus will reach the country, if it has not already. The potential negative societal impacts of this conservation threat are immense: frogs serve a critical role in ecosystem health, are basal members of many terrestrial food webs, are important food sources for humans in parts of China and are important indicators of environmental quality. The catastrophic loss of large portions of China’s amphibian biodiversity would be a disaster of global proportions and will likely become a reality if this conservation threat is left unchecked. Since the first step in finding a solution is diagnosing the problem, we urge rapid and comprehensive chytrid fungus surveys throughout China36, 37 to attempt to evaluate the severity

Figures 10, 11 (left, top to bottom) & 12 (right)-A spinturnicid mite (Ancystropus sp.) collected from a fruit bat (Rousettus leschenaulti), scanning electron micro-

graph by H. C. Proctor; Light micrograph of trypanosome (blood parasite) surrounded by blood cells, photo by C. T. Atkinson; New species of horseshoe bat

(Rhinolophus) reported from southern China, including Kuankuoshui Nature Reserve in Guizhou Province. Photo by Judith L. Eger © Royal Ontario Museum.

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of the potential problem and develop a national strategy for preserving China’s highly unique amphibian fauna. Our samples will contribute to a baseline survey for chytrid fungus in southern Asia, with results expected in late 2008.

Biodiversity studies also have implications for ecotourism and sustainable development of protected area systems. As individual prosperity increases with economic development,

Figure 13- Neighbor-joining tree clustering individuals of 61 spe-

cies based on molecular sequence divergence from a DNA barcod-

ing analysis of mammalian biodiversity in southern China. New

species have been identified and described in conjunction with mor-

phological analysis within horseshoe bats and tube-nosed bats.

greater numbers of domestic Chinese tourists will be visiting more remote parts of their vast country. Likewise, as the Chinese population shifts from a rural society to an urban society, ecotourism is bound to increase in popularity as an escape from the hustle and bustle of the city to the tranquility of the countryside. Provincial and national nature reserves are ideal destinations to accommodate and educate people on the environment. China has almost 2200 protected areas that account for roughly 15 percent of the total national land mass. However, critics have indicated that many of these “protected” areas are only paper parks on maps,38 and that they are focused in broad areas of little use for humans, such as deserts. Investment in infrastructure and programs such as interpretation centers is essential to inform visitors of the flora and fauna being preserved within the reserves. Bird-watching is a popular pastime throughout the world with great potential to generate revenues not only for parks, but also for the local tourism industry. Locally trained wardens and rangers knowledgeable of the plants and wildlife can encourage positive experiences for visitors and help them to develop a better appreciation of nature. Biodiversity surveys and ongoing monitoring programs can thus support the core objectives of the reserves to protect the ecosystem and inform the general public.

RECOMMENDATIONS AND SUMMARY

China needs to re-initiate comprehensive biotic surveys of provincial and national nature reserves that began in the 1950s but waned in subsequent years. Summaries of Chinese biodiversity have been developed39 and a Biodiversity Working Group has been established as part of the China Council for International Cooperation in Environment and Development.24 However, in addition to compilation of existing information and discussion of species diversity, new field studies are necessary to build upon and update historical data for accurate estimates of biological diversity and species’ distributions. The Kunming Institute of Zoology, a branch of the Chinese Academy of Sciences, has recently taken a lead role in initiating such studies in southern China.

The emphasis on high-technology realms of science, such as molecular biology, is a good investment for leading-edge areas of research, but it should not be at the expense of more basic scientific studies of biodiversity, particularly in light of the threats of habitat loss and species extinction caused by population pressures and development. Systematics and taxonomy may not be growing proportionally to other areas of scientific research, but a core group of universities

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and museums throughout the world remain dedicated to the principals of Linnaean classification and Darwinian evolution that form the foundation of comparative biology. China would benefit greatly from a parallel emphasis.

Although biodiversity research worldwide has never enjoyed the high profile and financial support as have other scientific endeavours, it forms the basis for many important studies related to health and environmental issues. In particular, loss of habitat and threat of species extinction continues today in China because of economic policies encouraging growth, as opposed to the ideological policies of a generation ago. It will certainly be a challenge to find an appropriate balance between preserving the environment and developing the economy of the country. Establishment of a firm scientific basis for the understanding of Chinese biodiversity as a natural resource is necessary for making informed decisions for sustainable management and legislation; otherwise, surely, many more species (including the giant panda) will follow the Yangtze river dolphin and be lost forever.

