Biodiversity v2 Screen

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Biodiversity:Its Importance toHuman Health

A Project

of the Centerfor Healthand the GlobalEnvironment

Harvard Medical Schoolunder the auspices of the World Health Organization,the United Nations Development Programme, and the United Nations

Environment Programme

EditorEric Chivian M.D.

Interim Executive Summary


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The project Biodiversity: Its Importance to Human Healthhas been made possible through the generous supportof several individuals and the following foundations:

Bristol-Myers Squibb CompanyNathan Cummings FoundationRichard & Rhoda Goldman FundClarence E. Heller Charitable FoundationJohnson & JohnsonJohn D. and Catherine T. MacArthur FoundationThe New York Community TrustThe Josephine Bay Paul and C. Michael Paul Foundation, Inc.The Pocantico Conference Center of the Rockefeller Brothers FundV. Kann Rasmussen FoundationWallace Genetic FoundationWallace Global FundThe Winslow Foundation

Johnson & Johnson generously provided the fundingfor this second printing.


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Working Group 1: BiodiversityChairs Stuart PimmMaria Alice dos Santos AlvesMembers Christer NilssonCallum Roberts

Terry RootStephen SchneiderMelanie Stiassny

Working Group 2: Ecosystem ServicesChairs Jerry MelilloOsvaldo SalaMembers Amy AustinDonald Boesch

Scott CollinsNorma FowlerLinda JoyceWilliam LauenrothRoger PielkeJose SarrukhanMary ScholesPier VallingaBrian WalkerRusong Wang

Working Group 3: Medicines from

Natural SourcesChairs David NewmanJohn KilamaMembers Gordon CraggGabriela Coelho de SouzaElaine ElisabetskyWilliam FenicalAna Paula Schulte HaasCharles Wambebe

Working Group 4: The Value of Plants, Animals,and Microbes to Medical ResearchChairs Eric ChivianJoshua RosenthalMembers Mark Cattet

John DalyAndrew HendrickxToshio NarahasiRalph NelsonBaldomero OliveraKen PaigenGary Ruvkun

Working Group 5: Ecosystem Disturbance,Biodiversity, and Human Infectious DiseasesChairs David MolyneuxRichard OstfeldMembers Felix AmerasingheRobert BosPeter DaszakPaul EpsteinThomas KristensenStephen MorseYasmin Rubio

Working Group 6: The Role of Biodiversity

in World Food ProductionChairs Daniel HillelCynthia RosenzweigMembers Francisco Garcia-OlmedoAndrew PierceDavid ShermanZhao ShidongAmos TandlerDiana Wall

Working Group 7: Policy OptionsChairs Jeffrey McNeelyMadhav GadgilMembers Martha Chouchena-RojasVernon HeywoodWalter ReidSetijati Sastrapradja


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1 Biodiversity

Biodiversity:Its Importance toHuman Health

EditorEric Chivian M.D.

Associate EditorsMaria Alice dos Santos Alves Ph.D. (Brazil)Aaron S. Bernstein (USA)Robert Bos M.Sc. (WHO)Paul Epstein M.D., MPH (USA)Madhav Gadgil Ph.D. (India)Hiremagular Gopalan Ph.D. (UNEP)Daniel Hillel Ph.D. (Israel)John Kilama Ph.D. (USA/Uganda)Jeffrey McNeely Ph.D. (IUCN)Jerry Melillo Ph.D. (USA)

David Molyneux Ph.D., Dsc (UK)Jo Mulongoy Ph.D. (CBD)David Newman Ph.D. (USA)Richard Ostfeld Ph.D. (USA)Stuart Pimm Ph.D. (USA)Joshua Rosenthal Ph.D. (USA)Cynthia Rosenzweig Ph.D. (USA)Osvaldo Sala Ph.D. (Argentina)

Interim Executive Summary

A Project of the Center for Health and the Global EnvironmentHarvard Medical School

under the auspices of the World Health Organization,the United Nations Development Programme,and the United Nations Environment Programme


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2002 Center for Health and the Global EnvironmentHarvard Medical School

2003 2nd printing (with revisions)

The views expressed in this report are those ofthe authors and do not necessarily reect those of

the World Health Organization, the United NationsDevelopment Programme, the United NationsEnvironment Programme, or other cooperatinginstitutions or agencies. The mention of acommercial company or product does not implyendorsement by any of the institutions or agenciesinvolved in this report.

Design by WGBH Design

Cover Photo: Blue Poison Arr ow Frog (Dendrobates azureus) Art Wolfe 1991

0410093


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Contents Chapter 1:Biodiversity 6Chapter 2:Ecosystem Services 13

Chapter 3:Medicines from Natural Sources 19

Chapter 4:The Value of Plants, Animals,and Microbes to Medical Research 26

Chapter 5:Ecosystem Disturbance, Biodiversity,and Human Infectious Diseases 34

Chapter 6:The Role of Biodiversityin World Food Production 41

Chapter 7:Policy Options 49


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4 Biodiversity: Its Importance to Human Health

Introduction

E.O. Wilson once said about ants we need themto survive, but they dont need us at all. The same, in fact, could be said about countless other insects, bacteria, fungi, plankton, plants, and other organisms. This central truth, however, is largely lost to most of us. Rather, we act as if we were totally independent of Nature, as if it were an innite source of products and services for our use alone, and an innite sink for our wastes.

During the past 50 years, for example, we have squandered one fourth of the worlds topsoil,one fth of its agricultural land, and one third of its forests, while at the same time needing these resources more than ever, having increased our population from 2.5 billion to over 6.1 billion.We have dumped many millions of tons of toxic chemicals onto soils and into fresh water, the oceans, and the air, while knowing very little about the effects these chemicals have on other species, or, in fact, on ourselves. We have changed the composition of the atmosphere, thinning the ozone layer that lters out harmful ultraviolet radiation, toxic to all living things on land and insurface waters, and increasing the concentrationof atmospheric carbon dioxide to levels not present on Earth for more than 420,000 years. Thesecarbon dioxide emissions, caused mainly by our burning fossil fuels, are unleashing a warming of the Earths surface and a change in the climate that will increasingly threaten our health, and the survival of other species worldwide. And we are now consuming or wasting almost half of all the planets net photosynthetic production on land and more than half of its available freshwater.Most disturbing of all, we are so damaging the habitats in which other species live that we are driving them to extinction, the only trulyirreversible consequence of our environmental assaults, at a rate that is hundreds or perhaps even thousands of times greater than natural background rates. As a result, some biologists are

calculating, on the basis of habitat destructionalone, that as many as two thirds of all species onEarth could be lost by the end of this century, a proportion of lost species that matches the great extinction event, 65 million years ago, that wiped out the dinosaurs. That event was most likely the

result of a giant asteroid striking the Earth;this one we alone are causing.We have done all these things, our species,

Homo sapiens sapiens, one species out of perhaps ten million or more, and a very young species at that, having evolved only about 130,000years ago, behaving as if these alterations were happening someplace other than where we live, as if they had no effect on us whatsoever.

This mindless degradation of the planet is

driven by many factors, not the least of which is our inability to take seriously the implications of our rapidly growing populations and of our unsustainable consumption, largely by people inindustrialized countries, of its resources.Ultimately, our behavior is the result of a fundamental failure to recognize that humanbeings are an inseparable part of Nature and that we cannot damage it severely without severely damaging ourselves.

This report was rst conceived ten years agoat the Earth Summit in Rio de Janeiro when the great promise of that event and its ambitious goals for controlling global climate change and conserving the worlds biodiversity were rst elaborated.What was recognized then, and what is even more widely appreciated now, was that, in contrast tothe issue of climate change, there was inadequate attention being paid to the potential consequences for human health resulting from species loss and the disruption of ecosystems. This general neglect of the relationship between biodiversity and human health, it was believed, was a very serious problem. Not only were the full human dimen- sions of biodiversity loss failing to inform policy decisions, but the general public, lacking anunderstanding of the health risks involved, was


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Introduction 5

not grasping the magnitude of the biodiversitycrisis, and not developing a sense of urgency toaddress it. Unfortunately, aesthetic, ethical,religious, even economic, arguments had notbeen enough to convince them.

To address this need, the Center for Health

and the Global Environment at Harvard Medical School proposed that it coordinate an international scientic effort to compile what was knownabout how other species contribute to humanhealth, under the auspices of the World HealthOrganization (WHO), the United Nations Development Programme (UNDP), and the United Nations Environment Programme (UNEP), and to produce a report on the subject that would be the most comprehensive one

available. Happily, the WHO, UNDP, and UNEP agreed to this proposal.What follows is the Interim Executive

Summary for this report Biodiversity: Its Importance to Human Health. It is interimbecause the nal report, to be published by Oxford University Press as a book written for a general audience, and the nal Executive Summary for Policy-Makers based on that book, will not appear until late 2004. Upon completion, the report will be presented to the WHO, UNDP, UNEP,to the U.N. Convention on Biological Diversity,and to other agencies and policy-making bodies,including the U.S. Congress.

