Ann

ual

Rep

ort

of t

he I

nsti

tute

of

Zool

ogy

Scie

nce for

Conserv

atio

n2000

The

rese

arch

of

The

Zool

ogic

al S

ocie

ty o

f Lo

ndon

the instit

ute

of zoolo

gy a

ims to

main

tain

and s

trength

en its

positi

on a

s a

leadin

g c

entre for

researc

h w

hic

h b

enefit

s the

conserv

atio

n o

f anim

al specie

s

To this end the Institute:

Carries out research of the highest

priority for species conservation in the

fields of animal behaviour, population

and evolutionary ecology, conservation

genetics, reproductive biology and

veterinary science.

Puts this work into practice through the

application of sound scientific principles

to the conservation of animal species in

the wild, in captive breeding programmes

and in reintroductions to natural or

restored habitats.

Disseminates information about the

science underpinning conservation and the

application of this knowledge

through a programme of teaching and

training and by the transfer of

advanced biological techniques to other

organizations and countries.

Through its Veterinary Science Group,

maintains the highest standards of health

and welfare in the animal collections at

London Zoo and Whipsnade Wild Animal

Park in support of their programmes in

conservation education and the husbandry

and breeding of threatened species.

Contents

Foreword by Paul Harvey

Director’s introduction

Funding and Collaborations

Evolutionary ecology

Population biology

Origins and maintenance of biodiversity

Conservation biology and management

Scientific publications and meetings

Education and training

Staff

Representation

Publications

1

2

4

6

10

14

18

22

24

28

30

31

For the Institute of Zoology, the year2000 saw fundamental changes withfar reaching consequences. TheInstitute has long aspired to becomea National Centre for ConservationBiology and now, with our new andsynergistic association with theUniversity of Cambridge, we areworking together in this role.

The appointment of Dr GeorginaMace OBE as the Institute's newDirector strengthens further ouracademic leadership of this field.Georgina has worked closely andsuccessfully with eminenttheoretical, laboratory and fieldbiologists from across the world tomake conservation biology an appliedscience. The result is that ever moreaccurate predictions aboutpopulation changes in the light ofenvironmental pressures can bemade to inform international andnational decision-making processes.Academic distinction has beeninterwoven with other activities in thecareer of the Institute's new Director.Georgina has led ZSL DiscussionMeetings and Symposia, and editedseveral books as well as the Society'ssuccessful new journal ‘AnimalConservation’. She was alsoinstrumental in forging andformalizing the new association withthe University of Cambridge.

It is my pleasure as Secretary of The Zoological Society of London topresent this report of a selection ofthe Institute of Zoology's scientificactivities over the past year. The

report spans not only scientificresearch of the highest quality, butalso the Society's scientificpublications from journals to books,postgraduate training, veterinarywork, and practical conservation.Each of those facets of the Institute'sscientific activities is set to flourishwith the new administrativestructures and academic inputavailable to its staff.

Paul Harvey FRSSecretary, The Zoological Society of London

foreword 1

fore

word

2 director’s introduction

directo

r’s

introductio

n

It was a great privilege for me to beappointed as Director of Science. Mythanks go to Dr Bill Holt who was amost capable Acting Director duringthe difficult period followingProfessor Morris Gosling’s departurein 1999.

Our scientific mission to undertakeresearch in conservation biology hasbeen greatly strengthened this yearthrough a new funding partnershipwith the University of Cambridge.The Institute’s core research work issupported by an annual grant ofabout £1.7 million from the HigherEducation Funding Council forEngland (HEFCE). Since 1988 wehave received this grant through theUniversity of London. However,following an audit by HEFCE in1998, it became clear that tostrengthen our standing as aconservation biology researchinstitute we needed to identify a newfunding partner. Much time over theyear was spent investigating andevaluating alternative newarrangements. Our preferred choicewas for a strategic partnership withthe University of Cambridge, whichwould provide a first class researchenvironment as well as linkages tothe network of conservation NGOs inthe Cambridge area. A new strategicplan for the Institute was drawn upwith colleagues in the ZoologyDepartment in Cambridge, and wasaccepted by HEFCE as a basis forfuture funding. The newarrangements came into effect at theend of the year. As I write this we are

pursuing various routes to strengthenthe linkages with Cambridge: weexpect this to be a closer academicpartnership than was the casepreviously with the University of London.

All staff participated in variousstages of strategic planning to defineour five-year plan for HEFCE. Thisexercise was particularly helpful forhighlighting our comparativestrengths and weaknesses, and theway in which our work relates to thatof our parent organizations – TheZoological Society of London (ZSL)and the University of Cambridge. Wereviewed all current projectsaccording to three criteria: scientificexcellence, mission-relevance andpotential for external funding. Ideallyour work should score highly on all ofthese but we aim to support someimportant, but difficult to fund,projects where they are of greatstrategic value. Our research shoulddevelop at the interface betweensignificant practical conservationprogrammes (by ZSL among others)and the excellent academic work ofour partners in Cambridge, to supportthe conservation of animal species.We value our position as aconservation biology researchinstitute with a wide network ofcollaborators incorporating academic,governmental and non-governmentalorganizations, and hope to developfurther our role in forging linkagesand providing solutions to pressingconservation problems.

The year included some importantscientific publications, internationalprizes, new grants and othersuccesses. Despite this having beena somewhat uncertain year withchanges in academic partner anddirector, the IoZ staff have continuedto deliver excellent scientific resultsin an increasingly competitive field.This report bears testament to thatwork which will, I am sure, continueto flourish under our newarrangements.

Georgina MaceDirector of Science

director’s introduction 3

4 funding and collaborations

fundin

g a

nd

colla

bora

tions

FUNDING ORGANIZATIONS

A H Schultz-Stiftung (Switzerland)Alistair Voller Overseas Travel FundAssociation for the Study of Animal BehaviourAssociation of British Wild Animal KeepersBat Conservation InternationalBBC Natural History UnitBBSRCCook (UK) LtdDalgety/PICDepartment of the Environment, Transport and the RegionsEnglish NatureEuropean UnionFFIG & A Claraz-Schenkung (Switzerland)GlaxoWellcomeGoethe-Stiftung (Switzerland)HEFCEIntervetIUCNJoint Nature Conservation CommitteeLincoln Park ZooMAFFMerial Animal HealthNational Geographic SocietyNATONERCNorth American Freshwater Fishes TAGNovartis Stiftung (Switzerland)People’s Trust for Endangered SpeciesPrimate Conservation Inc. (USA)Royal Geographical SocietyRoyal Society for the Protection of BirdsSchweizerische Akademie der Naturwissenschaften

(Switzerland)Schweizerischer Nationalfonds zur Förderung der

Wissenschaftlichen Forschung (Switzerland)Smithsonian National Zoological Park FundThe British Andrology SocietyThe British CouncilThe Leverhulme TrustThe Natural History MuseumThe Royal SocietyThe Wellcome TrustTimes Cheetah AppealUniversities Federation of Animal WelfareUPB PorcoframWildlife Conservation SocietyWWF-UKXY Inc., Fort Collins (USA)

COLLABORATORS

UniversitiesAnglia PolytechnicBerne (Switzerland)Brigham Young (USA)BristolCalifornia (USA)CambridgeCardiffColumbia (USA)Duke (USA)DundeeEast AngliaEdinburghGeorgia (USA)Hong Kong (China)Imperial College, LondonIshinomaki (Japan)King’s College, LondonLausanne (Switzerland)LeedsLisbon (Portugal)LiverpoolLouisiana (USA)LutonMahajanga (Madagascar)Michigan State (USA)Montpellier (France)Murcia (Spain)National University of Ireland (Cork)New England (Australia)OxfordPierre et Marie Curie (Paris)Princeton (USA)Queen Mary & Westfield College, LondonQueensland (Australia)Regensburg (Germany)Royal Veterinary College, LondonSan Juan (Puerto Rico)SheffieldSurrey RoehamptonSussexUniversity College, LondonVermont (USA)Wageningen (The Netherlands)Washington (USA)West of EnglandYorkZurich (Switzerland)

funding and collaborations 5

OtherAnimal Gene Storage and Resource Centre of AustraliaBBSRC Silsoe Research InstituteBombay Natural History Society (India)Centre for Ecology & Hydrology (NERC)Centre for Environment, Fisheries and Aquaculture ScienceChinese Academy of Science, BeijingCSIRO Australian Animal Health LaboratoryDepartment of Agriculture and Rural Development for Northern IrelandDesert Research Foundation of Namibia Direction Générale de Forêts (Tunisia)Dulwich HospitalDurrell Wildlife Conservation TrustEnglish NatureEstación Experimental de Zonas Aridas, Consejo Superior de Investigaciones

Científicas (Spain)Fisheries Research Services (Aberdeen and Pitlochry)Foundation for Nature Research (Norway)GlaxoWellcomeHungarian Academy of SciencesInstitut für Zoo- und Wildtierforschung, BerlinInstitute of Animal HealthInstituto Nazionale per la Fauna Selvatica, BolognaIUCN Species Survival CommissionKing Khalid Wildlife Research Centre (Saudi Arabia)KORA (Switzerland)MAFF Veterinary Laboratories AgencyMarwell Zoological ParkMoredun Research InstituteNational Museums of ScotlandNational Wildlife Health Center, WisconsinPig Improvement CompanyPoultry Diagnostic and Research Centre of the Venkateshwara Hatcheries Ltd (India)Queensland Department of the Environment and Heritage (Australia)Royal Society for the Protection of BirdsTanzania National ParksTanzanian Wildlife Research InstituteThe Natural History MuseumThe Wildfowl & Wetlands TrustUniversities Federation for Animal WelfareWildlife Conservation SocietyZooDent International

Institute of Zoology Income 2000

(£2,386,229)

Core grant

Research grants and contracts

Other income

Research Grants and

Contracts (£383,093)

Goverment Bodies

Research Councils

European Union

Other organizations

Causes and consequences ofgenetic structure in the greaterhorseshoe bat RhinolophusferrumequinumBats represent nearly one quarter of allmammal species world-wide andcontribute most to Britain’smammalian biodiversity. The majorityof species are highly social, formingcolonies in caves, mines, trees orbuildings. Over the past few decadesmany of the suitable roosts andforaging sites on which bats so criticallydepend have been lost, contributing toa decline of European populations. Yetecologists have afforded surprisinglylittle attention to these highly elusiveanimals. Breeding behaviour inparticular, which can have importantconsequences for the maintenance ofgenetic variation and is therefore ofinterest to conservation biologists, ispoorly understood in most species.