Endnotes

1 Mittermeier, R.A., P.R. Gil, and C.G. Mittermeier. 1997. Megadiversity: Earth’s Biologically Wealthiest Nations. Mexico City: CEMEX.2 Hoffman, R.S. 2001. “The Southern Boundary of the Palaearctic Realm in China and Adjacent Countries” Acta Zoologica Sinica, vol. 47, pp. 121-131.3 Allen, G.M. 1938. “The Mammals of China and Mongolia (Natural History of Central Asia)” in W. Granger, ed., Central Asiatic Expeditions of the American Museum of Natural History, New York, vol.

11, part 1, pp. 1-620.4 Wang, S. 2008. “History of Chinese Mammalogy” in A.T. Smith and Y. Xie, eds., A Guide to the Mammals of China. Princeton: Princeton University Press, pp. 4-9.5 Zhang, Y. 1997. Distribution of Mammalian Species in China. Beijing: China Forestry Publishing House.6 Shapiro, J. 2001. Mao’s War Against Nature: Politics and the Environment in Revolutionary China. Cambridge: Cambridge University Press.7 Wilson, E.O., ed. 1986. Biodiversity. Washington, DC: National Academy Press.8 Wilson, D.E. and D.M. Reeder. 2005. Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd ed. Baltimore: Johns Hopkins University Press.9 Turvey, S.T., R.L. Pitman, B.L. Taylor et al. 2007. “First human-caused extinction of a cetacean species?” Biology Letters, vol. 3, pp. 537-540.10 Price, P.W. 1980. Evolutionary Biology of Parasites. Princeton, NJ: Princeton University Press.11 Whiteman, N.K. and P.G. Parker. 2005. “Using Parasites to Infer Host Population History: a New Rationale for Parasite Conservation” Animal Conservation, vol. 8, pp. 175-181. 12 Koh, L.P., R.R. Dunn, N.S. Sodhi, R.K. Colwell, H.C. Proctor, and V.S. Smith. 2004. “Species Coextinctions and the Biodiversity Crisis” Science, vol. 305, pp. 1632-1634.13 McCallum, H. and A. Dobson. 1995. “Detecting Disease and Parasite Threats to Endangered Species and Ecosystems” Trends in Ecology and Evolution, vol. 10, pp. 190-194.14 de Castro, F. and B.M. Bolker. 2005. “Parasite Establishment and Host Extinction in Model Communities” Oikos, vol. 111, pp. 501-513.15 Thomas, F., M.B. Bonsall, and A.P. Dobson. 2005. “Parasitism, Biodiversity, and Conservation” In F. Thomas, F. Renaud and J.F. Guegan, eds., Parasitism and Ecosystems. Oxford: Oxford University Press.16 Markwardt, K. 2002. “Hirudin as Alternative Anticoagulant: A Historical Review” Seminars in Thrombosis and Hemostasis, vol. 28, pp. 405-414.17 Komar, O., B.W. Benz, and G. Chen. 2005. “Late Summer Ornithological Inventories of Mt. Shunhuang and Mt. Dawei in Hunan, China” Zoological Research, vol. 26, pp. 31-39.18 Robbins, M.B., A.T. Peterson, A. Nyari, G. Chen, and T.J. Davis. 2006. “Ornithological Surveys of Two Reserves in Guangxi Province, China, 2004-2005” Forktail, vol. 22, pp. 140-146.19 National Geographic. 2008. Atlas of China. Washington, DC: National Geographic.20 Boyd, R.L., Á.S. Nyári, B.W. Benz, and G. Chen. 2008. “Aves, Province of Guizhou, China” Check List, vol. 4, pp. 107-114,21 Zhou, Z.-M., A. Guillén-Servent, B.K. Lim, J.L. Eger , Y.-X. Wang, and X.-L. Jiang. Submitted. 2009. “A New Species from Southwestern China in the Afro-Palaearctic Lineage of the Horseshoe Bats (Rhinolophus)” Journal of Mammalogy, vol. 90, issue 1, in press.22 Stuart, B. L., H. K. Voris, and R. F. Inger. 2006. High levels of cryptic species diversity revealed by sympatic lineages of forest frogs. Biology Letters vol. 2, pp. 470–474.23 Hastriter, M.W. and S.E. Bush. 2006. “Maabella gen. nov. (Streblidae: Ascodipterinae) from Guangxi Province, China and Vietnam with Notes on Preservation of Ascodipterinae” Zootaxa, vol. 1176, pp. 27-