We have divided the project into sevenworking groups, each of which will produce achapter, led by two co-chairs and composed of experts from industrialized and developingcountries, and from a wide range of disciplines.

Chapter 1 looks at the status of global

biodiversity and examines the forces thatthreaten it.

Chapter 2 summarizes ecosystem services thatsupport all life, including human life, on this planet.

Chapter 3 covers medicines and natural pesticides that are derived from plants, animals,and microbes.

Chapter 4 traces the dependency of medicalresearch on other species.

Chapter 5 examines the complex relationshipsamong ecosystem disruption, biodiversity, andthe emergence and spread of human infectiousdiseases.

Chapter 6 discusses the role of biodiversity inworld food productionon land, in freshwater,and in the oceans.

Chapter 7 provides for the policy-maker a preliminary list of suggested options to considerin addressing all of the above issues.

More than 60 scientists from around the world,each bringing an enormous wealth of experience and expertise, have joined me in compiling the material for this report. I cannot thank themenough for their creativity and wisdom and just plain hard work. All of us believe this report canhelp the public understand that human beingsare an integral part of Nature, and that our health depends ultimately on the health of its

species and on the natural functioning of its ecosystems. All of us hope that our efforts will help guide policy-makers in developing innovative and equitable policies based on sound science that will effectively preserve biodiversity and promote human health for generations to come. And all of us share the conviction that once people recognize how much is at stake with their health and lives,and particularly with the health and lives of their children, they will do everything in their power to protect the global environment.

Eric Chivian M.D.Director Center for Health and the Global Environment Harvard Medical School


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chapter 1 Biodiversity

Figure 1 Cone snail species.

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Biodiversity 7

What Is Biodiversity?

Biodiversity is the variety of lifeits ecosystems,species, populations, and genes. Human actionstowards the land, freshwater, and oceans have alreadycaused biodiversity to decline. Even greater losseswill occur in the future if humanity continues its

present unsustainable use of natural resources. Indocumenting this decline, there has been a focus onspecies extinctions, the most obvious manifestationof biodiverity loss. In addition, there is the loss ofecosystems, populations, and genes. All these are theonly truly irreversible consequences of environmentalchange. When any of these is lost, it is gone forever.Species losses are also the aspect of biodiversity lossthat is most often considered, for example, by the U.N.Convention on Biological Diversity. This chapter, too,will focus on species extinctions. The subject is broaderand more complex than this, however. Even a species

that survives can lose much of its genetic diversity if local populations are lost from most of its originalrange. Furthermore, ecosystems may shrink in areadramatically and lose many of their functions, eventhough their constituent species manage to survive.The loss of ecosystems, species, populations, and genesall have implications for human health.

The Rates of Natural and PresentDay Species Extinction

Estimation of the absolute rates of speciesextinction: how many species are there?Any absoluteestimate of extinction rate, such as thenumber of extinctions per year, requires that we knowhow many species there are. We do not, and theproblems of estimating their numbers are formidable.Taxonomists have described, that is, given names to,slightly more than one and a half million species (seeTable 1). Only about 100,000 of theseterrestrial verte-brates, some owering plants, and invertebrates withpretty shells or wingsare popular enough for taxono-mists to know them well. Birds are exceptionally well-known, with roughly 10,000 species described, and onlyone or two new species named each year.

In some groups, we may have more names thanthe species they represent. Those who describe speciescannot always be certain that the specimen in hand hasnot been given a name by someone else in a differentcountry and (sometimes) in a different century. Themore serious error, however, is that in all potentiallyspecies-rich groups, the estimates of numbers of speciesfar exceed the number of named species. Moreover, tax-onomists have only sparsely sampled some potentially

rich communities, such as the deep oceans, thecanopies of rainforests, and the microscopic world.Table 1 also provides estimates of how many species arelikely to exist.

These estimates of species numbers excludemicrobes, for there is no universally accepted denitionof species for such organisms as bacteria and viruses.

The genetic diversity of microbes is substantial: a pinchof soil may contain thousands of different types, andrecent surveys of the human mouth have identiedhundreds of different bacteria. How widespread arethese typesfor example, do all soils have the same ordifferent varieties is still a matter to be resolved.

What has limited our appreciation of the diversityof microbes has been their small size, the fact that theyare often morphologically identical, and the fact thatmost microbes cannot be cultured. It was not untilmolecular sequencing (by looking at ribosomal RNA)that the size and complexity of the microbial world

began to be uncovered. Today, many biologists acceptthat the tree of life, rather than being dominated byanimal and plant kingdoms, is, instead, divided intothree domainsBacteria and Archaea (which lack anucleus), and Eucarya (which have a nucleus)allthree domains are composed almost entirely ofmicrobial organisms (Figure 2). For the purposes of thischapter, we shall concentrate on the macroscopicworld of plants, animals, and fungi, for that is what weknow best.

If we exclude most of the microbial world inestimates of the total number of species, then we come

up with a gure of between 7 and 15 millionsay 10million to the nearest factor of 10.

Group

ProtozoaAlgaePlantsFungi

AnimalsVertebratesNematodesMolluscsArthropods Total

CrustaceansArachnidsInsects

Other animalsTotal

Number OfNamed Species(in thousands)

4040

27070

4515

708554075

72095

1,500

Estimated TotalNumber of Species(in thousands)

100300320500

50500120

4650150500

4000250

6,800

Table 1 Number of Named Distinct Living Species andEstimated Total Number of Species.

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Relative rates of extinction: calculating background extinction ratesWhat is the background rate of extinction: that is, howfast did species disappear in the absence of humanimpacts? Various sources of information support thebenchmark of a species lifetime at a million years or so,and the consequent background rate of extinction at nomore than one species per million species per year.

Relative rates of extinction:Recent extinction ratesTo what extent has our species increased extinctionrates above background levels? If we are to use exam-ples of species extinctions from certain groups that are

well studied, it is necessary that they be representative.It is believed, with high statistical condence, that thosethat have been used are indeed highly representative,being diverse in their natural histories and evolutionaryorigins. Extrapolating from these examples, one arrivesat a current global rate of extinction that is at leastseveral hundred times background rates (see Table 2) .

Relative rates of extinction: predicting futurerates of extinction from species currentlythreatenedFor vertebrates, there are also world-wide surveys of thenumbers of threatened species. Threatened has a specicmeaning: it means that experts consider the species tohave a high probability of extinction within the next few

decades. For birds, 1,100 of the roughly 10,000 speciesknown are considered to be threatened. Suppose that all these threatened species were to become extinct in thenext 100 years (many would go sooner, of course). If so,then future rates of extinction for birds would be 1,100extinctions per million species per year, or more thanone thousand times background rates (Table 2).

There are many factors that can threaten speciessurvival that we cannot easily anticipate. For example,accidentally or deliberately introduced species may bethe cause of many species extinctions.

While predicting future extinctions from

introduced species or from other factors such as globalclimate change may not be possible, it may be possibleto predict the magnitude of extinctions from habitatdestruction, the factor usually cited as being themost important cause of extinctions (for birds, it isimplicated in ~75% of the 1,100 threatened species).Habitat destruction is continuing and, in some cases,accelerating, so that some now-common speciesmay lose their habitat within decades.

The loss of populations and genesWhile much of the concern over the loss of biodiversitycenters on the global loss of species, most of the benetsbiodiversity confers depend on localspecies populations.An obvious example is a forest that provides protectionto a citys watershed. While no species might becomeextinct globally if the forest were to be cut down, therewould be a loss of the ecosystem services the forestprovidede.g. in preventing soil erosion and lteringout pollutants in ground water. Simply, it is the local loss of diversity that is important in this case. Inaddition, populations also supply genetic diversity, sincedifferent populations across a species range will differto varying degrees in their genetic composition. Suchgenetic diversity has a value for agricultural crops, forexample, where plant breeders may rely on the diversityof genes in the wild relatives of those crops as a sourceof genes that confer resistance to disease. Thus, aspopulations are eliminated locally, genes may becomeextinct globally.

An average species consists of 220 populations,suggesting that there may be more than 2 billion popu-lations globally, of which, it is estimated, 160 millionpopulations (8%) are lost each decade. If present trends


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Figure 2 Three Domains of Living Organisms (The phylogenetic tree based on small-subunit ribosomal RNA sequences. N.B. theposition of the branches Coprinusfungi, Homoanimals,and Zeaplants).