In collaboration with Drs GarethJones and Roger Ransome at BristolUniversity, we used microsatellites tostudy breeding in the endangeredgreater horseshoe bat Rhinolophusferrumequinum which underwent adramatic tenfold decrease in Britainduring the last century. Female greaterhorseshoe bats form summer breedingcolonies, returning annually to thesame roost. Single offspring are born inearly summer. During autumn femalesvisit and mate with territorial males incaves, some of which guard theirterritories for many years. Shortly aftercopulation a plug forms in thereproductive tract of the female,probably preventing further matings.Sperm are then stored throughout

evo

lutio

nary

ecolo

gy

hibernation until fertilization occurs in spring.

To determine paternity, wecompared the paternally derivedgenotypes of five cohorts of offspringborn at a colony in Gloucestershire,south-east England, with those of adultmales sampled throughout thesurrounding area. We found thatbreeding in this species is polygynous;while some males sire few offspringborn at the roost, others are repeatedlysuccessful over successive years.Females breed with males from bothwithin and outside their natal colony,thereby promoting gene flow amongpopulations. Interestingly, a fewsuccessful males are revisited by thesame females in separate years, leadingto full-siblings within the roost.

By combining data on highlysuccessful males with observations ofterritory tenure we have been able toidentify several important maleterritories which can now besafeguarded from future disturbance.Our ongoing work will hopefully shedmore light on this interesting breedingsystem, as additional individuals aresampled.

ROSSITER S J, JONES G, RANSOME R D & BARRATT EM (2000). Parentage, reproductive success and breedingbehaviour in the greater horseshoe bat (Rhinolophusferrumequinum). Proceedings of the Royal Society ofLondon Series B 267: 545-551.

ROSSITER S J, JONES G, RANSOME R D & BARRATT EM (2000). Genetic variation and population structure inthe endangered greater horseshoe bat Rhinolophusferrumequinum. Molecular Ecology 9: 1131-1135.

Quantified interaction websIt would be useful if we could predictwhat happens to communities when a species extinction occurs or when a

new species invades because this wouldallow us to establish bettermanagement plans for the conservationof whole communities. Thesepredictions are difficult because notonly do direct effects on residentspecies occur but also a whole sweep ofindirect effects may result. One suchindirect effect is ‘apparent competition’which occurs when two prey speciesshare a predator. If a new prey speciesinvades the community, the predatorpopulation is able to persist at a higherpopulation density. The higher densityof predators will causegreater consumerpressures and canlead to theextinction ofall preyspeciesexcept theone thatresistshighestpredatorpressure.Thereforeapparentcompetition can beresponsible for additionalspecies exclusions and ultimately theorganization of a community.

One way to evaluate the potential ofapparent competition is the samplingof fully quantified food webs. Foodwebs depict trophic relationships andenergy flows between interactingspecies. They are abstractions and, assuch, often pool data into classes orgroups, blurring species boundaries andtherefore important species

interactions. We have used a modelsystem of aphids and their parasitoids(page 8) that, because of the one-to-onerelationship of host to adult parasitoid,offers a unique opportunity to fullyquantify all species interactions withinthe web.

The potential for apparentcompetition to occur is analysed byoverlap diagrams (below) which showthe extent to which parasitoids areshared and how symmetrical theinteractions are. We found thestrongest potential for apparent

competition via the highestconsumer level of

secondaryparasitoids.

Althoughquantifiedwebs arevaluable forpredictingthe mostimportant

speciesinteractions,

they do notprovide direct

evidence for suchinteractions or how they

affect species distribution and theseneed to be tested in controlled fieldexperiments. This can conveniently becarried out on model assemblages ofinsects but would be impossible formost vertebrate systems of majorconservation concern. Theaccumulation of similarly resolvedwebs from various communities cantell us whether some properties of foodwebs are general. If generalities across

evolutionary ecology 7

Studies on the breedingsystem and social structureof the endangered greaterhorseshoe bat Rhinolophusferrumequinum led to aPhD award.

9

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insect model food webs exist, thiscould lead to significant insights onimportant species interactions for thecomposition and complexity of anynatural community.

MÜLLER C B, ADRIAANSE I C T, BELSHAW R &GODFRAY H C J (1999). The structure of an aphid-parasitoid community. Journal of Animal Ecology 68: 346-370.

Innately vulnerable to extinction?New compilations of information onthe severity of threat faced by theworld’s mammals have made it possiblefor us to undertake a systematic studyon the relationship between basicbiological traits of species and theirvulnerability to extinction. Fromgeneral observations it has beensuggested that relatively large-bodied,slow-reproducing species and those atthe top of food chains would be morevulnerable to extinction. However, this

had not previously been tested, norhad it been possible to evaluate therelative contributions to threat statusfrom the biological traits of speciescompared to the impacts from humanactivities. Our study included over 300species of mammals belonging to theorders Carnivora and Primates wherewe had independent information onthe severity and nature of threats theyface, as well as on their life history,distribution and ecology. Usingmethods that control for phylogeneticrelationships, we showed that species ata high trophic level, with lowpopulation density, slow life historyand, in particular, a small geographicalrange size are all more likely to have ahigh extinction risk, even when theassociations between these variables arecontrolled for. Altogether these traitsexplain c. 50% of the variation inextinction risk between species. Weshow how much of the remainingvariation is directly attributable to theintensity of human-induced processesthat can threaten species, whatevertheir basic biology. For example,several of the Madagascan lemurs are,according to our model, biologicallyrobust against extinction but they havea high threat rate because their habitatis disappearing. In contrast, otherspecies, such as baboons, that appearbiologically vulnerable are apparentlyquite secure because they havesignificant populations in relativelyundisturbed habitats.

PURVIS A, GITTLEMAN J L, COWLISHAW G & MACE G M(2000). Predicting extinction risk in declining species.Proceedings of the Royal Society of London Series B 267:1947-1952.

8 evolutionary ecology

Parasitoids are insects thatfeed and develop mainly onother insects. Aphidsmaintain large communitiesof parasitoids that occupydifferent trophic levels withina web: ‘primary parasitoids’attack the aphid host and‘secondary parasitoids’ attackthe primary or secondaryparasitoid.

Living with the enemy: cheetahs,lions and hyaenas in the SerengetiPredator avoidance has beendocumented for a number of speciesand could potentially play a key role instructuring species communities. This isthe case even when the actual mortalityowing to predation is low, as mortalitymay be low because predator avoidanceis effective. Where competition isintense, then competitor avoidancemay also be important. This year wedocumented avoidance behaviourwithin a large carnivore community forthe first time. Cheetahs in theSerengeti, Tanzania, lose kills and theircubs to two species of large carnivores:lions and spotted hyaenas. Cheetahscan do little to defend themselvesbecause they have small jaws and are ofa much lighter build than these othercarnivores. Cheetahs might thereforebe expected to employ avoidancebehaviours, particularly when they arelikely to be hunting and hence morelikely to attract attention. Lion andhyaena calls were played to cheetahs

through a loudspeaker to examine therisk perceived by cheetahs from thesecarnivores. The results show thatcheetahs actively moved away fromboth lion and hyaena calls. Cheetahswere also much less likely to hunt afterlion and hyaena calls than when nosound was played through theloudspeaker. This reduction in huntingactivity resulted in a lower kill ratesuggesting that the perceived presenceof other carnivores by cheetahs causedthem to suffer reduced food intakerates. Also, while cheetahs moved justas far after lion calls as after hyaenacalls, they spent significantly more timelooking at the loudspeaker and wereless likely to make a kill after lion calls,suggesting that cheetahs perceived lionsto be a greater threat than hyaenas.

Does avoidance have implicationsfor the distribution of cheetahs withinthe Serengeti ecosystem? A previousstudy has shown that whenevercheetahs are found near high densitiesof lions or hyaenas they are less likelyto be hunting and more likely to be

moving than at low densities.Furthermore, both lions and hyaenasare found near high densities ofgazelle, the main prey of cheetahs onthe Serengeti plains, whereas cheetahsare more frequently found near lowdensities of gazelle, while avoidingareas with no gazelles. By avoidingcompetitors, cheetahs might moveaway from areas with high preydensities to areas of lower preydensities, where they can survivebecause of their higher hunting successon small groups or isolated individuals. The mobility of cheetahsand their ability to avoid directcompetition in an ever changinglandscape of competitors and prey maybe the key to their coexistence withlions and hyaenas.

DURANT S M (2000). Predator avoidance, breedingexperience and reproductive success in endangeredcheetahs (Acinonyx jubatus). Animal Behaviour 60:121-130.

DURANT S M (2000). Living with the enemy: pedatoravoidance of hyaenas and lions by cheetahs in theSerengeti. Behavioral Ecology 11: 624-632.

evolutionary ecology 9

0.0

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Distance moved from lion and hyaena playbacks

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Dummy playbacks

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young cheetahs

old cheetahsold cheetahs

young cheetahs

Investigating a recent massmortality of Caspian seals Phoca caspicaThe Caspian seal Phoca caspica isunique to the Caspian Sea and is listedas Vulnerable by the IUCN (WorldConservation Union). Between Apriland August 2000 a mass die-offoccurred affecting many thousands ofindividuals. The die-off, first reportedin Kazakhstan in the northernmost partof the Caspian Sea, spread southwardsto Azerbaijan and Turkmenistan. Ourscientists formed part of aninternational team of researchers(predominantly from the UK and TheNetherlands) investigating the cause ofthe mortality. The investigation wasfunded in Azerbaijan by the WorldBank Ecotoxicology Project via theJapanese Consultant Trust Fund, and in Kazakhstan by the OffshoreKazakhstan International OperatingCompany.

Initial postmortem examinations ofdead seals from Kazakhstan andAzerbaijan did not produce anyconsistent findings, although manyseals were emaciated. However,microscopic examination of tissuesamples from these seals revealed aconsistent pattern of lesions that washighly suggestive of distemper, adisease of terrestrial and aquaticmammals caused by specific viruses ofthe genus Morbillivirus. Tissue sectionswere subsequently examined using animmunohistochemical technique with aprimary monoclonal antibody that isknown to cross-react with canine andphocine distemper viruses, andcetacean morbilliviruses. Morbillivirus

popula

tion

bio

logy

antigen was detected in a range oflesions and tissues in seals exhibitingdistemper-like lesions. Thesemultisystemic tissue lesions associatedwith positive morbillivirus-specificimmunohistochemical tests confirmedthe presence of distemper in Caspianseals during the mortality event.

Morbillivirus nucleic acid was alsopositively identified in tissues from sealcarcasses found on the coasts ofKazakhstan, Azerbaijan andTurkmenistan by carrying out reverse-transcriptase polymerase chain reaction(RT-PCR) with two pairs of ‘universal’morbillivirus primers. This techniquedetects morbillivirus RNA andtranscribes it to DNA, which isamplified to allow subsequentpurification and sequencing. Theresulting sequences matched those ofcanine distemper virus (CDV) and wereclearly distinct from those of othermembers of the genus Morbillivirus.The high degree of similarity of the RT-PCR sequences from these regions ofthe Caspian Sea indicated that theseseals were infected with the same strain of CDV, thus establishing clearspatial and temporal links between theseal mortalities in these widelyseparated regions.