Figure 14- New genus and species (Maabella stomalata) of bat fly found

in southern China and northern Vietnam, photo by M. W. Hastriter.23

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40.24 Wang, Y.-X. 2003. A Complete Checklist of Mammal Species and Subspecies in China: A Taxonomic and Geographic Reference. Beijing: China Forestry Publishing House.25 Smith, A.T. and Y. Xie, eds. 2008. A Guide to the Mammals of China. Princeton: Princeton University Press.26 Li, W, A. Shi, M. Yu, et. al. 2005. “Bats are Natural Reservoirs of SARS-like Coronaviruses” Science, vol. 310, pp. 676–679.27 Lau, S.K.P., P.C.Y. Woo, K.S.M. Li, et al. 2005. “Severe Acute Respiratory Syndrome Coronavirus-like Virus in Chinese Horseshoe Bats” Proceedings of the National Academy of Sciences, vol. 102, pp. 14040–14045.28 Csorba, G., P. Ujhelyi, and N. Thomas. 2003. Horseshoe Bats of the World (Chiroptera: Rhinolophidae). Shropshire, UK: Alana Books.29 Webster, R.G., W.J. Bean, O.T. Gorman, T.M. Chambers, and Y. Kawaoka. 1992. “Evolution and Ecology of Influenza A Viruses” Microbiology Review, vol. 56, pp. 152-179.30 Kilpatrick, A.M., A.A. Chmura, D.W. Gibbons, R.C. Fleischer, P.P. Marra, and P. Daszak. 2006. “Predicting the Global Spread of H5N1 Avian Influenza” Proceedings of the National Academy of Sciences USA, vol. 103, pp. 19368-19373.31 Alford, R.A., and S.J. Richards. 1999. “Global Amphibian Declines: a Problem in Applied Ecology” Annual Review of Systematics and Ecology, vol. 30, pp. 133-165.32 Houlahan, J.E., C.S. Findlay, B.R. Schmidt, A.H. Meyer, and S.L. Kuzmin. 2000. “Quantitative Evidence for Global Amphibian Population Declines” Nature, vol. 404, pp. 752-755.33 Lips, K.R., J.R. Mendelson III, A. Munoz-Alonso, L. Canseco-Marquez, and D.G. Mulcahy. 2004. “Amphibian Population Declines in Montane Southern Mexico: Resurveys of Historical Localities” Biological Conservation, vol. 119, pp. 555-564.34 Lips, K.R., J. Diffendorfer, J.R. Mendelson III, and M.W. Sears. 2008. “Riding the Wave: Reconciling the Roles of Disease and Climate Change in Amphibian Declines” Plos Biology, vol. 6, pp. 441-454.35 Pounds, J.A., M.R. Bustamante, L.A. Coloma, J.A. Consuegra, M.P.L. Fogden, P.N. Foster, E. La Marca, K.L. Masters, A. Merino-Viteri, R. Puschendorf, S.R. Ron, G.A. Sanchez-Azofeifa, C.J. Still, and B.E. Young. 2006. “Widespread Amphibian Extinctions from Epidemic Disease Driven by Global Warming” Nature, vol. 439, pp. 161-167.36 Boyle, D.G., D.B. Boyle, V. Olsen, J.A.T. Morgan, and A.D. Hyatt. 2004. “Rapid Quantitative Detection of Chytridiomycosis (Batrachochytrium dendrobatidis) in Amphibian Samples Using Real-time Taqman PCR Assay” Diseases of Aquatic Organisms, vol. 60, pp. 141-148.37 Hyatt, A.D., D.G. Boyle, V. Olsen, D.B. Boyle, L. Berger, D. Obendorf, A. Dalton, K. Kriger, M. Hero, H. Hines, R. Phillott, R. Campbell, G. Marantelli, F. Gleason, and A. Colling. 2007. “Diagnostic Assays and Sampling Protocols for the Detection of Batrachochytrium dendrobatidis” Diseases of Aquatic Organisms, vol. 73, pp. 175-192.38 Xu, J. and D.R. Melick. 2007. “Rethinking the Effectiveness of Public Protected Areas in Southwestern China” Conservation Biology, vol. 21, pp. 318-328. State Environmental Protection Administration. 1998. China’s Biodiversity: A Country Study. Beijing: China Environment Science Press.