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Animal GroupBirdsMammalsReptilesFrogs and toadsFresh water clams

continue, while many species may be saved in protectedareas (such as national parks and zoos), those specieswill be just remnants of their once geographicallyextensive and genetically diverse selves.

The loss of ecosystemsWhile conservation justiably prioritizes tropical moistforests because they are thought to hold such a largefraction of the worlds species, a comprehensive strategyshould also save distinctive ecosystems, not onlybecause of the services that they provide, but because of the characteristic species they contain. Tropical dryforests, tundra, temperate grasslands, lakes, polar seas,and mangroves are all examples. Importantly, thesebiological communities house distinctive ecological andevolutionary phenomena. Some of these major habitattypes, such as tropical dry forests and Mediterranean-climate shrublands are, on average, even morethreatened than are tropical moist forests and requireimmediate conservation action. The Everglades of Florida or Brazils Pantanal, for example, do not rank asplaces with a high concentration of species, but achieveprominence because ooded grasslands are globallyscarce and uniformly vulnerable. Other regions attainprominence because of the biological phenomena theyhouse, such as the Arctic tundra and its migratoryshorebirds, polar bears, and caribou.

The Factors Causing Extinction

Habitat loss: On landHabitat loss is widely believed to be the predominantcause of extinction. There are parts of the world, suchas Europe and eastern North America, however, wherehuman actions have extensively modied terrestrialhabitats, yet these areas are not extinction centers.Clearly, habitat destruction causes different numbersof extinctions in different places.

What are the features common to centers of human-caused extinctions? For one, each area holds ahigh proportion of species found nowhere else.

Scientists call such species endemics. Remote islandsare rich in endemics.Endemics constitute 90% of Hawaiian plants, 100% of Hawaiian land birds. Thereare continental areas that are rich in endemics, too.About 70% of the plants in the southern part of SouthAfrica, 74% of Australian mammals, over 90% of NorthAmerican sh and the great majority of that continents

freshwater molluscs are endemic to those regions. Incontrast, only ~1% of Britains birds and plants areendemics.

Past extinctions are so concentrated in small,endemic-rich areas that the analysis of global extinctionis effectively the study of extinctions in one or a fewextinction centers. Why should this be?

Consider some simple models of extinction. Thesimplest supposes only that some species groups aremore vulnerable than others. This model does a poorjob of predicting global patterns. First, the modelpredicts that the more species present, the more therewill be to lose. Yet the number of species an area housesis not a good predictor of the number of extinctions.Relative to continents, islands house few species yetsuffer many extinctions. Second, if island birds wereintrinsically vulnerable to extinction, then Hawaii andBritain with roughly the same number of breeding landbirds, and both with widespread habitat modication,would have suffered equally. Hawaii had more than100 extinctions, Britain only three.

All the Hawaiian species were restricted to theislands; none of the British species were. This suggestsanother model of extinction. Imagine a cookie-cuttermodel where some cause destroys (cuts out) arandomly selected area. Species also found elsewheresurvive, for they can re-colonize. Only some of theendemics go extinct, the proportion depending on theextent of the destruction (see below). In this model, thenumber of extinctions correlates weakly with the areastotal number of species, but strongly with the numberof its endemics. By chance alone, small endemic-richareas will contribute disproportionately to the totalnumber of extinctions.

Biodiversity 9

Numberof Species

96004300470040001082

Number ofPast Extinctions

756020

521

Time (years)200200200

25100

Past Number of ExtinctionsPer MillionSpecies Per Year

39702150

194

EstimatedNumber of FutureExtinctions

110065021089

120

Time (years)100100100100100

EstimatedFuture Number of ExtinctionsPer MillionSpecies Per Year

11461512447223

1109

Table 2 Past and Estimated Future Extinction Rates.


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This model is consistent with knownmechanisms of extinction. Habitat destruction cutsout areas as the model implies. (Introduced speciesand other factors may also destroy species regionally.)This entirely self-evident model emphasizes thelocalization of endemics as the key variable inunderstanding global patterns of recentand futureextinctions.

Species with small ranges are geographicallyconcentrated. Scientists call these areas centers of endemism. Most of these areas are where threatened and

recently extinct species are concentrated.Hotspots:they are the combination of centers of endemism and unusual levels of habitat destruction.Only about 12% of the original habitat of these areassurvives in the year 2000. Currently, hotspots make uponly 1.4% of the Earths total land surface, yet theycontain more than one third of all known mammals,birds, reptiles, and amphibians. Of the survivinghotspot habitat, only about 37% is protected in anyway. Sixteen of the 25 areas are forests and most of them are tropical forests. Even in the three that arerelatively undisturbedin the Amazon, the Congo, and

New Guineaonly about half the original tropical forestremains (see Figure 3) . As a consequence of these highlevels of habitat loss, these 25 hotspots are where themajority of threatened and recently extinct species areto be found.

Habitat loss: In the oceansThe seas cover more than two-thirds of the planetssurface, yet despite their extent, taxonomists havenamed only 250,000 to 300,000 marine species,compared to more than one million on land. Theircount of marine species may be even more of anunderestimate than it is for land, however, as the oceans

are still very poorly explored, particularly microbiallyand at great depth. As on land, the peak of marinebiodiversity lies in the tropics. Coral reefs account foralmost 100,000 of marine species, yet their combinedarea is just 0.2% of the ocean surface. There arebetween four to ve thousand species of sh on coralreefs, about 40% of the worlds known marine shes.

The global center of marine biodiversity lies inthe South-East Asian archipelago, encompassing thePhilippine and Indonesian islands. In the AtlanticOcean, the highest levels of biodiversity are in theCaribbean.

An estimated 26% of the planets reefs have beenseriously damaged or destroyed by a combination of human activitiescoastal development, over-shing,land and marine based pollution, and global climatechange. The reefs of South-East Asia and the Caribbeanare the most threatened.

Figure 3 Extensive deforestation in the Amazon, Rondonia,Brazil, 2001. Landsat photo Courtesy of U.S. Geological Survey.

Cone SnailsExtremely Valuableto Medicine and Under ThreatCone snails, a large genus of approximately 500species (see Figure 1), inhabit shallow waters in trop-ical coral reefs and associated soft bottom habitatssuch as mangroves, seagrass beds, and mud ats.They defend themselves and paralyze their preyworms, sh, and other molluscsby injecting acocktail of toxic peptides through a hollow,harpoon-like appendage. South-East Asia is homefor 56% of the worlds cone snail species, with thePhilippines being an especially rich zone(8 species are found only in the Philippines).A new report estimates that 88% of the coral reefsin South-East Asia are threatened by humanactivities; in the Philippines, the gure is 97%.Threats to cone snails come from destruction of the reefs and of their other habitats (e.g. 50% of the worlds mangroves have been cleared for woodand for development and aquaculturein thePhilippines, 60% have been cleared), and fromdirect exploitation, as cone snails are widelygathered for collectors and, recently, for biomedicalresearch. Those species with highly restrictedgeographic ranges are the most at risk.


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Habitat loss: FreshwaterFreshwater ecosystems are divided into two majorclassesowing (such as rivers and streams) andstatic (such as lakes and ponds). While the distributionof species is not as well known as for marine andterrestrial ecosystems, it is still clear that freshwaterspecies are similarly concentrated. For sh, the major

tropical rivers, such as the Amazon and its tributaries,hold a large fraction of the freshwater sh species onEarth. Tropical lakes, particularly those in the Rift Valleyof East Africa, also have large numbers of endemicspecies. Some freshwater species are found in greatestnumbers in temperate zonesfor example, the greatestdiversity of crayshes, freshwater turtles, and molluscsis found in the United States.

Riverine habitats have been extensively modiedby damming and by channelizationthe process of straightening rivers and forcing them to ow alongpre-determined channels (as opposed to their natural

meanderings). These processes have threatened manyof the species that live in these habitats, as has pollutioncaused by the run-off of toxic substances and ofnutrients from sewage and fertilizers. Some lakespecies, especially those in boreal regions, may be atparticular risk from the synergistic effects of climatewarming, acid precipitation, and increasedlevels of ultraviolet radiation.

PollutionPollution is a special case of habitat destructionchemical destruction rather than the more obviousphysical destruction. Pollution occurs in all habitatsland, sea, and freshwaterand in the atmosphere. Agrowing body of evidence has implicated some syntheticorganic pollutants with developmental abnormalities,and with effects on the endocrine, reproductive,neurologic, and immunologic systems of wildlife thatmay threaten their survival.

Introduced speciesThe problems of introduced species may be accelerat-ing. After habitat loss, invasive species are thought to bethe leading current cause of species extinctions. Fasterand more extensive international travel makes acciden-

tal introductions more likely. Some introductions aredeliberate. These include potential introductions thatare radically new, such as genetically engineeredorganisms, be they microbes, plants, insects, or sh.