The origin of CDV infection inCaspian seals and its overall effect onthe seal population remain to bedetermined although it is possible thatthe CDV virus may have originatedfrom contact with terrestrial carnivores.Although tests for algal toxins in sealtissues were negative, very high levelsof organochlorine contaminants(particularly DDTs and PCBs) have

been identified in Caspian seals,including some individuals that died inthis mortality event. The possibilitythat high-level exposure to suchpotentially immunosuppressivepollutants may have played asecondary role in the mortality eventmust be considered.

KENNEDY S, KUIKEN T, JEPSON P D, DEAVILLE R,FORSYTH M, BARRETT T, VAN DE BILDT M W G,OSTERHAUS A D M E, EYBATOV T, DUCK C,KYDYRMANOV A, MITROFANOV I & WILSON S (2000).Mass die-off of Caspian seals caused by canine distempervirus. Emerging Infectious Diseases 6 (6): 637-639.

Purging inbreeding depressionresulting from deleteriousmutationsThe phenomenon of inbreedingreducing fitness, known as inbreedingdepression, has been widely observedin most species of plants and animals.Although still in dispute, substantialevidence from studies involving variousfitness traits in diverse organisms hasaccumulated, supporting thehypothesis that most inbreedingdepression is a result of many partiallyrecessive and deleterious alleles that aremaintained by mutation and selectionbalance, and not to a fewoverdominant loci.

Inbreeding increases homozygosityand thus exposes the harmful effects ofthe partially recessive and deleteriousmutations on fitness. This results ininbreeding depression which mayendanger the immediate survival ofsmall populations. At the same time,however, there is a potential forpurging these mutations and theresultant depression in fitness. In recentyears the effectiveness of purging

inbreeding depression by deliberateinbreeding has been explored boththeoretically and empirically. Thevarious empirical studies yieldconflicting results, and the broaddiscrepancy about the effectiveness ofpurging inbreeding depression isunderstandable considering the manyfactors involved. For example, amongthe factors which may influencepurging are: the genetic basis ofinbreeding depression, such asdistributions of selection coefficientsand dominance coefficients ofmutations; rates of inbreeding andgenetic drift; the pattern and strengthof selection; reproductive capacity;organization of the genome.

An important issue in purginginbreeding depression that has notbeen investigated in previoustheoretical studies is the effect ofselection between inbred lines. Becausegenetic variation is progressivelyreduced within lines and increasedbetween lines, particularly for recessivegenes, between-line selection shouldbecome increasingly effective withinbreeding, compared to within-lineselection. Successful highly inbredlines, with a performance at least asgood as the ancestral outbredpopulation, in organisms such as miceand maize are usually developed byinbreeding a large number of lines inparallel and applying between-lineselection so that the poorest lines areeliminated and the best are retained.Therefore one possible strategy formore effectively purging inbreedingdepression is to apply artificialbetween-line selection, in addition to

population biology 11

Bladder epithelial cellsfrom Caspian seals stainedwith H&E (right) or amonoclonal antibodyagainst distemper virus(left) gave results which arecharacteristic of distempervirus infection.

within-line selection and naturalextinction of lines.

Another issue that has received littleattention is the interaction betweeninbreeding, genetic drift and selection.Inbreeding facilitates the selectiveelimination of partially recessivedeleterious mutations, while geneticdrift hinders the purging process andmay drive the deleterious mutations tofixation. Usually inbreeding andgenetic drift cannot be separated andoperate simultaneously at the samestrength (measured by inbreeding andvariance effective sizes) in a smallpopulation. However, under certaincircumstances, such as partialinbreeding in a single population orsubdividing the population into linesand limiting migration, inbreeding canoccur at a higher rate than drift, at leasttemporarily. In a highly subdividedpopulation a deleterious mutation isquickly eliminated from, or fixed in, aline owing to the high rate ofinbreeding and genetic drift withinlines. However, even if the mutation isfixed in a line, it segregates and issubject to selection again aftermigration or crossing among lines.

The effect of populationsubdivision, combined with within-lineand between-line selection and linecrossing, on purging deleteriousmutations of variable effects wasinvestigated. Extensive simulationsindicated that the breeding schemewith equal within- and between-lineselection and crossing alternatively withfull-sib mating is generally the mostefficient for purging deleteriousmutations. However, unless most

deleterious mutations have relativelylarge effects on fitness in species withreproductive ability high enough tocope with the depressed fitness owingto inbreeding, it is not justified toapply a breeding programme aimed atpurging inbreeding depression byinbreeding and selection to apopulation of conservation concern.

WANG J (2000). Effects of population structures andselection strategies on the purging of inbreedingdepression due to deleterious mutations. GeneticalResearch 76: 75-86.

WANG J, HILL W G, CHARLESWORTH D &CHARLESWORTH B (1999). Dynamics of inbreedingdepression due to deleterious mutations in smallpopulations: mutation parameters and inbreeding rate.Genetical Research 74: 165-178.

Sarcoptic mange and spatialorganization of red foxesTheoretical studies have viewedterritory size as a function of the trade-off between different costs and benefitsto territory holders. Among group-living carnivores, two territorialstrategies have been described. Basedon co-operative behaviour,‘expansionists’ may occupy territoriesgreater than the minimum necessary tosupport the basic social unit (abreeding pair) in order that additionalanimals can share the territory. Incontrast, ‘contractionists’ show little orno co-operative behaviour andbreeding individuals defend territoriesof the minimum size necessary toprovide their requirements. Despite theabsence of co-operation, groups mayarise as a result of the rules by whichterritories are configured. The resourcedispersion hypothesis (RDH) assumesthat the basic social unit occupiesterritories that are just large enough to

provide the minimum requirements ofthe breeding pair during limitedresource availability. Outside criticalperiods of limited resource availability,these minimum territories may containmore resources than needed by thebreeding pair alone, and can sustainphilopatric subordinate animals.

In collaboration with Professor S Harris, Bristol University, we haveexamined qualitative predictions arisingfrom the RDH in relation to resourceavailability using red fox as a model.Red foxes have previously beendescribed as exemplifying a‘contractionist’ strategy. The outbreakof sarcoptic mange in an urban red foxpopulation provided an opportunity totest the RDH and the ‘contractionist’strategy because fox density changed

12 population biology

Effects of rate of inbreeding(population size, N) on the meanviability relative to the initialpopulation. One deleteriousmutation was assumed to occur perdiploid genome per generation, withmean homozygous and heterozygouseffects of 0.05 and 0.02 (both inexponential distributions),respectively. The lethal mutationrate is 0.03 and the dominancecoefficient of lethal alleles is 0.02.

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dramatically as a result of mange, anddata from previous intensive ecologicalstudies were available. In contrast tothe predictions of the RDH and the‘contractionist’ strategy, foxes survivingthe mange epidemics increased theirterritories after neighbouring groupshad died out but the increases wereneither accompanied by therelinquishment of other parts of theexisting territories, nor were they aresponse to a decline in foodavailability strategy.

BAKER P J, FUNK S M, HARRIS S & WHITE P C L(2000). Flexible spatial organization of urban foxes, Vulpesvulpes, before and during an outbreak of sarcoptic mange.Animal Behaviour 59: 127-146.

Population dynamics in ungulatesThe relative influence of density-dependent and density-independentprocesses on population dynamics hasbeen debated in ecology for over half acentury. Although both processes arenow known to be potentiallyimportant, it is currently not possibleto make many generalizations. Previousresearch has typically used pattern-orientated approaches to decomposetime-series into contributions fromdensity-dependent and density-independent processes. An alternativeprocess-orientated approach is toestimate the relative roles of eachprocess on inter-annual variation invital rates. We compared pattern-orientated analyses of time-series withprocess-orientated analyses of a vitalrate in three contrasting ungulatespecies. Analyses of time-series andvital rates gave different results. Analyses of fecundity rates in Soay

sheep (right), saiga antelope and reddeer identified that both density andwinter temperature were important inone or more age class. In each species,high density and cold wintersdepressed fecundity. In contrast,analyses of the time-series for eachspecies did not identify significanteffects of density on populationfluctuation. The approach of analysingrelationships between vital rates, density and climatic variablesmay detect important processesinfluencing population dynamics thattime-series methodologies mayoverlook. However, an approach toanalysing population dynamics datathat uses both process-orientated andpattern-orientated methodologieswould be best.

COULSON T, MILNER-GULLAND E J & CLUTTON-BROCKT (2000). The relative roles of density and climaticvariation on population dynamics and fecundity rates inthree contrasting ungulate species. Proceedings of theRoyal Society of London Series B 267: 1771-1779.

Ecological basis of extinction riskA high proportion of mammal andbird species is threatened withextinction. In the last decade or so,huge efforts have been made byinternational conservation agencies todescribe the geographic distribution ofbiodiversity and extinction risk in thesetaxa. Now we can be reasonably sure ofwhich species are threatened withextinction and which regions haveunusually high concentrations ofthreatened species. However, while thedescription of biological diversity andextinction patterns among mammaland bird species is becoming morecomplete and precise, we have littleknowledge of the evolutionaryprocesses and ecological mechanismsthat underlie these patterns. Until veryrecently we could not answer suchdeceptively simple questions as whysome species are threatened whileothers appear secure, and why somefamilies contain large numbers ofspecies while others have only a few.

Understanding the evolutionaryprocesses and ecological mechanismsthat underlie extinction is fundamentalto conservation biology. Previously,using statistical and phylogeneticapproaches, we established that not allbird families are equally vulnerable toextinction. For example, parrots andalbatrosses are unusually vulnerablewhereas woodpeckers and cuckoos areunusually secure. However, the reasonsfor these differences are poorlyunderstood. This may be, in part,because different bird taxa arethreatened by different mechanisms.Among 1012 threatened bird species,

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habitat loss, human persecution andintroduced predators were by far themost common threats. Habitat loss wascited as a source of risk for over 70% ofthreatened species, while humanpersecution and/or introducedpredators were cited in 35% of cases.Furthermore, twice as many species(54%) were classified as being

threatened by either habitat loss aloneor by human persecution/introducedpredators alone, than being threatenedby both sources together (27%).

Theoretically, sources of extinctionrisk that perturb the balance betweenfecundity and longevity, such as humanpersecution and introduced predators,should be particularly hazardous fortaxa that have slow rates of populationgrowth. In contrast, sources ofextinction risk that reduce nicheavailability, such as habitat loss, shouldrepresent a particular threat to taxa thatare ecologically specialized. We testedthese predictions using a phylogeneticcomparative method and a database on95 families of birds. Our analysessupport the predictions that differentlineages are threatened by differentmechanisms of extinction, and thatdifferent ecological factors predispose

taxa to different sources of extinctionrisk. As predicted, extinction risk frompersecution and introduced predators isassociated with large body size andlong generation time but is notassociated with degree of specialization,whereas extinction risk incurredthrough habitat loss is associated withhabitat specialization and small bodysize but not with generation time.