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CONTENTSEditorial Staff

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Area Editors

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Justin Liang, Japan Kennedy School of Government

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4 Beyond the Social Contract: Science, Knowledge and the Democratic Imagination in India

BY SHIV VISVANATHAN

The debate between knowledge and democracy in India can be divided into four phases. First is the colonial period where India conducted a civilizational debate about the possibilities of science. The second is the era of the nation state where science was seen as the dominant form of knowledge. The contract between science and state virtually determined India’s sense of identity as a modern state. Our science policy was as important as our flag. The imposition of emergency, a period of dictatorship between 1975-77, opened a debate between state and scientific knowledge on one side and civil society and alternative systems of knowledge and technology on the other. Knowledge became a site for the new definitions of democracy in this third phase. Knowledge was no longer seen as abstract, but as a grounded system tied to life, livelihood and life chances. The fourth period was the era of liberalization and globalization where science recovered its legitimacy in a more privatized form around IT and biotechnology. Questions of choice, alternative and risk opened up new debates on knowledge. This paper traverses these four phases of the knowledge debate to argue that the debates on knowledge have been central to democratic imagination in India.

BY BURTON K. LIM, JUDITH L. EGER , A. TOWNSEND PETERSON, MARK B. ROBBINS, DALE H. CLAYTON, SARAH E. BUSH, & RAFE M. BROWN

For the general public, the state of biology and conservation in China is inextricably linked to giant pandas. “Flagship” species are excellent vehicles by which to establish innovative conservation programs and mobilize environmental initiatives. However, in China, as in many other countries, the broader diversity of organisms that make-up the totality of biodiversity has taken a backseat to a focus on larger, charismatic animals. The diversity of more enigmatic groups, such as small vertebrates, invertebrates, and parasites is poorly known, but important for establishing environmental and sustainable management policies to ensure proper functioning of ecosystems and preservation of natural resources for future generations. China is one of the most biodiversity-rich countries in the world, but also has the world’s largest human population and one of the fastest-growing economies. If Chinese flora and fauna are to have a chance of surviving human encroachment and development, a firm knowledge and understanding of this biological richness is necessary as a foundation for sound legislation and management. Our 4-year field program represents one of few modern, broad biotic surveys and inventories of the terrestrial vertebrates and their associated parasites in the country. We summarize the principal components of the project and notable findings, including discovery of species new to science and many first records for known species in the country. Biotic survey and inventory projects such as this one set the stage for value-added research and benefits relevant to the local, regional, and international communities.

12 Biodiversity in China: Lost in the Masses?

2

Volume XI, No. 4Fall 2008

BY RAVIPRASAD NARAYANA

This paper addresses the environmental and economic values of Japan’s 14 World Heritage sites. The World Heritage sites have outstanding universal value, which can be classified into two types: use value and non-use value. While tourism is one example of the use value of the sites, examples of non-use value include wildlife habitat, ecosystem and biological diversity. Because there is no market mechanism for pricing non-use value, the non-use value of the World Heritage sites is often slighted. Therefore, it is important for the policy managers of such sites to evaluate a total value, which includes both the use value and non-use value. In the literature of environmental economics, some valuation methods have been developed including replacement cost, hedonic pricing, travel cost and contingent valuation. The contingent valuation, a survey-based method, which is calculated based on how willing people are to pay for environmental resources, can provide a proper estimate of the total value. Empirical results of the contingent valuation study on the Yakushima World Heritage Site show that the use value of tourism is only 61percent of the total value, therefore non-use values such as biodiversity should not be ignored.

Sino-Indian relations have shown significant improvement in the last decade despite the existence of obstacles in the form of an unresolved boundary and the issue of Tibet. The improvement in bilateral relations has come about due to the emergence of a political connective, economic incentive and a strategic imperative best revealed during the tenure of the current United Progressive Alliance (UPA) coalition government in New Delhi. This article analyzes the main themes, issues and aspects of contention dominating Sino-Indian relations.

Based on first hand experiences, the author provides an incisive and in-depth perspective on the Democratic Republic of Korea’ s intractable food insecurity, which has gone on for more than a decade. The problem of famine and food shortage is examined against the backdrop of economic disarray, degradation of natural resources and unsustainable agricultural policies.

32 Environmental and Economic Values of World Heritage Sites in Japan

BY KOICHI KURIYAMA

24 India-China Relations: The United Progressive Alliance (UPA) Phase

41 A Decade of Food Insecurity in North Korea (DPRK)

BY AJMAL M. QURESHI

3

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