Not all species devastate the communities theyenter. Some do, however, and the example of theaccidentally introduced snake Boiga irregularison Guamillustrates just how damaging an invasive species canbe. Boigadrove seven endemic species of birds to

extinction on Guam. Were this snake to successfullycolonize Hawaii, (some individuals have arrived but arethought not to have lived long), then all of its birdscould be at risk.

Over-harvestingHumans harvest some species to very low numbers anddrive others to extinction. Over-harvesting by hunting,shing, or collecting means that species are driven tosuch low levels that the exploitation is not sustainable.While the most famous examples involve marineresourceswhales and sheriesplants (especiallythose valued for medicines) and higher primates, hunt-ed for bushmeat, can be exterminated in this way.

Secondary extinctionsOnce one species goes extinct, there will likely be manyother extinctions as a consequence. Some are simple tounderstand: for every bird or mammal or insect thatgoes extinct, there will likely be a number of parasite

species or bacteria that will also disappear, as they arehost specicunable to live on any other host.Other changes can be quite complicated. Species

are bound together in ecological communities to form afood web of species interactions. Once a species is lost,the species that fed upon, were fed upon, beneted, orcompeted with that species will also be affected. Thesespecies in turn may affect yet other species. Ecologicaltheory suggests that the patterns of secondary extinc-tions may be quite complicated and thus difcult todemonstrate or predict.

Global climate changeThe global climate has warmed over the last century byabout 0.6 degrees C., and animals and plants haveresponded in many ways as a consequence. Plants leaf out or ower earlier, migratory birds arrive earlier in thespring, and species ranges move towards the poles or tohigher altitudes. Some ecosystems such as alpinemeadows, cloud forests, arctic tundra, and coral reefsare especially sensitive to warming, and species in theseregions may be particularly at risk.

While many species have demonstrated changesin the timing of life stages and in their ranges thatcould affect survival, it is not certain whether globalclimate change has caused any extinctions to date. Twopossible examples are the golden toad and the harlequinfrog from Costa Ricas Monteverde Cloud ForestReserve, whose disappearances seem strongly linked tounusually warm and dry weather caused by the power-ful El Nio event of 1996 and 1997. There is growingevidence, although not conclusive, that global warminghas played a role in the increased strength and durationof El Nio events over the past decade. Mean global

Biodiversity 11


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surface temperatures are expected to increase by1.4 to 5.8 degrees C. (2.5 to 10.4 degrees F.) by the year2100. The magnitude and the rate of this increase,unprecedented for the last 10,000 years, will threatenthe survival of many species, especially those unableto migrate to new ranges or otherwise adapt. Globalclimate change, by itself or acting synergistically with

other environmental changes secondary to humanactivity, could well become the factor most responsiblefor species extinctions over the next 100 years.

Suggested Readings

FAO. 1999. State of the Worlds Forests.U.N. Food andAgricultural Organization, Rome, Italy.

Peters L, Lovejoy TE (eds.). 1992. Global Warming and Biological Diversity.Yale University Press, New Haven.

Pimm SL. 2001. The World According to Pimm: aScientist Audits the Earth.McGraw Hill, New York.

Pimm SL, et al. 2001. Can we defy Natures end? Science233:22072208.

Postel S. 1992. Last Oasis: Facing Water Scarcity.W. W. Norton and Company, London.

Raven P (ed.). 1997. Nature and Human Society:the quest for a sustainable world.National Academy Press,Washington, DC.

Wilkinson CR. 2000. The Status of Coral Reefs of theWorld. Australian Institute of Marine Sciences,Townsville, Australia.



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Ecosystem Services 13

chapter 2 EcosystemServices

Figure 1Hand-Pollination of AppleBlossoms in NepalBees in Maoxian County, at theborder between China andNepal, have gone extinct, forcing people to pollinateapple trees by hand.It takes 2025 people topollinate 100 trees, a task that can be performed by2 bee colonies.

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What Are Ecosystem Services?

An ecosystem is an array of living things (plants,animals, and microbes) and the physical and chemicalenvironment with which they interact. Examples of ecosystems include forests, wetlands, grasslands,streams, and estuaries. Healthy ecosystems provide theconditions and processes that sustain human life. Inaddition to providing goods such as foods andmedicines, ecosystems also provide us with services,such as purication of air and water, the binding oftoxins, decomposition of wastes, mitigation of oods,moderation of storm surges, stabilization of landscapes,and regulation of climate. We tend to take these servicesfor granted and do not generally recognize that we can-not live without them, nor can other life on this planet.

What Is the Value of These Services?

Healthy ecosystems deliver life-sustaining services forfree, and in many cases on a scale so large and complexthat humanity would nd it practically impossible tosubstitute for them. With respect to complexity, weoften do not know which species are necessary for theservices to work, what numbers they must be presentin, and whether there are keystone species for ecosys-tem services. Disruption of these natural services canhave catastrophic effects. For example, if natural pestcontrol services ceased or populations of bees and otherpollinators crashed, there could be major crop failures(see Figure 1). If the carbon cycle were badly disrupted,rapid climate change could threaten whole societies.From an economic standpoint, numerous examplesillustrate that ecosystem services that have beendiminished by human activities can be restored for afraction of the cost of building articial substitutes.

New York Citys water quality was deteriorating dueto development in the Catskill Mountains where the cityswater supply originates. The cost of a ltration plant to deal with the increasing sewage and agricultural runoff would have been U.S. $58 billion plus an annual operating cost of U.S. $300$500 million. Alternatively, a one-time expen-diture of U.S. $1.5 billion was able to restore the integrity of the watersheds natural purication services by purchasing and halting development on land in the Catskills, compen-sating landowners for restrictions on private development,and subsidizing improvement of septic systems.

Examples of Ecosystem Services

Cycling and ltration processes1. Air PuricationForest canopies function as particulate lters andchemical reaction sites that help regulate thecomposition of the atmosphere and purify our air.

Particulates resulting from the combustion of coal andoil, cement production, lime kiln operation,incineration, and agricultural activities are captured byforest canopies. Moist leaf surfaces also provide siteson which potentially polluting compounds can betransformed into harmless ones (see Figure 2).

Microbes in well-drained soils of tropical forests can produce large quantities of nitric oxide. Nitric oxide is avery reactive gas, which, as it moves through the forest canopy, combines with other chemicals on leaf surfaces. Incombined form it does not reach the air above the canopy,where it otherwise would have catalyzed photochemical

reactions in the atmosphere leading to the production oftropospheric ozone. Tropospheric ozone is a greenhouse gasand is also a pollutant that adversely affects both plants and animals, including humans.

2. Watershed Services Forests regulate water ows to downstream areas,yielding relatively regular and predictable ows.Deforestation often leads to disruption of the naturalow pattern, causing cycles of ood and drought.Forests, especially forest soils, also act like massivelters, purifying water as it drips through the forestecosystem (Figure 2).

In a healthy, middle-aged forest in New England,rain falling enters with a nitrogen load of about 8 pounds per acre each year. Stream water leaving this forest will often contain less than one-tenth of the nitrogenentering in rainfall.

3. Purication of Fresh Waters Wetlands absorb and recycle nutrients from humansettlements. As water ows through wetlands, plant,microbe, and sediment processes strip out nutrientssuch as nitrogen and phosphorus. Plants take up thesenutrients and incorporate them into root, stem, and leaf material. Some microbes transform a water-solubleform of nitrogen into gaseous forms of nitrogen.Constructed wetlands are designed to use the nutrientretention and processing features of natural wetlands toremove nutrients and toxins from water.

Nitrogen pollution became a serious problem in thewaters around Stockholm, Sweden. Restoring wetlands toreduce nitrogen loading was considerably less expensive thanthe construction of wastewater treatment plants. Besides thenitrogen ltering, the restored wetlands of the archipelago


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around Stockholm supply a number of ancillary benetsincluding habitat for rare plants and animals andrecreational opportunities.

4. Maintaining Water Quality in Estuaries In many parts of the world, rivers carry excessivenutrients from runoff to coastal estuaries. The resultingnutrient over-enrichment (eutrophication) causes lowdissolved oxygen levels, harmful algal blooms, and lossof submerged aquatic vegetation. Bivalve molluscsincluding mussels, clams, and oysters act as lteringsystems for estuaries that remove suspended materialsand consume algae, addressing the overproductionproblem.

For centuries, the oyster population of the ChesapeakeBay was capable of ltering a volume of water equal to thecomplete volume of the Bay in a three-day period. Pollution,habitat destruction, over-harvesting, and other pressures havedramatically reduced the oyster population, greatly diminish-ing this critical ltering service. With the diminished oyster

population the ltering now takes a year, and the waters of the Bay are poorer in oxygen and generally more polluted .