Thus, our results corroborate theprediction that there are multipleroutes to extinction among birds. Oneroute is for large-bodied, slow-breedingspecies to become threatened when anexternal factor, such as humanpersecution or introduced predators,disrupts the delicate balance betweenfecundity and mortality in birdpopulations. In our analysis, thisapplies to families such as the kiwis,cassowaries, megapodes, penguins andalbatrosses. A second route is forecologically specialized species tobecome threatened by habitat loss.Such families include the trogons,scrub-birds and logrunners. A smallnumber of families are prone to bothsources of extinction risk. Theseinclude the parrots, rails, pheasants,pigeons, cranes and white-eyes. It isthis last set of families that wepreviously identified as beingsignificantly over-prone to extinction.

Our results demonstrate theimportance of considering separatelythe multiple mechanisms that underliecontemporary patterns of extinction.

OWENS I P F & BENNETT P M (2000). Ecological basis ofextinction risk in birds: habitat loss versus humanpersecution and introduced predators. Proceedings of theNational Academy of Sciences USA 97: 12144-12148.

origins and maintenance of biodiversity 15

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Phylogenetic misfortuneEvolutionary trees are hierarchical instructure. An inevitable consequence ofthis is that even if species extinctionrates are quite high, if they are more-or-less randomly distributed acrossspecies, then whole higher taxa arenearly always likely to persist simplybecause some constituent taxa do. Thismeans that surprising amounts ofevolutionary history (measured as thecomplete branch length of aphylogeny) can persist even if a largeproportion of species dies out. In aninfluential paper, Nee and May (1997)illustrated the potential significance ofthis effect by simulating theconsequences of species extinctions inhypothetical phylogenies. For example,in one very large hypotheticalphylogeny they showed that just 5% ofspecies could capture 81% of theevolutionary history represented in thephylogeny. However, there are variousreasons to doubt their assumption thatspecies extinctions will in fact berandomly distributed. Extinct andthreatened species are more likely tobe clumped in their distributionon a phylogeny because theyshare traits that increasevulnerability to extinction andbecause related taxa are oftenlocated within the same broadgeographical or habitat types wherehuman-induced threats areconcentrated. We were able to test thisdirectly using recently developedcomplete phylogenies for mammaliancarnivores and primates. We estimatedhow much evolutionary history wouldbe lost if all the species currently listed

as being threatened with extinction were to actually go extinct, and wecompared this estimate to the amountpredicted by the random model. Ourresults show that threatened species arefar from randomly distributed amongtaxa and among phylogenetic clades.As a consequence of this, the amountof evolutionary history that stands tobe lost as a result of the current speciesextinction spasm is much higher thanexpected – for primates we expectabout an extra 10 million years ofevolution to be lost per genuscompared to random expectation. Pastestimates of the effects of speciesextinctions on overall biodiversity losshave therefore given results thatwere too optimistic.

PURVIS A, AGAPOW P-M,GITTLEMAN J L & MACE G M(2000). Non-random extinctionand the loss of evolutionaryhistory. Science 288:328-330.

Emerging infectious diseases ofwildlife: threats to biodiversityconservation and human healthEmerging infectious diseases (EIDs) ofhumans have been a focus of publichealth interest for the past two decades.Recently, we have shown how EIDscan be a significant threat to theconservation of animal biodiversity.Increases in the number of reports ofepizootic wildlife EIDs (e.g. marinemammal morbillivirus disease,kangaroo blindness, amphibianranavirus disease, herpesvirus-associatedmass mortalities of pilchards) suggestthat these are a current and seriousglobal concern. Some of these diseases,such as cutaneous chytridiomycosis ofamphibians, have been implicated inthe declines, and even extinctions, ofwhole populations. This can happeneither through the direct (e.g. infectioncausing death) or the indirect, or‘knock-on’, (e.g. infection causing lossof prey species) effects of disease.

Although many of these diseaseoutbreaks are seemingly ‘natural’occurrences, we have shown thatanthropogenic (human-mediated)ecological changes have driven theemergence of the majority of recentwildlife EIDs, including those inotherwise pristine areas. These changesinclude the ‘spill-over’ of pathogensfrom domestic animals to wildlife,human encroachment into wildlifehabitat, deliberate or accidentaltranslocation of pathogens (with orwithout their hosts) into ‘naïve’ areasor populations (a process we havetermed ‘pathogen pollution’), and themanagement of wildlife for agriculture,

16 origins and maintenance of biodiversity

Translocation

• Encroachment• Introduction• “Spill-over” and

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• Biomedical manipulation

The relationships of emerginginfectious diseases in humans,domestic animals and wildlife.Arrows indicate key factorswhich drive disease emergence.

Reprinted with permission from Daszak, P.,Cunningham, A.A. & Hyatt, A.D. (2000)Emerging Infectious Diseases of Wildlife-Threats to Biodiversity and Human Health.Science. 287: 443-449. Copyright 2000American Association for the Advancementof Science.

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hunting and even for conservationreasons. Further analyses demonstratethat these anthropogenic changes towildlife ecology directly affect theemergence of disease in human beings,which can lead to significant morbidityand mortality (e.g. the emergence ofNipah virus disease in SE Asia, WestNile virus disease in the USA).Furthermore, it appears that pathogenpollution could be as important andfar-reaching a threat to biodiversityconservation as other major forms ofanthropogenic impacts, such as habitatloss or chemical pollution. Our workdemonstrates a need for increasedvigilance and research into the impactof anthropogenic change on theecology of disease in wildlife, domesticanimals and human beings.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Emerging infectious diseases of wildlife: global threats tobiodiversity and human health. Science 287: 443-449.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Conservation conundrum - Response. Science 288: 2320.

Hybridization between red deerCervus elaphus and introducedJapanese sika deer Cervus nipponin Argyll, ScotlandHuman introductions of exotic speciesfrequently have detrimental effects onnative ecosystems. Typically this occursvia competition for resources,predation on naïve species or throughhybridization with related native taxa.A current example of hybridization inthe UK is that of red deer Cervuselaphus and introduced Japanese sikadeer Cervus nippon. This hybridizationis progressing rapidly and has thepotential to have a serious impact both

in biological and economic terms onBritain’s largest remaining landmammal.

Sika deer were first brought to theBritish Isles in the 1860s and were bredand distributed to parks throughoutIreland, England and Scotland. Later,sika deer were either deliberatelyreleased or escaped from deer parks,establishing feral populations in severalplaces around the British Isles. InScotland, around ten introductionswere made between the 1860s and1930s and the descendants of escapeesfrom these introductions now occuracross 50% of the available deer habitatin Scotland. Phenotypic hybrids havebeen reported in Scotland from the1950s onwards where the two specieshave come into contact.

Following genetic studies ofhybridization between red and sikadeer in Scotland carried out at theInstitute of Cell, Animal andPopulation Biology, The University ofEdinburgh, a further analysis of thesedata is under way at the Institute ofZoology. The data are from anintensive survey in Argyll, includingc. 700 deer sampled during the1996–1997 annual cull which werescreened for 25 species diagnosticmicrosatellite markers and onemitochondrial marker. This newanalysis confirms the strong assortativemating and rarity of F1 hybridsbetween red and sika deer which wasobserved previously. The F1 hybrids aregenerated at a frequency of only1/500–1/1000 matings, however, thesehybrids go on to backcross successfullyinto both parental taxa. This leads to

substantial introgression between thetaxa and 62% of sika deer and 33% ofred deer had some hybrid ancestry.This new analysis suggests that in sikadeer selection is acting to removeintrogressed alleles. This may bebecause sika hinds with introgressedalleles tend not to breed in their firstyear whereas pure sika almost allbecome pregnant in their first year. If this selection is strong enough toprevent introgressed alleles fromaccumulating in the long term, it mightmean that red and sika deerphenotypes will be maintained, despiteongoing hybridization, instead ofcollapsing into a continuousdistribution of hybrid forms, asobserved in County Wicklow, Ireland.

A new project at the Institute alsosupports the view that distinctphenotypes of red and sika deer can bemaintained despite ongoinghybridization. Red and sika deer froman ancient natural hybrid zone ineastern Siberia were analysed using thesame genetic techniques. Preliminaryresults show that most deer have somehybrid ancestry in the recent past butthat they can all be classified as red orsika on the basis of phenotype.

Finally, recent analysis of new datafrom microsatellite screening showsthat the introduced sika deer originatedfrom the area around Nagasaki,Kyushu, Japan: until now, the originsof these deer had been obscure becauseof poor records of the introductions.

GOODMAN S J, BARTON NH, SWANSON G M,ABERNETHY K & PEMBERTON J M (1999). Introgressionthrough rare hybridisation: a genetic study of a hybrid zonebetween red and sika deer (genus Cervus) in Argyll,Scotland. Genetics 152: 355-371.

origins and maintenance of biodiversity 17

Sika stag (foreground) andred deer stag and red/sikahybrid hind (background) on a deer park in Ireland.Sika deer of both sexes are about half the size ofScottish red deer.

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Variation in boar spermatozoa fertilityafter freezing was investigated andgenetic markers associated with thisvariation were identified.

Our future in the freezer: a geneticbasis for boar sperm survivalfollowing cryopreservationMany threatened wild populations aresmall in number and fragmented indistribution, and captive-bredpopulations are also inevitably limitedin size. Genetic variation is lost rapidlyin small populations, leading to lessviable inbred individuals. A classicexample of inbreeding causing reducedreproductive fitness is the Floridapanther Felis concolor coryi in which aloss of genetic diversity has led toabnormal testis development andresulting infertility.

One possible solution to thisproblem is genetic resource banking,whereby sperm and other tissues fromthreatened species are frozen andstored for use in controlled breedingprogrammes. By cryopreserving thespermatozoa of ‘genetically valuable’males we could maintain maximumgenetic diversity in an endangeredpopulation. Of course it would benaïve to suggest that gametepreservation alone would end species extinction, however, genebanking has a valuable role to playwhen used in conjunction with otherconservation strategies.

The concept of preserving genesfrom threatened species is an attractiveoption but although semencryopreservation has been appliedsuccessfully in a few species, extensivevariation in post-thaw semen qualityexists between individuals. Our recentstudies, using pig as a model species,have confirmed that consistent inter-individual variation in sperm

‘freezability’ exists and is inherited.Three groups of boars were identifiedon the basis of a consistent response tosemen cryopreservation (poor, averageand good freezers). Semen viability wasdetermined using % motility, computerassisted semen analysis (CASA) ofmotility parameters, plasma membraneintegrity (SYBR-14 +ve by flowcytometry) and acrosome integrity(fluorescein-labelled peanut agglutinin+ve stained smears).