5. Binding Toxic Substances Human activities have concentrated heavy metals,radioactive elements, and other toxins in various places,rendering some locations unusable and dangerous. Incleaning up such contaminated sites, we can utilizethe capacity of some vascular plants to concentrate toxicsubstances without harming themselves. For example,mustard plants accumulate lead and certain ferns sopup arsenic.

In a small pond near the Chernobyl nuclear power plant that was contaminated with Strontium-90,Cesium-137, and other harmful radioactive substancesreleased during the reactor re in 1986, scientists grewsunowers on small styrofoam rafts. With the roots of thesunowers dangling in the water, the sunowers rapidlyaccumulated levels of radioactive cesium and strontium that

were several thousand times higher than the concentrationsin the water.

6. Detoxication of Sediments and Soils Microbes can help detoxify some human-generatedwastes. For example, oil spilled into estuaries andmarine ecosystems poses health risks to humans andother species. When certain compounds from petrole-um hydrocarbons adhere to sinking particles, they settleto the sediment surface, where naturally occurringmicrobes can detoxify the compounds and ultimatelydegrade them to carbon dioxide and water.

7. Maintenance of Soil Fertility Soils, with their active microbial and animalpopulations, have the capacity to supply adequatenutrients to plants in suitable proportions. Soil animalsand microbes break down organic matter and releasenutrients into the soil solution. Electrical chargescarried by tiny soil particles give them the ability toretain these nutrients and release them to plant roots.

Stabilization processes8. Control of potential pest and disease-causing species Many weeds, insects, rodents, bacteria, fungi, and otherpests compete with humans for food, affect ber

Forest canopy and leaf litter protect the soilsurface from the erosivepower of rain

Forest trees and plantsstore carbon and help

slow human-causedglobal climate change

Forest tree roots bindsoils and help preventerosion

Deep forest soils storelarge volumes of water

Forests help maintainthe water cycle andstabilize local climates

Forests provide goodssuch as food, timber,and medicines

Forests provide criticalhabitat for plants,animals, and microbes

Forest canopy purifies airby ltering particulatesand providing chemicalreaction sites wherepollutants are detoxified

Forest soils purify water,acting as a massive filter

Figure 2 Forest Ecosystem Services.


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production, or spread disease. Certain animals andmicrobes do us the service of naturally controlling someof these pests, which can cause disease in plants andanimals, including humans. In addition, using thesenatural controls as a model, scientists have developedsome biological controls to replace pesticides.

In the 1950s, Chinese ofcials became concerned that

birds were allegedly devouring large amounts of grain, and they declared small perching birds to be the enemy. Millionsof Chinese began killing birds with frightening success; over several days in 1958, an estimated 800,000 birds werekilled in Beijing alone. Major pest outbreaks resulted from this bird eradication program, leading to signicant croplosses. The mistake was ultimately realized and the bird killing halted.

9. Mitigation of Floods Floodplains are ecosystems that border rivers subjectto ooding. Following excessive rains, ood waters owover riverbanks and into these oodplain forests and

wetlands. Some of the water is soaked up by the soil.When the oodwaters recede, they leave behindnutrient-rich sediments that enhance soil fertility,making these ecosystems extremely productive.Unaltered ood plains also provide habitat for manyplant and animal species.

Because the ood mitigation services of theMississippi River oodplain were not adequately recognized,nine U.S. midwestern states suffered a terrible toll in the oods of 1993: 50 people were killed, 70,000 lost their homes, and property losses were estimated at U.S. $12billion. The high cost of the ood damage resulted, in part,

from drainage of oodplain wetlands, building of permanent structures on the oodplain, and construction of levees.

10. Stabilization of Landscapes against ErosionForests and grasslands provide natural protection forsoils against erosion in several ways. Plant canopiesintercept rainfall and reduce the force with whichrainwater hits the soil surface. Roots bind soil particlesin place and prevent them from washing down slopes.And old root channels help to minimize the powerfulforce of surface runoff by routing water into the soilprole. Human actions, like clearing forests andplowing up grasslands to expand agriculture, accelerateerosion, causing the loss of useable cropland and otherdestructive outcomes.

Hurricane Mitch stalled off the coast of Honduras inOctober 1998, dropping up to 25 inches of rain in one six-hour period in some places. The resulting ooding and mud-slides killed over 10,000 people. Many of the deadly mud-slides occurred in areas where forests had been cleared for agriculture (Figure 3).

11. Buffering the Land against Ocean Storms Salt marshes, mangrove forests, and other ecosystemsbuffer the coastline against ocean storms. Plants inthese ecosystems stabilize submerged soil (sediment),thereby preventing coastal erosion. These ecosystemsare also breeding grounds and nurseries for commer-cially important sh, and vital habitat for many bird and

other species. Unfortunately, these ecosystems are beingrapidly destroyed, lled in, and built upon.Scientists at the Mangrove Ecosystems Research

Centre in Hanoi, North Vietnam have found thatmangroves are more effective than concrete sea walls incontrolling raging oodwaters from tropical storms.Unfortunately, mangrove forests are under assault from coastal development, shrimp aquaculture, andunsustainable logging. Some countries, such as thePhilippines, Bangladesh, and Guinea-Bissau have lost70 percent or more of their mangrove swamps.

12. Carbon Sequestration on Land and Global Climate

Land ecosystems are large storehouses of carbon, bothin plant tissue and in soil organic matter. By absorbingcarbon, these ecosystems help slow the growth of atmospheric carbon dioxide. Were it not for thisterrestrial carbon sink, the rate of carbon dioxide accu-mulation in the atmosphere would be almost twice asfast as it is today, leading to more rapid climate change.

Biodiversity preservation13. Providing Critical HabitatEcosystems provide critical habitat for plant, animal,and microbial species that have intrinsic value, as well

as providing valuable services to humans.14. Genetic Library FunctionThe vast pool of novel genetic information stored in nat-ural ecosystems represents the possibility of solutions toan enormous range of challenges. Genetic diversity is arich, relatively untapped resource for present and futurebenets in agriculture and medicine. Thirteen of the 20best-selling prescription drugs in the U.S. are eithernatural products, natural products that have been slight-ly modied chemically, or manufactured drugs thatwere originally obtained from organisms.

Translocation processes15. Pollination of Crops and Natural VegetationMany owering plants rely on animals to help themmate by ensuring fertilization. Bees, butteries, beetles,hummingbirds, bats, and other animals transportpollen, the male reproductive structures, from one plantto another, with enormous benets to humanity (seeFigure 1). Approximately one third of the worlds food


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crops depends on these natural pollinators. In theU.S., honeybees pollinate about U.S. $10 billion worthof crops.

The oil palm was introduced into Malaysia from the forests of Cameroon in West Africa in 1917, but the weevil that pollinates the African oil palm was not introduced at the same time. For decades, the palm growers of Malaysiarelied upon expensive, labor-intensive hand pollination. In1980, the weevil was imported to Malaysia, boosting fruit

yield in the palms 4060 percent, and generating savings inlabor cost of U.S. $140 million per year.

16. Dispersal of Seeds Animals such as toucans, monkeys and fruit batsconsume tree fruits and scatter piles of seed-rich dungacross the landscape. Similarly, gray squirrels distributeacorns over broad areas propagating the spread of oaktrees. This service helps trees populate their habitat,and migrate across the land in response to a variety of disturbances, including climate change.

Life-fullling functions

17. RecreationHuman health and well being are greatly enhanced byoutdoor activities including hiking, skiing, camping,swimming, bird watching, bicycling, shing, boating,and more. Ecosystems provide us with the naturalenvironment in which to enjoy such activities.

18. Aesthetics The natural world is a thing of beauty largely becauseof the diversity of life in its ecosystems. Being in Naturegives us comfort and hope. Nature inspires painters,writers, architects, and musicians to create worksreecting and celebrating its beauty. There is gatheringevidence that our emotional well-being is enhanced by

being in Nature.

Factors Affecting Ecosystem Services

Climate changeHuman activities (such as burning fossil fuels) areincreasing atmospheric concentrations of carbondioxide and other gases, intensifying Earths naturalgreenhouse effect. Global average surface temperaturerose 0.6 C (1.o F) during the 20th century and isprojected to rise another 1.4 to 5.8 C (2.5 to 10.4 F) inthe 21st century, mostly due to human activities. This

temperature rise is associated with more extremeprecipitation and faster evaporation of water, leadingto greater frequency of both very wet and very dryconditions. Global sea level is rising, as water expandswhile warming, and as mountain glaciers around theworld melt.