DNA from boars classified as goodand poor freezers was analysed usingthe amplified restriction fragmentlength polymorphism (AFLP)technique to identify molecularmarkers linked to genes controlling theability of sperm to freeze successfully.The AFLP technique is based on theselective PCR amplification offragments of genomic DNA and allowsus to screen the genome without priorknowledge of nucleotide sequence. TheDNA fragments are visualized on asequencing gel and assessed rather likea DNA ‘fingerprint’. Clear differencesin the DNA profiles of individual boarswere observed and these were related tothe variation in semen freezability,confirming that freezability isinherited. Sixteen candidate molecularmarkers linked to genes influencingsemen cryopreservation were identified.

Important practical applications ofthis research extend to bothdomesticated and endangered species.By identifying markers for genes whichmay influence semen freezability, wehave the potential to influence animalproduction systems. Current methodsof sperm preservation impose

significant costs on UK agriculturethrough wastage of semen held atambient temperatures and the loss ofgenetic information from importantboars. The identification of geneticmarkers linked to semen freezabilitywill have a direct impact on methodsof semen preservation in the artificialinsemination (AI) industry andpromote cryopreservation as a viableoption for porcine AI. Rigorousvalidation of these molecular markersas a predictive measure of semenfreezability will provide an opportunityto improve the quality of cryopreservedsemen through selective breedingprogrammes, leading to improvedefficiency for UK agriculture.

The identification of genetic markerslinked to ‘freezability’ genes will allowus to promote genome banking as aviable conservation tool. Future workmust aim to identify what aspects ofsperm function are controlled by thefreezability genes and developprotocols to minimize the effects offreezing on these cellular components.The development of successfulcryopreservation protocols wouldensure the maintenance of viablestored spermatozoa, protecting bothgenetic and species diversity for future generations.

THURSTON L M (2000). An investigation into sources ofvariation and the genetic basis of boar sperm survivalfollowing cryopreservation. PhD Thesis, University ofLondon.

THURSTON LM, SIGGINS K, MILEHAM A, WATSON P F &HOLT W V (2000). Identification of amplified restrictionfragment length polymorphism (AFLP) markers linked togenes controlling boar sperm viability followingcryopreservation. Journal of Reproduction and FertilityAbstract Series 25.

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conservation biology and management 19

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Veterinary monitoring of scimitar-horned oryx Oryx dammahreintroduced to TunisiaThe reintroduction of a mammal intopart of its former range is notstraightforward. In order to succeed,the reason for the disappearance of thespecies from the area must have beenidentified and removed or dealt with,and sufficient habitat for the animals’requirements must be available. Diseaseis another important factor. Animalsraised in captivity may carry pathogensthat were natural in their former rangebut may also carry exotic pathogens,contracted from domestic animals orother exotics, especially closely relatedspecies. The stress of transportationmay exacerbate infections or lowerresistance and the mixing of animalsfrom different collections may exposesome to pathogens to which they areunaccustomed. Finally, on arrival at thereintroduction site, the animals mayencounter novel pathogens to whichthey have no immunity.

The scimitar-horned oryx Oryxdammah was formerly widespread inthe arid grasslands of the Sahel but isnow extinct in the wild in most, if notall, North African countries. Thecaptive population has increaseddramatically over the last 30 years andthere are many animals available forreintroduction. In 1985 ten oryx werereturned to the Bou Hedma NationalPark in central Tunisia. This populationhas grown to c. 100 animals but isinbred owing to the relatedness of thefounders. In March 1999 two male and11 female scimitar-horned oryx weresent from European institutions to

southern Tunisia for reintroduction totwo National parks, and a further malewas sent to Bou Hedma to introduce afresh genetic line.

Our veterinary involvement with theoryx reintroduction included: (1) co-ordination of pre-export health checksperformed by the veterinarians at thezoos providing animals, (2) monitoringthe oryx during transportation and the30 day post-import quarantine period,and carrying out treatment andpreventative health measures, and (3)monitoring health after release andassisting with movement of oryxbetween release sites. All 14 oryx weretransported to Tunisia without incidentand were quarantined at the Sidi TouiNational Park. After 1 month, severalanimals were immobilized; one malefor transport to the Bou Hedma Park,one male and two females for transportto start a third group at Oued Dekoukreserve, and two females for fittingradio-collars. At each opportunity theanimals were re-examined and all werein good health. Further monitoring has been continued by a zoologist andPark staff.

A follow-up visit was made inNovember 2000. The majority of thereleased animals, plus six offspringborn since the reintroduction, weresighted during visits to the Bou Hedmaand Sidi Toui National Parks. Trainingworkshops on immobilization andhealth checks were held for TunisianNational Park staff. At a meeting with

the Tunisian Direction Générale deForêts, Park officials and vets from theMinistry of Agriculture and VeterinaryFaculty considered the managementand monitoring of disease in wildlife.

FLACH E J, D’ALTERIO G-L, ZAHZAH K, MOLCANOVA R,WAKEFIELD S, BAROSSI D, EULENBERGER K, KOPCOKM, OLLIVET F, PETIT T, VAHALA J & FRÖLICH K (2000).Veterinary monitoring of captive-bred scimitar-horned oryx(Oryx dammah) prior to reintroduction in Tunisia.Proceedings of the 3rd Scientific Meeting of the EuropeanAssociation of Zoo and Wildlife Veterinarians (Paris). 31May - 4 June 2000: 91-97.

Parapoxvirus disease and mortalityin red squirrels Sciurus vulgarisIn our studies to explain the effects ofinfectious disease on the populationsize of endangered species we haveused red squirrel parapoxvirus (RSPPV)and squirrels as a model. Theepidemiology of this infection was ofinterest because there is good evidencethat parapoxvirus disease causessignificant mortality in red squirrelsSciurus vulgaris, a species which isundergoing a marked decline on theUK mainland. A serological survey wascarried out on red squirrel and greysquirrel Sciurus carolinensis populationsusing an enzyme-linkedimmunoabsorbant assay (ELISA). The results showed that 61% of greysquirrels, an introduced species, hadantibody levels consistent withexposure to RSPPV, compared with2.9% of red squirrels. This findingrepresents evidence of endemicinfection of low pathogenicity in greysquirrels and suggests that they are areservoir host of the virus. This couldexplain why outbreaks of parapoxvirusdisease continue to occur in small,isolated populations of red squirrel.

20 conservation biology and management

The survey results suggested arelationship between the geographicdistribution of grey squirrels withantibody to RSPPV and locations where parapoxvirus disease is eitherknown to, or believed to, haveoccurred. At sites where parapoxvirusdisease, or disease of similardescription, has never been known tooccur, grey squirrels were seronegative.The transmission of infectious agentsfrom an abundant reservoir host to a smaller population of another species is now a well recognized threat toendangered species, a good examplebeing the occurrence of rabies inAfrican wild dogs Lycaon pictus, whichwas transmitted from a reservoir indomestic dogs. Where such threats areshown to be attributable to humanactivities, the case for intervention toprotect the endangered species deserves consideration. Vaccination of redsquirrels against parapoxvirus is now under investigation.

SAINSBURY A W, NETTLETON P, GILRAY J & GURNELL J(2000). Grey squirrels have high seroprevalence to aparapoxvirus associated with deaths in red squirrels.Animal Conservation 3: 229-233.

Monitoring reproduction in the wildmongoose lemur Eulemur mongozof MadagascarThe lemurs of Madagascar make up asubstantial proportion of themammalian diversity on the island and,

together with most of thenative fauna, are

threatened with extinctionprimarily owing to habitat

alteration and destruction. Zoo, fieldand laboratory scientists have beencollaborating for a number of years inorder to gain more insight into thebiology of one particular species, themongoose lemur Eulemur mongoz,classified as Endangered by IUCN. A study of mongoose lemur socio-ecology carried out in 1994/95provided basic knowledge of E. mongozin the wild and, in order to improvethe immediate success of captive-breeding, a detailed chemical analysisof the diet was carried out. Geneticvariablity in wild and captivepopulations is currently being assessedand a species management group,which includes researchers from zoosand universities, was formed last year.

As part of this collaborative effortour reproductive biologists havestudied female reproductive traits inone of the first attempts to monitorreproduction in a group of wildprimates using non-invasive methods.In 1995 sexual behaviour wasmonitored in two wild family groupsand faecal samples were collected fromadult females and their sub-adultdaughters over a 20 week period.Samples were stored in ethanol andsubsequently analysed for progestagenand oestrogen content. These data werecompared with results from samplescollected from two captive animals in the UK.

Ethanol storage was a successfulmethod of preservation for samples

collected in the field. The hormoneswere extracted into the ethanol duringthe storage period thereby reducing thelaboratory processing required.Furthermore, although faecal samplescontained variable amounts ofindigestible fibrous matter and seeds, aswell as stones, these did not interferewith the hormone assays. Our resultsshowed that most females conceivedduring the first oestrus of the breedingseason and conception was precededby a pseudooestrus, which probably didnot result in ovulation. Pseudooestrusand oestrus were identified byinvestigating the oestrogen:progestagenratio on each day. Pregnancy wasreliably diagnosed c. 47 days afterconception when progestagen andoestrogen excretion increased abovebreeding season levels. Gestation wasfurther characterized by highprogestagen concentrations and adecline in oestrogen excretion70–80 days after conception. A sub-adult daughter in the wild conceivedwhile still a member of her natal groupand aborted at 70–80 days ofpregnancy, when progestagens declinedbut oestrogens remained high.

Our results will make a significantcontribution to the captive-breedingand conservation of E. mongoz and itsrelatives, and have furthered ourunderstanding of their reproductivephysiology.

CURTIS D J, ZARAMODY A, GREEN D I & PICKARD A R(2000). Non-invasive monitoring of reproductive status inwild Mongoose lemurs (Eulemur mongoz). ReproductionFertility and Development 12: 21-29.

conservation biology and management 21

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An essential part of ZSL’s work isfacilitating the communication ofinformation between professionalzoologists, researchers and the generalpublic. We achieve this through avaried programme of meetings, whichis open to the public and members ofstaff, and the publication of scientificjournals and books.

The Journal of Zoology, ZSL’s pre-eminent international journal dedicatedto academic zoology, continues toattract contributions from topresearchers. During the year 160original peer-reviewed articles werepublished in 12 monthly parts ofVolumes 250–252, providingcomprehensive coverage of the latestresearch and developments in zoology.

ZSL’s quarterly journal, AnimalConservation, provides an importantforum for the rapid publication ofrigorous empirical or theoretical studiesrelating to species and populationbiology. The journal continues to bringtogether exciting new research andideas from evolutionary biology andecology that contribute to the scientificbasis of conservation biology.