Many ecosystems will be highly vulnerable to theprojected rate and magnitude of climate change. Some,including alpine meadows, mangrove forests, and coralreefs are likely to disappear entirely in some places.Other ecosystems are projected to become fragmentedor experience major species shifts. The services lostthrough the disappearance or fragmentation of certainecosystems will be costly or impossible to replace.

DeforestationTemporary or permanent clearing of forests for agricul-ture or other uses is of major concern, particularly inthe tropics. Forest destruction threatens the survival of native peoples. It results in decreased soil fertility andincreased erosion. Uncontrolled soil erosion can affectthe production of hydroelectric power as silt builds upbehind dams. Increased sedimentation of waterwayscan harm downstream sheries, and in coastal regionscan result in the death of coral reefs. Deforestation alsoleads to a greater incidence of oods and droughts inaffected regions.

Deforestation contributes to loss of species, withtropical species especially vulnerable to habitatmodication and destruction. Migratory species, includ-ing birds and butteries, also suffer. Deforestation canlead to changes in both regional and global climate.When a large forest is cleared, rainfall may decline anddroughts may become more frequent in the region.

Figure 3 Severe Erosion from Hurricane MitchMiramondoRoad, Honduras.The combination of deforestation andtorrential rains from Hurricane Mitch at the end of Octoberand early November, 1998 contributed to massive landslidesin Honduras,destroying innumerable roads,33,000 homesand 95 bridges,and resulting in 7000 deaths,5000 missing,and tens of thousands of cases of cholera, malaria, anddengue fever.

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Deforestation contributes to global warming byreleasing stored carbon into the atmosphere andby eliminating a potential sink for atmosphericcarbon dioxide.

DeserticationDesertication, affecting 70 percent of the worlds dry-lands, is the degradation of once fertile arid and semi-arid croplands, pastures, and woodlands into desertsthat have lost their biological or economic productivity.It is due mainly to climate variability and unsustainablehuman activities such as over-cultivation, over-grazing,deforestation, and poor irrigation practices.

Desertication undermines food production.Stabilization of soil against water and wind erosion isdiminished. Degraded land may cause downstreamooding, reduced water quality, sedimentation in riversand lakes, and the accumulation of silt in reservoirsand navigation channels. It can cause dust stormsthat exacerbate human health problems includingeye infections, respiratory illnesses, allergies, and casesof meningococcal meningitis. Critical habitat for plantand animal species is lost as desertication proceeds,leading to economic losses, including those fromdeclining tourism.

UrbanizationThe worlds human population is becoming increasinglyurban. Land-use changes and pollution associated withurbanization cause the loss of plant and animal habitatand diminish stabilization functions. For example,urbanization often leads to increased erosion and

reduced natural watershed control of oods. The llingin of wetlands for urban expansion eliminates theirwater cleansing function.

Wetland drainageOver the 20th century, some 10 million squarekilometers of wetlands have been drained across theglobe, an area about the size of Canada. In the lower 48states of the U.S., drainage has reduced wetland areasby half, mostly for agriculture. In the process, criticalwildlife habitat has been lost, as have oodplains, whichare safety valves for ood events and natural lters forowing waters.

PollutionPollution of air, rain (and snow), surface waters, and theland diminishes ecosystem services in many ways. Theair pollutant ozone, for example, can reduce growth of agricultural crops and plants in natural ecosystems.Pollution of rain with sulfur and nitrogen compoundsresults in acid rain that damages plants, impoverishessoils, and acidies surface waters, killing plant and

animal inhabitants. Nitrogen pollution causes harmfulalgal blooms that deplete the water of oxygen,sometimes severely enough to cause major sh kills.Heavy metals from smelters accumulate in soils, killingplant life and thus creating erosion problems. Persistentorganic pollutants such as DDT and PCBs can alterfood webs and thereby diminish the ability of

ecosystems to deliver services such as pest control.Dams and water diversionDams and diversions change the natural ows of rivers,altering the quality of aquatic habitat and causingspecies losses. Reservoirs created by dams destroyformer land plant and animal habitats, degradingnatural beauty and compromising certain forms of recreation. In arid regions, reservoirs lead to greaterwater evaporation, resulting in increased salinity. Whenthis water is used for irrigation, salt accumulates in thesoil, resulting in a decline in crop yields, and in extremecases, rendering the soil unt for agriculture.

Invasive speciesBy affecting ecosystem functions, for example, byaltering the food web, invasive species reduce the abilityof ecosystems to deliver life-sustaining services.

Lake Victoria, bordered by Kenya, Uganda, and Tanzania, is an essential source of water and sh protein for the surrounding human population. Invasive species and excess nutrient enrichment have transformed Lake Victoria from a clear, well-oxygenated lake with an incredible diversi-ty of cichlid shes to a murky, oxygen-depleted, weed-choked lake with reduced sh diversity (dominated by predators).

The changes have been so dramatic that the ability of thelake to meet human needs is now threatened.

Suggested Readings

Aber J, Melillo J. 2001. Terrestrial Ecosystems(SecondEdition). Academic Press, San Diego, CA.

Baskin Y. 1997. The Work of Nature.Island Press,Washington, D.C.

Burger J, et al (eds.). 2001. Protecting the Commons.Island Press, Washington, D.C.

Daily G (ed.). 1997. Natures Services.Island Press,Washington, D.C.

Watson R, et al (eds.). 1998. Protecting Our Planet,Securing Our Future. The World Bank, Washington, D.C.



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Medicines from Natural Sources 19

chapter 3 Medicines fromNatural Sources

Figure 1 Taxus brevifolia(Pacic Yew Tree).

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History

Plants have formed the basis of traditional medicinesystems that have been in existence for thousands of years. The rst records are from Mesopotamia and datefrom about 2600 B.C.; among the substances used wereoils of Cedrus species (cedar) and Cupressus sempevirens(cypress), Glycyrrhiza glabra (licorice), Commiphoraspecies(myrrh), and Papaver somniferum (opium poppy),all of which are still in use today for the treatment of various ailments. Egyptian medicine dates from about2900 B.C., with the best known Egyptian pharmacopeiabeing the Ebers Papyrus dating from 1500 B.C.; thisdescribes some 700 drugs (mostly plants), and includesmany formulas. The Chinese Materia Medica has beenextensively documented over the centuries, with the rstrecord containing 52 medicines (Wu Shi Er Bing Fang,1100 B.C.), followed by 365 medicines (Shennong Herbal ~100 B.C.), and then 850 medicines (Tang Herbal, 659A.D.). Similarly, documentation of the Indian Ayurvedicsystem dates from about 1000 B.C.; this system formedthe basis for the primary text of Tibetan Medicine,Gyu-zhi (Four Tantras; translated ~8th century A.D.).

In the ancient Western world, the Greeks con-tributed substantially to the development of herbaldrugs, with Theophrastus (~300 B.C.), Dioscorides (100A.D.) and Galen (130200 A.D.) being the majorinuences. Except for some recording of this knowledgeby monasteries in Western Europe during the Dark andMiddle Ages (fth to twelfth centuries), it was the Arabswho were mainly responsible for preserving much of the Greco-Roman expertise, and for expanding it toinclude the use of their own resources, notably Chineseand Indian herbs unknown to the Greco-Roman world.The Persian physician philosopher Avicenna (9801037A.D.), contributed much to the sciences of pharmacy andmedicine through works such as Canon Medicinae,which attempted to integrate the medical teachings of Hippocrates and Galen with the biological insights of Aristotle, and which served as a textbook for medicalstudents for centuries.

Current Usage of Plant-derived

MaterialsEven in modern times, plant-based systems continue toplay an essential role in health care. It has been estimat-ed by the World Health Organization that approximately80% of the worlds population from developing coun-tries rely mainly on traditional medicines (mostlyderived from plants) for their primary health care. TheWHO has recently decided to begin cataloguing and

evaluating the safety and efcacy of these remedies.Plant products also play an important role in the healthcare for the remaining 20% in developing countries,and for those in industrialized countries as well. Forexample, analysis of data on prescriptions dispensedfrom community pharmacies in the United States from1959 to 1980 indicated that about 25% contained plant

extracts or active principles derived from higher plants.And at least 119 chemical compounds, derived from 90plant species, are important drugs currently in use inone or more countries. Of these 119, 74 % were discov-ered during attempts to isolate the active chemicalsfrom plants used in traditional medicines. Such com-pounds are not only useful as drugs in their own right,but may be even more useful as leads to other mole-cules, though synthetic in nature, that are based uponthe active natural products.

There are many examples of such plant-baseddrugs in current use, some which are given below:

Quinine The isolation of the anti-malarial drug, quinine, fromthe bark of Cinchona species (e.g., C. ofcinalis), wasreported in 1820 by Caventou and Pelletier. The barkhad long been used by indigenous people of theAmazon region for the treatment of fevers, and wasintroduced into Europe (early 1600s) to treat malaria.Using the structure as a lead, chemists synthesized theanti-malarial drugs, chloroquine and meoquine.