The Conservation Biology bookseries, published in association withCambridge University Press, includesinternationally significant advances inthe science that underpins conservationbiology. Titles are based either onsymposia held at ZSL or on othertopics which meet these aims. Threetitles were published during the year:Behaviour and conservation, edited by L Morris Gosling and William JSutherland, Priorities for the conservationof mammalian diversity, edited by

Abigail Entwistle and Nigel Dunstone,and Genetics, demography and viability offragmented populations, edited by AndrewG Young and Geoffrey M Clarke.

Volume 37 of the International ZooYearbook was published and contains 43articles, 32 of which are on theconservation of Psittacines. NigelCollar, BirdLife International, gives anauthoritative overview of the 90 speciesof parrots which are threatened withextinction, while others provideinformation on breeding, husbandry,conservation, health and captivemanagement of these fascinating andbeautiful birds. Articles in Section 2,The Developing Zoo World, rangefrom the husbandry and breeding ofthe Kerry spotted slug to hand-rearingand reintroduction of a Sumatranorang-utan. The Guest Essay by SallyWalker addresses the continuingestablishment of regional or nationalnetworks of the Conservation BreedingSpecialist Group.

After five years in preparation, thisyear also saw the publication byChicago University Press of PrimateConservation Biology by Guy Cowlishaw(Institute of Zoology) and RobinDunbar (University of Liverpool). Thiswork is both a review and synthesis ofcurrent theory and practice in primateconservation. Beginning with anoverview of the diversity and biologyof primates, the book goes on toaddress extinction processes in primatesand the key forces that currently drivethem, namely habitat disturbance andhunting. The last part of the bookfocuses on possible conservationsolutions to these problems, including

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protected areas, sustainable tourism,and captive-breeding and reintroductions.

The first ZSL Symposium of the newmillennium Reproduction and IntegratedConservation Science, was held on 9th

and 10th November. The objectiveswere to critically evaluate the role ofreproductive sciences in conservationand to suggest priorities for the futureapplication of reproductive research inthis field. The meeting was organizedby Bill Holt and Amanda Pickard(Institute of Zoology), David Wildt(Smithsonian Institution, USA) andJohn Rodger (Marsupial ConservationResearch Center, Australia). There was alarge international attendance with over160 delegates from the Americas,Antipodes, Africa, Asia and Europe.The papers will be collated in an editedbook to be published in theZSL/Cambridge University Press serieson conservation biology.

At our regular Scientific Meetings,three speakers provide an overview ofimportant research within a particularfield. The eight Meetings held duringthe year covered diverse subjects, suchas Can parks protect Africa’s predators?,The conservation of animal diversity inriver basins and Cycles in animalpopulations.

Tuesday Talks are aimed at a generalaudience. Nine talks were held during the year covering a wide range oftopics, including Gorilla tactics,Mudflats, misconceptions and themillennium, and From concrete to warblers- the story of the Wetland Centre. TheLiving Wild, a collection of stunningimages presented by internationally

recognized wildlife photographer Art Wolfe, was particularly popular.

The Science and Conservationseminars held by the Institute ofZoology included talks by invitedspeakers on subjects relevant to ourresearch, for example, Biology after thehuman genome, Snake venom proteins: anew male contraceptive and Life history andextinction risk in bats.

The 2000 Sir Stamford RafflesLecture, How the brain generatesconsciousness, was presented by ProfessorSusan Greenfield, Director of the RoyalInstitution of Great Britain. The event was sponsored by the SingaporeTourism Board and Singapore Airlines;we are most grateful for theircontinuing support of this event.

The Zoological Record, published jointlywith BIOSIS, is the oldest continuousinformation service for the life sciences. As a record of all aspects ofzoological research, it is considered theforemost publication in its field. Thecontinued generous support of variousinstitutions, principally the BritishLibrary Document Supply Centre atBoston Spa and the Natural HistoryMuseum, London, in providing accessto material for indexing is greatlyacknowledged.

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Our PhD students continue to be oneof the Institute’s greatest assets. Theirindividual and scientific backgrounds,sources of funding support and thesissubjects reflect the range of researchand collaboration typical across the restof the Institute. Students regularlypresent their work through informaldiscussions, at the Institute’s annualStudent Conference and outside theInstitute at research meetings.

Eighteen PhD students wereregistered at the Institute at the end of2000. Gina Caplan, a BBSRC CASEstudent, joined us in October toinvestigate the potential use of the fieldvole Microtus agretis as a novelenvironmental biomarker. In a projectcombining the bioengineering skills ofstaff at the Silsoe Research Institutewith the Institute’s expertise in non-invasive hormone monitoring, she willdevelop techniques for the automatedmonitoring of reproductive status infield voles under both laboratory andfield conditions.

Three NERC-funded studentsstarted in 2000. Julie Anderson willstudy individual dispersal decisions andemergent metapopulation dynamics ofthe Angolan black and white colobusmonkey in East Africa. Sonya Gowtage-Sequeira will investigate theimportance of jackals and domesticdogs in the transmission of infectiouscanine disease to endangered carnivoresin southern Africa, and Fredi Devaswill study mechanisms which mediatethe impacts of both predators andcompetitors on foraging success in asocial forager, the desert baboon.

Four students, Stephen Casey, Jim

Groombridge, Stephen Rossiter andLisa Thurston, were successful inobtaining their doctorates during theyear. The key results from StephenRossiter and Lisa’s research are featuredelsewhere in the report.

Stephen Casey received his PhD forresearch on the evolutionary andpopulation genetics of seahorsesHippocampus spp., funded by NERC.Seahorses are threatened by loss ofhabitat, trade and by trawls, and theimpact of this exploitation has beendifficult to determine; with few variableexternal characters which can be scored,species identification has been difficult.A taxonomic revision of Vietnamesespecies was completed andphylogenetic analyses of species world-wide were carried out. Populationstudies of the heavily fished H. comes inthe Philippines showed low levels ofgenetic differentiation over tens ofkilometres, indicating high levels ofgene flow and suggesting that marineprotected areas may be effective atpromoting the recovery of adjacentsites.

Jim Groombridge, funded by theMauritius Wildlife Foundation andDurrell Wildlife Conservation Trust,carried out molecular genetic studieson three critically endangered birdspecies endemic to Mauritius(Mauritius kestrel Falco punctatus, pinkpigeon Nesoenas mayeri, echo parakeetPsittacula echo). His research on theMauritius kestrel showed that recoveryof the population from an extremebottleneck (a single wild breeding pairin 1974 to over 250 wild pairs)occurred despite the erosion of

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previously high genetic diversity.Therefore although half of allendangered bird species are islandendemics, some can make remarkablerecoveries. This collaborative study willhelp to promote the conservationpriority of other critically endangeredisland species. Jim is now Project Co-ordinator on the Maui Forest BirdRecovery Project in Hawaii.

Stephen Rossiter, funded by aNERC CASE award, investigated thebreeding system and social structure ofthe greater horseshoe bat Rhinolophusferrumequinum in the UK. Patterns ofgenetic exchange and differentiationwere investigated together with theconsequences of population structureon individual fitness and the evolutionof kin-biased behaviour at colony level.Stephen is now at Queen Mary andWestfield College, London.

Lisa Thurston, a CASE studentfunded by BBSRC, studied sources ofvariation in boar spermatozoa fertilityfollowing cryopreservation. Her resultsprovided evidence of a genetic basis forthe individual variation in post-thawsemen quality, and AFLP technologywas used to identify molecular markerslinked to genes influencing thisvariation. Ultimately this work couldlead to the identification of specificgenes which are crucial to aspects ofsperm function. Lisa is now at theRoyal Veterinary College.

Frank Clarke was presented with the Thomas Henry Huxley Award fororiginal work submitted as a doctoralthesis, a highly competetive andprestigious award with contenders from

all over the UK. Frank is a graduate ofGlasgow University where he wasPresident of the Zoological Society,Vice-Chair of the Exploration Societyand team leader of expeditions toNorth Cyprus and Trinidad. His PhDresearch was on the hormonal,behavioural and genetic correlates ofdominance and breeding status incaptive colonies of naked mole-rats.After completing his PhD Frankworked at the University of Pretoria,South Africa, and is now at TheUniversity of Aberdeen.

Our second Student Conference, opento Institute staff, external supervisorsand collaborators, was held on 28September in the ZSL EducationDepartment. Research Councils stressthe importance of transferable skillsand training in the career developmentof students. Our aim is to providestudents with excellent experience inresearch and help them gain skills tomake informed choices about theirfuture careers. One crucial skill is theability to prepare and presentinformation in a way that inspires andinforms those receiving it, and byasking students to give yearly talkswithin the conference setting weprovide an opportunity for them to

develop these skills, and to learn fromand support each other. The informalnature of the conference is ideal forthose who are presenting work for thefirst time.

The presentations this year were allexcellent and the standard was evenhigher than last year, reinforcing thefact that this is an opportunity forstudents to progressively develop theirpresentation skills. SaffronTownsend,Lisa Thurston and Octavio Paulo gaveparticularly well structured andpolished presentations on sheepdomestication, boar spermcryopreservation and phylogeographyof the Iberian lizard, respectively.Projects currently range from studies ofbumble bee foraging ecology inLondon, to human-bear interactions inSouth America, MHC polymorphismand fitness in the great tit, leking intopi and analysis of giraffe subspeciesdesignations.

In October the Institute held itsAnnual Research Conference which isalso open to all staff and students andprovides another forum for exchange ofideas and discussion.

In addition to supporting PhDstudents, the Institute provides valuableresources and skills for training andcollaboration with many researchers inthe laboratory and the field. In any oneyear we host a large number of visitors,including undergraduate and MScstudents, visiting postdoctoralresearchers and others. This year wasno exception, with undergraduatestudents from Queen Mary andWestfield College and the University of

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Frank Clarke (below right)received the Thomas HenryHuxley Award for his PhDresearch on naked mole-ratsfrom Sir Martin Holdgate (left)and Mr Brian Marsh (centre).

East London, MSc students fromUniversity College London, Berne andMontpelier, and postdoctoralresearchers from the Royal VeterinaryCollege, Paris and the USA. Forexample, Janice Long (MRes Studies,Environmental Science, UCL) workedwith Georgina Mace for 3 months on‘Global conservation priorities formammals and birds — comparingdiversity and threat among regions’,and Conrad Scofield (MResStudies,York University) carried out hisresearch project with Chris Carboneexamining predator—prey sizerelationships in snakes. In the field,John Shemkunde, a Tanzanian studentwith a wildlife management diplomafrom Mweka College, was seconded tothe cheetah project from TanzanianNational Parks. As part of his Mastersdegree (University of Wales) he willconduct a leafleting campaign to solicitphotographs from visitors to the Parksto help estimate numbers of cheetahsand cub survival across the northerncircuit in Tanzania. If successful, thisscheme may be incorporated withinNational Parks as part of a carnivore-monitoring plan, enabling us toanticipate and prevent problems tocheetah populations across Tanzania.