ArtemisininAnother plant used in the treatment of feversfor morethan 2000 years in traditional Chinese medicineArtemisia annua (Quinhaosu) yielded the agentartemisinin in 1985. Its more soluble derivatives,artemether and artether, are currently in use againststrains of malaria increasingly resistant to the rst linetreatmentschloroquine and sulfadoxine-pyrimethamineand are considered to be the mosteffective anti-malarial agents on the market today.

Morphine This opiate, isolated in 1816 by Serturner from theopium poppy, Papaver somniferum,had been used as ananalgesic for over 4000 years. By using the structure as

a model, chemists subsequently developed a series of highly effective synthetic opiate analgesic agents.

Paclitaxel (Taxol Bristol-Myers Squibb)Probably the most signicant drug discovered anddeveloped through the U.S. National Cancer InstitutesDevelopmental Therapeutics and Clinical TrialsEvaluation Programs is paclitaxel, isolated in 1969 aspart of a broad plant screening program, from the bark


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of the Pacic Yew tree (Taxus brevifolia) (Figure 1). Inearly clinical trials (1989), it was found to be effectivefor inducing remission in cases of advanced ovariancancers (by a mechanism unlike that of other knownchemotherapeutic agents), and since that time, it hasshown signicant therapeutic benet for other advancedmalignancies, including lung cancers, malignant

melanomas, lymphomas, and metastatic breast cancers.It has also shown promise in preventing the smoothmuscle cell proliferation that can block arteries openedby stents. As its natural source of supply could not berelied upon (the number and distribution of Pacic Yewtrees was simply not known), paclitaxel and other tax-oids have been produced by semi-synthetic conversionsof a precursor compound found in renewable yew treeneedles. The paclitaxel story illustrates the great impor-tance of conserving natural resources, as this highlyeffective therapeutic agent was discovered only becauseof a random screening of 35,000 plant samples. It alsodemonstrates how highly complex bioactive moleculesfound in nature like paclitaxel (Figure 2) are unlikely tobe discovered by combinatorial chemistry alone, buthow, once they are discovered, they can serve as modelsfor synthetic or semi-synthetic therapeutic agents thatmay be as, or even more, effective than the originalnatural product.

South American IndigenousKnowledge and Medicinal Plants

Unlike the case in Asia and the Indian subcontinent,where written records were kept about medicines, knowl-edge about the use of specic plants for treating diseasesin South America was mostly passed on orally amongindigenous peoples. Below are two examples of materialsthat are currently used, both in the countries of origin

Figure 2 Taxol (Paclitaxel) molecule, demonstrating a highly complex, interlocking ring structure that would be nearly impossible to discover by synthetic means alone.

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and in the West. There are numerous other exampleswhere ethnomedical information may be of utility.

CurareThis is a generic term for a group of arrow poisonsfrom South America. They were rst described byexplorers such as Sir Walter Raleigh, dating from theend of the 16th Century. However, it was another 200years before von Humboldt conducted a systematicsearch for the botanical sources of curares. Somecurares from eastern Amazonia are derived mostlyfrom various species of plants from the genus Strychnos.But it is the extracts from the South American vineChondodendronthat are the most common curares, andwhich, because of their observed ability as neuromuscu-lar blocking agents, were successfully employed (in1932) for the treatment of tetanus muscle spasms andother spastic disorders. Isolation of the most activeagent from C. tomentosum, t-tubocurarine, led to a num-ber of synthetic and semi-synthetic reversible paralyzing

agents, which are very widely used in general surgerytoday to achieve deep muscle relaxation (especiallyimportant during abdominal and orthopedic operations)without the need for high doses of general anesthetics.

jaborandi, ruda-do-monte This material is extracted from the leaves of Pilocarpus jaborandi and is known in the West as pilocarpine.Indians of northeast Brazil, including the Apinaye, haveused it as a stimulant for lactation and as a diuretic. Theactive principle, pilocarpine, was rst isolated in Brazilby Coutinho in 1875. Pilocarpine is currently usedmedically to stimulate salivation following head andneck radiation treatments or in Sjogrens syndrome(which affects the salivary glands), and in the treatmentof open-angle glaucoma.

Microbially-derived Agents

Although signicant emphasis has been given to plant-derived agents in the general literature, from the per-spective of biodiversity, the most diverse organisms onthe planet are the microbes. It is estimated that lessthan 5% of all microbial ora has been investigated todate, but it is likely that the percentage is much lowerthan this gure, as the micro-organisms present inmost environments have barely been studied. Ordinaryseawater, for example, contains more than 1000microbes of multiple species per cubic centimeter.Similarly, in one cubic centimeter of soil, more than1000 different species of microbial ora have beenfound, with less than 5% of these able to be culturedusing current techniques.


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cillin was developed, and over the next several years,it proved to be a remarkably effective antibiotic formillions of patients. In the late 1940s, however, initialreports of bacterial resistance due to destruction ofthe antibiotic by microbes surfaced. Another group of-lactam antibiotics, rst isolated from the fungusCephalosporium acremonium,was developed and was

found to overcome these early cases of resistance.With modication of the basic nucleus of the -lactamstructure, whilst still maintaining activity, medicinalchemists were able to synthesize over 40,000 active-lactam-containing molecules, approximately 30 of which are currently in use today.

The Aminoglycosides Stimulated by the discovery of penicillin, Waksman andhis co-workers investigated a number of tropical soilbacteria, the actinomycetes, to determine if they toocontained anti-microbial compounds. In 1944, theyreported the discovery of streptomycin, isolated from

the bacterium Streptomyces griseus,that was highlyeffective against the bacterium causing tuberculosis,Mycobacterium tuberculosis.With the advent of resistancein M. tuberculosisand in other microbes, and with theidentication of bacterial resistance mechanisms byDavies and his colleagues in the early 1970s, manysemi-synthetic variants of the natural compounds dis-covered by Waksman, the aminoglycosides, have beenmade. These agents are still widely used in infectiousdisease treatment.

What is particularly exciting in recent years is thework by a number of marine natural product chemistsand molecular biologists who have begun to examinethe essentially unexplored marine microbial world as asource for novel structures and pharmacologic activity.The work of Fenicals group, for example, on marinemicrobes associated with invertebrates and plants,

as well as on those that are free-living, has provided asmall glimpse of the vast potential that is present inthe oceans for the development of new medicines,made even greater by modern techniques of genemanipulation.

The microbes were an unappreciated resource formedicines until the chemical identication of the antibi-otics penicillin and streptomycin was made in the early1940s. The discovery of antibiotics and their subsequentproduction in massive quantities has revolutionized thetreatment of many infectious diseases. However, asmicrobes rapidly evolve to develop resistance to avail-able anti-microbials, it is a constant race for scientists tond novel compounds that are effective.

There are many examples of antibiotics originallyobtained from microbes that are in current use, some of which are given below:

Penicillins and Cephalosporins (the -lactam antibiotics)In 1928, Alexander Fleming noticed that a fungus,Pencillium notatum, that had contaminated one of hiscultures of staphylococcus bacteria, killed the bacteriaadjacent to it. A decade later, the systemic drug peni-

Figure 3 Natural Product Drug Discovery and Development inthe United States (in developing and other developed countries,a similar model is used).

ACQUISITION DISCOVERY PRECLINICAL DEVELOPMENT CLINICAL DEVELOPMENT

Source of Test SamplesNatural Products

Extract PreparationCrude extractsRemoval of unwanted compoundsEnrichment

Preassay WorkupFormatting for AssaysStorage/Retrieval of Samples

Screening StrategiesRandomTargettedRational(Ethnobotanically directed)

Conrmatory ScreeningConrmationSpecicityMechanism(s) of Action

Chemical Isolation & IdenticationIsolation of pure compound(s),based on bioactivity

Initial Chemical SuppliesAcquisition of sufcient raw mate-rial or derivation of a syntheticscheme to provide enough drugsubstance

Preliminary Animal StudiesActivity in living modelsSimple toxicity studiesInitial drug distribution in animals

Large-scale SupplyProduction Drug Substance indened lots meeting govern-ment standards

Advanced Animal StudiesFormulation(s)Toxicology (up to two years in twospecies)StabilityExtended animal efcacy studiesFull drug distribution studies

Investigational New DrugApplication (INDA)to US Food and DrugAdministration or equivalent

Clinical Trials in Man Phase ISafety in healthy volunteers orpatients (cancer/AIDS)

Clinical Trials in Man Phase IISafety and Efcacy in patients

Clinical Trials in Man Phase IIIEfcacy versus established treat-ments in larger numbers of patients

New Drug Application (NDA)to US Food and DrugAdministration or equivalent

Commercial Product

Post Market Surveillance(essentially a Phase IV)Continued studies on safety andefcacy


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Cone SnailsEach of the approximately 500 cone snail speciesis believed to produce its own distinct set ofpeptide toxins, numbering 100 on average, sothere may be as many as 50,000 different toxinsin all. Less than 0.2% of these have been character-

ized, and only a small subset of this number hasbeen analyzed for biological activity. Despite theselimited studies, several potential new medicinesderived from conotoxins are being investigated:

a pain killer called Prialt (ElanPharmaceuticalsformerly called Ziconotide)that is in extended Stage III clinical trials(Figure 3) and is reputed to be 1000 times morepotent than morphine, but unlike morphine andother opiates, it does not lead to tolerance oraddiction.

a broad spectrum anti-epileptic agent that is in

Stage I clinical trials for intractable epilepsy and drugs that may be used to prevent nerve

cell death following strokes or head injuries,treat spasticity secondary to spinal cord injuries,and provide for the early diagnosis and treat-ment of small cell carcinomas of the lung, oneof the most aggressive human cancers.