The Master of Science Course in WildAnimal Health (MSc WAH), runjointly with the Royal VeterinaryCollege (RVC), continues to beoversubscribed and a maximumcompliment of 15 students started the2000/2001 course in October. Thishighly successful course is now in itsseventh year and the current group of

students maintains the internationalmix, with five students from Spain andothers from Egypt and Japan. There arenow 70 course graduates, from 31countries on six continents. Weregularly hear news from the graduatesas they develop their careers and wecontinue to advise them as and whennecessary. All veterinarians on the1999/2000 course passed and BeckiLawson (left) won the prize for the beststudent. Some graduates have gone onto key posts in zoo and wildlifemedicine, for example, Dr MaudLafortune who is now a veterinarian atCalgary Zoo.

The Quality Assurance Agency(QAA) carried out an assessment of thestandard of teaching in January 2000,and, like the other courses run by theRVC, the MSc WAH was awarded ascore of 24/24 (100%). The QAAreport noted the high level ofenthusiasm and satisfaction expressedby the veterinarians on the course andthat the pass rates were excellent.

Institute staff also teach on the ‘Sex, genes and evolution’ course atUniversity College London, and onreproductive biology at King’s CollegeLondon, St George’s Medical Schooland the RVC.

The Centre for Ecology and Evolution(CEE) was set up in 1994 to create acentre of excellence for research andteaching in the fields of ecology andevolution and is now a partnershipbetween many UCL Departments, theInstitute of Zoology and the NaturalHistory Museum. As well as weekly

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Becki Lawson was awardedthe prize for best student on the MSc Wild AnimalHealth course. The prize issponsored by Mazuri Zoo Foods.

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seminars, the CEE sponsors a series ofworkshops. This year the ZSL MeetingRooms were the venue for a workshopon ‘Adaptive Molecular Evolution’ anda one-day conference entitled ‘Sex andasex from microbes to multicells’, withspeakers including John MaynardSmith (Sussex), Matthew Meselson(Harvard), and Bill Rice (Santa Barbara).www.gene.ucl.ac.uk/cee/

For students and more experiencedscientists alike, explaining the details ofyour research to fellow scientists isoften a difficult task. However,explaining it to an audience comprisingNobel laureates, Members ofParliament, Fellows of the RoyalSociety, school teachers, sixth formpupils and the general public is moreof a challenge. The research on thesocial behaviour of ants beingconducted by Andrew Bourke, RobHammond and Mike Bruford (Cardiff)formed one of the invited exhibits inthis year’s New Frontiers in Scienceexhibition organized by the RoyalSociety. Assisted by Roselle Chapman,the exhibit was shown for 3 days inLondon and a further 2 days inEdinburgh. The aim is to promote awider understanding of science and thisis an excellent opportunity to inform a wider audience about the work of the Institute. www.royalsoc.ac.uk

Andrew Cunningham, our VeterinaryPathologist, was one of the AmphibianDisease Team, comprising researchers inAustralia and the USA, which solvedone of the world’s most puzzling

environmental problems; the reasonfor the sudden disappearance ofrainforest frogs in protected habitats in Australia and Central America. The study demonstrated how amultidisciplinary approach could solvea complex environmental problem. TheTeam determined that the frog declineswere the result of mass die-offs andidentified the cause of the deaths as anew genus of chytrid fungus whichinfects the skin. The research strategyhas been identified internationally asthe way forward in investigating globalproblems associated with wildlife

diseases and related fields ofconservation. The research hashighlighted the potential ofintroduced/new pathogens as a majorthreat to natural ecosystems, including those previously considered pristineand outside the sphere of humaninfluence. The research also indicatedthat disease threats to globalbiodiversity may be as significant asother forms of anthropogenicenvironmental threats, such as globalwarming or chemical pollution.

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Andrew Cunningham (below second from right),our Veterinary Pathologist,was one of theinternational AmphibianDisease Team awarded theprestigious CSIRO medal(pictured above).

THE ZOOLOGICAL SOCIETY OF LONDON

OfficersPRESIDENT: Sir Martin Holdgate CB MA PhD DSc (h.c.) CBiol FIBiol SECRETARY: Professor Paul H Harvey BA MA DPhil DSc FRS TREASURER: Harry Wilkinson OBE MA FCA

DirectorsDIRECTOR GENERAL: Michael Dixon BSc ARCS DPhil DIRECTOR OF SCIENCE: Georgina Mace OBE DPhil DIRECTOR, LONDON ZOO: Jo Gipps OBE PhD DIRECTOR, WHIPSNADE WILD ANIMAL PARK:

Stuart Earley MInstD MInstM FInstSMM DIRECTOR OF FINANCE: Norman Reed BSc FCA DIRECTOR OF PERSONNEL: Ian Meyrick BA FCIPD

INSTITUTE OF ZOOLOGY STAFF AND STUDENTS

Senior Management StaffDIRECTOR: Georgina M Mace OBE DPhilACTING DIRECTOR OF SCIENCE/REPRODUCTIVE BIOLOGY: William Holt PhDINSTITUTE ADMINISTRATOR: Christina Herterich LLM ACISACTING HEAD OF CONSERVATION GENETICS: William Jordan PhDECOLOGY: Richard Pettifor DPhilVETERINARY SCIENCE: Anthony Sainsbury BVetMed CertLAS MRCVS

Administrative and Support StaffASSISTANT INSTITUTE ADMINISTRATOR: Philip Cottingham BTec (CED) MIScTPA to DIRECTOR OF SCIENCE: Joanne KeoghADMINISTRATIVE ASSISTANT: Katrine Garn MScSECRETARIES: Anna-Marie Cummins, Catherine Kerr BACHIEF TECHNICIAN (ANIMALS): Carol Williams BTec HNCANIMAL TECHNICIANS: Mandy Gordon IIAT; Jake RozowskiSENIOR WORKSHOP TECHNICIAN: Selwyn MundySENIOR PHOTOGRAPHIC TECHNICIAN: Terry Dennett MInstPlGENERAL LABORATORY ASSISTANT: Breda Farrell

Honorary Research FellowsClaudio Ciofi PhDSarah Cleaveland VetMB PhDPeter Daszak PhDProfessor George DuBoulay CBE MB BSM FRCP DMRDJulie Garnier DVMHeather Hall PhDPeter Kertesz BDS LDSProfessor James Kirkwood BVSc PhD MRCVS FIBiolMark O’Connell PhDAmanda Vincent PhDProfessor Paul Watson PhD BVetMed DSc MRCVSStuart Williams PhDBruce Winney PhD

Postdoctoral Staff and Veterinary OfficersPeter Armbruster PhD Michelle Bayes PhD Peter Bennett PhDAndrew Bourke PhDKate Byrne PhD Christopher Carbone DPhilTimothy Coulson PhD Guy Cowlishaw PhDAndrew Cunningham BVMS MRCVSSarah Durant PhDAlireza Fazeli PhDEdmund Flach MA VetMB MSc MRCVSStephan Funk PhDSimon Goodman PhD Rob Hammond PhDLouisa Jenkin PhDPaul Jepson BVMS MRCVSAlison Moore PhDChristine Müller PhD Amanda Pickard PhDAndrew Routh BVSc, RCVS Marcus Rowcliffe PhDStuart Semple PhDTaina Strike BVSc MSc MRCVSSusan Thornton BVetMed MRCVS Jinliang Wang PhD

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TechniciansCHIEF TECHNICIAN: David Cheesman BTec HNCSENIOR TECHNICIANS: Dada Gottelli BSc; Daphne Green HNC AIScT; Tracy Howard BScTECHNICIANS: Miranda Kadwell BSc Shaheed Karl Macgregor, HTec MSc FIBMSElisabeth Thornton BSc

RESEARCH ASSISTANTSRob Deaville BScRobert Hutchinson BSc Janice Long MRes

SENIOR VETERINARY NURSEGillian Ahearne VN

VETERINARY NURSESGillian Bell VN BScChristine Dean VN Joanne Dodds VNIlona Furrokh

Postgraduate Research StudentsZelealam Ashenafi BScJonathan Baillie MESDaisy Balogh MResJacob Bro-Jørgensen MScGina Caplan MScAngus Carpenter MScStephen Casey BScRoselle Chapman MScDavid Cope BAJuliet Dukes MScSonya Gowtage-Sequeira MSc Jim Groombridge BScThomas Maddox BScSusan O’Brien MPhilSusannah Paisley BScOctavio Paulo BScStephen Rossiter BScRussell Seymour MScLisa Thurston BScSaffron Townsend BSc

Scientific Publications and Meetings

ZSL Scientific BooksEDITORSPeter Olney BSc DipEd CBiol FIBiol FLSFiona A Fisken BScASSISTANT EDITORHelen F Stanley PhDSALES ADMINISTRATORMychael Barratt (p/t)

ZSL Journals and MeetingsMANAGING EDITOR Journal of ZoologyJuliet Clutton-Brock PhD DScEDITORSIan Boyd PhD DScTim Halliday MA DPhilPhilip S Rainbow PhD DSc

EDITORS Animal ConservationMichael W Bruford PhDJohn L Gittleman PhDGeorgina M Mace OBE DPhilRobert K Wayne PhDASSISTANT EDITORLinda DaVolls BAEDITORIAL ASSISTANTPatricia ManlySCIENTIFIC MEETINGS CO-ORDINATORDeborah Body MSc (p/t)

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Animal Conservation G M Mace (Editor)

Animal Reproduction Science W V Holt (Member, Editorial Board)

Behavioral Ecology A F G Bourke (Editor)

Behaviour G Cowlishaw (Member, Editorial Board)

British Andrology Society A Moore (Committee Member)

British Veterinary Zoological Society E J Flach (Council Member)

British Wildlife Rehabilitation Council A W Sainsbury (Member, Steering Committee)

Centre for Ecology and Evolution (London) A F G Bourke, G M Mace, J M Rowcliffe

(Members, Steering Committee)

Durrell Wildlife Conservation Trust G M Mace (Council Member; Member, Scientific Advisory Committee)

European Commission Working Group on Transmissible Agents A A Cunningham (Member)

Insectes Sociaux A F G Bourke (Member, Editorial Board)

Institute of Biology W V Holt (ZSL representative)

IUCN Cat Specialist Group S M Durant (Member)

IUCN Declining Amphibian Population Task Force A A Cunningham (Chair, Pathology and Diseases Working Group)

IUCN Species Survival Commission G M Mace (Member, Executive Committee)

IUCN Species Survival Commission Conservation Breeding Specialist Group A A Cunningham, P M Bennett, E J Flach,

G M Mace, A W Sainsbury (Members)

IUCN Species Survival Commission Red List Committee G M Mace (Member)

IUCN Species Survival Commission Reintroductions Specialist Group G M Mace (Member)

IUCN Species Survival Commission Veterinary Specialist Group E J Flach, A W Sainsbury (Member)

Marwell Zoological Park, Animal Heath and Welfare Committee A A Cunningham, E J Flach (Member)

NERC Science and Technology Board G M Mace (Member)

Primate Society of Great Britain G Cowlishaw (Council Member)

Reproduction and Fertility W V Holt (Member, Editorial Board)

Royal Society for the Protection of Birds G M Mace (Council Member)

Society for Conservation Biology G M Mace (Member, Board of Governors)

Society for Low Temperature Biology W V Holt (Committee Member)

Society for the Study of Fertility A R Pickard (Committee Member)

UK Pig Reproduction Research Liaison Group W V Holt (Committee Member)

World Association of Wildlife Veterinarians A W Sainsbury (President)

AKÇAKAYA H R, FERSON S, BURGMAN M A, KEITHD A, MACE G M & TODD C R (2000). Makingconsistent IUCN classifications under uncertainty.Conservation Biology 14: 1001-1013.