Cone snails may contain the largest and mostclinically important pharmacopoeia of any genusin Nature.


The Tetracyclines These were another discovery by the Waksman group,which systematically screened soil samples frommany parts of the world to nd antibiotic-producingmicro-organisms. In conjunction with majorpharmaceutical companies such as Lederle and Abbott,they isolated or synthesized many thousands of

derivatives. The basic tetracyclines are still widely usedas therapeutic agents, and currently, relatively simplederivatives of the original structures from 50 years ago,are in clinical trials as potential new therapies againstresistant microbes.

The Anthracyclines Rather than being used against microbes, thesenaturally-occurring agents, and the many thousands of their derivatives that have been synthesized and/ordiscovered over the last 40 years, are predominatelydirected against cancer cells. Perhaps the best knownis Adriamycin, rst reported in the late 1960s, which

despite having signicant side effects (irreversiblecardiac toxicity), is still a prime treatment for breastand ovarian carcinomas.

Current Examples from Vertebrateand Invertebrate Sources

In addition to plants and microbes, there has beenincreasing attention paid to animals, both vertebratesand invertebrates, as sources for new medicines. Oneexcellent example is the work initially conducted byDaly during the 1960s of the skin secretions ofdendrobatid frogs from Ecuador, and of other poisondart frog species in Central and South America (seecover photo and Chapter 4). This work has led to theidentication of a number of alkaloid toxins that bindto multiple receptors in the membranes of nerveand muscle cells. One compound derived from thesestudies, which binds to nicotinic acid receptorsassociated with pain pathways, the synthetic ABT 594(Abbott Laboratories), is in Phase II clinical trials, andhas generated a great deal of interest, as it has beenshown to be 30100 times more potent as an analgesicthan morphine.

Natural Pesticides

Most lay people usually think of natural products fromonly a drug, or natural treatment, perspective.However, a very important area that is not usuallyconsidered is the use of natural compounds asagricultural agents of many types, that keep peoplehealthy by maintaining adequate food supplies andpreventing malnutrition. These natural product agricul-tural agents, ranging from crude enriched extracts andtheir derivatives to puried compounds, are particularlyimportant in developing countries, where the use of expensive synthetic agents is not possible. They arebeing used increasingly in developed countries as well,as organic farming methods proliferate.

Perhaps the most important use of such naturalcompounds is as insecticides. Insect pests are one of the major causes of poor agricultural yields, and the useof these natural insecticides can lower the costs of foodproduction (or, for that matter, the production of


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medicinal plants). Below are some importantexamples where traditional knowledge is being used inconjunction with modern chemistry.

Pyrethroids One of the oldest and most successfully used plantproducts (from the 19th Century) is the powder frompyrethrum owers, Chrysanthemum cinerariaefolium,originally native to the Dalmatian Mountains in Croatia(major producers currently are Kenya, Uganda, Rwanda,and Australia). Conventionally, the natural productsfrom the pyrethrum owers are referred to aspyrethrins; "pyrethroids" refer to insecticides that usepyrethrins as prototype structures. The pyrethroids actquickly on insects and do not concentrate in surfacewaters. All the decomposition products are of lowertoxicity than the parent compound. Hence, there seemslittle risk that toxic residues will accumulate andcontaminate the environment.

Carbamate-based Insecticides Biologically active carbamates were used as far back asthe 17th century in the old Calabar region of southeastNigeria. The Efks used to collect the beans from aplant later named Physostigma penenosum in order tosubject prisoners to its toxic effects as a means of uncovering admissions of guilt. In 1925, the structureof the active agent, physostigmine, was determined,followed by its synthesis in 1935. Subsequently, a largenumber of similar compounds were synthesized andshown to inhibit the enzyme acetylcholinesterase, whichis essential to the operation of muscles in all animals.These compounds cause rapid paralysis of insects, butfrequently they are not lethal by themselves, so are oftenused in combination with other products.

NeemNative to India and Burma, the neem tree is a memberof the mahogany family Meliaceae,and is known as themargosa tree or Indian lilac, Azadirachta indica (Figure4). A perennial, requiring little maintenance for grow-ing, it has been introduced to West Africa and otherparts of the world. Its insect control efcacy was rstrecognized by the fact that locusts would swarm on theA. indica tree but not feed. Extracts from the seeds and

leaves have insect control activity and can be usedwithout further renement. Active ingredients have alsobeen isolated and formulated as commercial products.In addition to its agricultural usage, Neem has beenused medicinally for generations in India as a generalantiseptic. No comprehensive toxicological data,however, is available.


Nereistoxin-Related Insecticides The marine environment is also a source for insecticides.Nereistoxin is an insecticidal poison isolated from themarine worm, Lumbrineris brevicirra.Syntheticmodication of neristoxin has led to a family of agents(cartap, bensultap, and thiocyclam) that have beendeveloped as commercial insecticides, and which arepotent contact and stomach poisons for sucking andleaf-biting insects.

Examples of Values of Natural Productsas Pharmaceuticals

A question that is often asked is whether there is anydata on the nancial value of natural product-deriveddrugs for pharmaceutical companies. A recent analysisby Newman and Laird (1999) demonstrated that thepercentage of sales (not prots) derived from naturalproducts or related compounds ranged from 50% forMerck to 8% for Johnson and Johnson, with the majori-ty of companies falling between 15 and 30 percent.Companies were not included unless they had at leastone drug that sold for more than US $1 billion. Itshould be emphasized that this was a one-time studyusing only 1997 sales gures for drugs that sold morethan US $1 billion that year, and that almost all of thenatural product-derived drugs in this analysis weremicrobial in origin. It was not for another two years thatthe rst plant-derived drug to break sales gures of US$1 billion arrived, and that was Taxol .

Figure 4 Neem tree (Azadirachta indica).

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B a u m a r

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J a v a , B

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d S t e i n d r u c k e r e i v o n

F a . P . W . M . T

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Suggested Readings

Balick MJ, Elisabetsky E, Laird SA (eds.). 1996.Medicinal Resources of the Tropical Forest: Biodiversity and its Importance to Human Health. Columbia UniversityPress, New York.

Balick MJ, Cox PA. 1996. Plants, People and Culture:

The Science of Ethnobotany.Scientic American Library,New York.

Cragg GM, Boyd MR, Cardellina II JH, et al. 1994.Ethnobotany and the Search for New Drugs.In CibaFoundation Symposium Vol. 185, Chadwick DJ & MarshJ (eds.). Wiley & Sons, Chichester, U.K. pp. 178196.

Daly JW. 1998. Thirty years of discovering arthropodalkaloids in amphibian skin. Journal of Natural Products.61:162172.

Kingston DGI. 2001. Taxol, a Molecule for All Seasons.Chemical Communications. Issue 10, 867880.

National Research Council. 1999. From Monsoons toMicrobes: Understanding the Oceans Role in HumanHealth, National Academy Press, Washington, D.C.

Newman DJ, Cragg GM, Snader KM. 2000.The inuence of natural products upon drug discovery.Natural Product Reports, 17:215234.

Newman DJ, Laird SA. 1998. The Inuence of Natural Products on 1997 Pharmaceutical Sales Figures.In Thecommercial use of biodiversity, ten Kate K, Laird SA(eds.). Earthscan Pubs. London, U.K. pp 333335.

Olivera BM, Cruz LC. 2001. Conotoxins, in retrospect.Toxicon. 39:714.

Plotkin MJ. 2000. Medicine Quest,Viking Penguin,New York.



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chapter 4 TheValue of Plants,Animals, and

Biodiversity v2 Screen

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