ALBON S D, COULSON T N, BROWN D, GUINESS FE, CLUTTON-BROCK T H & PEMBERTON J M (2000).Temporal changes in the key factors influencing thepopulation dynamics of red deer. Journal of AnimalEcology 69: 1096-1109.

ARMBRUSTER P, HUTCHINSON R A & LINVEL T(2000). Equivalent inbreeding depression underlaboratory and field conditions in a tree-hole-breedingmosquito. Proceedings of the Royal Society of LondonSeries B 267: 1939-1945.

BAKER P J, FUNK S M, HARRIS S & WHITE P C L (2000).Flexible spatial organization of urban foxes, Vulpesvulpes, before and during an outbreak of sarcopticmange. Animal Behaviour 59: 127-146.

BARKAI-RONAYNE A (2000). Retrospective analysis ofmortality records and population viability analysis oftrumpeter swans (Cygnus buccinator) in southernOntario. MSc Thesis, University of London.

BAYES M K, SMITH K L, ALBERTS S C, ALTMANN J& BRUFORD M W (2000). Testing the reliability ofmicrosatellite typing from faecal DNA in the savannahbaboon. Conservation Genetics 1: 173-176.

BILLINGTON S (2000). Extraction and semi-quantification of environmental Mycobacterium aviumat the Wildfowl and Wetlands Trust, Slimbridge, using polymerase chain reaction. MSc Thesis,University of London.

CASEY S (2000). Conservation genetics of seahorses(Hippocampus species). PhD Thesis, University of London.

CATCHPOLE E A, MORGAN B J T, COULSON T N,FREEMAN S N & ALBON S D (2000). Factors influencing Soay sheep survival. AppliedStatistics 49: 453-472.

CLAUSS M, FLACH E J, GHEBREMESKEL K, TACK C& HATT J-M (2000). Supplementing the diet ofcaptive giraffe (Giraffa camelopardalis) with linseedextraction chips. In Zoo Animal Nutrition: pp. 271-279. (Eds J Nijboer, J-M Hatt, W Kaumanns, ABeijnen & V Ganslosser). Filander-Verlag, Fürth.

COULSON T, MILNER-GULLAND E J & CLUTTON-BROCK T H(2000). The relative roles of density and climaticvariation on population dynamics and fecundity rates inthree contrasting ungulate species. Proceedings of theRoyal Society of London Series B 267: 1771-1779.

COWLISHAW G & DUNBAR R (2000). PrimateConservation Biology. Chicago University Press, Chicago.

CRANDALL K A, BININDA-EDMONDS O R P, MACE G M & WAYNE R K (2000). Consideringevolutionary processes in conservation biology. Trendsin Ecology and Evolution 15: 290-295.

CUNNINGHAM A A, DASZAK P & HYATT A D (2000).Emerging infectious diseases and amphibianpopulation declines. Proceedings of the BVZS SpringMeeting. 13-14 May 2000: pp. 35-37.

CUNNINGHAM A A, DASZAK P & HYATT A D (2000).Emerging infectious diseases of wildlife: implicationsfor conservation & public health. Proceedings of the

BVZS Spring Meeting. 13-14 May 2000: pp. 17-18.

CURTIS D J, ZARAMODY A, GREEN D I & PICKARD A R(2000). Non-invasive monitoring of reproductive status inwild mongoose lemurs (Eulemur mongoz). ReproductionFertility and Development 12: 21-29.

CURTIS D J, ZARAMODY A, GREEN D I & PICKARD AR (2000). Non-invasive monitoring of reproductivestatus in wild mongoose lemurs (Eulemur mongoz): aninvestigation of faecal steroid excretion patterns.Proceedings of the European Federation of Primatology (Zoological Society of London). 28-29November 2000.

DASZAK P & CUNNINGHAM A A (2000). Extinctionby infection. Trends in Ecology and Evolution 14: 279.

DASZAK P & CUNNINGHAM A A (2000). More on theecological impact of fungal infections on wildlifepopulations. Parasitology Today 16: 404-405.

DASZAK P & CUNNINGHAM A A (2000). Areassessment of ‘Maladaption syndrome’. 49th AnnualWildlife Disease Association Meeting (Jackson Hole,Wyoming, USA). 4-8 June 2000.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Emerging infectious diseases of wildlife - threats tobiodiversity and human health. Science 287: 443-449.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Conservation conundrum - Response. Science 288: 2320.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Emerging infectious diseases of wildlife: implicationsfor human health. International Conference onEmerging Infectious Diseases (ICEID 2000) (Atlanta,Georgia, USA). 16-19 July 2000.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Amphibian chytridiomycosis, emerging diseases andpathogen pollution. Getting the Jump! on amphibiandisease. International Conference on AmphibianDisease (Cairns, Australia). 26-30 August 2000.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Amphibian chytridiomycosis. International VirtualConference in Veterinary Medicine (University ofGeorgia, Athens, USA). 16 October - 16 November2000.

DASZAK P, CUNNINGHAM A A & HYATT A D (2000).Viral emergence within the human–wildlife continuum.Emergence and control of zoonotic ortho-paramyxovirus diseases: an international symposium.Fondation Marcel Merieux.

DASZAK P, CUNNINGHAM A A, BERGER L, HYATT AD, GREEN D E, SPEARE R & PORTER D (2000).Chytridiomycosis - the cause of amphibian populationdeclines. Mycological Society of America AnnualMeeting (Burlington, Vermont USA). 31 July - 3August 2000.

DURANT S M (2000). Predator avoidance, breedingexperience and reproductive success in endangeredcheetahs, Acinonyx jubatus. Animal Behaviour 60:121-130.

DURANT S M (2000). Living with the enemy: avoidance ofhyenas and lions by cheetahs in the Serengeti. BehavioralEcology 11: 624-632.

DURANT S M (2000). Dispersal patterns, socialstructure and population viability. In Behaviour and

Conservation: pp. 172-197. (Eds L M Gosling & W JSutherland). Cambridge University Press, Cambridge.

FAZELI A, MOORE A & HOLT W V (2000). BritishAndrology Society’s Workshop: sperm interactions with epithelia and their products. Human Fertility 3:166-171.

FINCH A M, ANTIPATIS C, PICKARD A R &ASHWORTH C J (2000). Timing and prevalence ofrunting in large white X landrace and Chinese meishangilts. British Society of Animal Science Symposium on‘Early Regulation of Mammalian Development’(Aberdeen, Scotland). 18-20 September 2000.

FLACH E J, D’ALTERIO G-L, ZAHZAH K, MOLCANOVA R,WAKEFIELD S, BAROSSI D, EULENBERGER K, KOPCOK M,OLLIVET F, PETIT T, VAHALA J & FRÖLICH K (2000).Veterinary monitoring of captive-bred scimitar-horned oryx(Oryx dammah) prior to reintroduction in Tunisia.Proceedings of the 3rd Scientific Meeting of the EuropeanAssociation of Zoo and Wildlife Veterinarians (Paris). 31May - 4 June 2000: pp. 91-97.

FLACH E J, RILEY J, MUTLOW A G & McCANDLISH IA P (2000). Pentastomiasis in Bosc’s monitor lizards(Varanus exanthematicus) caused by an undescribedsambonia species. Journal of Zoo and WildlifeMedicine 31(1): 91-95.

FLACH E J, TAYLOR P, BROWN K & DODDS J (2000).Immobilisation of giraffe with medetomidine andketamine. Proceedings of BVZS Autumn meeting,Exotic Animal Anaesthesia & Surgery, (ZSL). 20-21November: pp. 55-57.

GODFRAY H C J, MÜLLER C B & KRAAJIEVELD A R(2000). Habitat heterogeneity and the behavioural andpopulation ecology of host parasitoid interactions. InEcological Effects of Habitat Heterogeneity: pp. 215-236. (Eds M J Hutchings, A E John & A J A Stewart).Blackwell Science, Oxford.

GOLDSWORTHY C (2000). Study into the associationbetween chronic exposure to polychlorinated biphenylsand thymic involution and cystic change in harbourporpoises (Phocoena phocoena) from British waters.MSc Thesis, University of London.

GOOSSENS B, CHIKHI L, UTAMI SRI S, DE RUITER J& BRUFORD M W (2000). A multi-samples, multi-extracts approach for microsatellite analysis of faecalsamples in an arboreal ape. Conservation Genetics 1:175-162.

GRENFELL B T, FINKENSTÄDT B F, WILSON K,COULSON T N & CRAWLEY M J (2000). Nonlinearityand the Moran effect. Nature 406: 847.

GROOMBRIDGE J (2000). Conservation genetics ofthe Mauritius kestrel, pink pigeon and echo parakeet.PhD Thesis, University of London.

GROOMBRIDGE J J, JONES C G, BRUFORD M W &NICHOLS R A (2000). Conservation biology – ‘Ghost’alleles of the Mauritius kestrel. Nature 403: 616.

GURNELL J, GILRAY J, LURZ P, NETTLETON P,RUSHTON S, SAINSBURY A W (2000). Parapoxvirusdisease in red squirrels: is it responsible for thedemise of the red squirrel in Europe? 2ndInternational colloquim of tree squirrels (Oregon,USA). May 2000.

publications 31

HILTON-TAYLOR C, MACE G M, CAPPER D R,COLLAR N J, STUART S N, BIBBY C J, POLLOCK C,THOMSEN J B (2000). Assessment mismatches mustbe sorted out: they leave species at risk. NatureCorrespondence 404: 541.

HOLBROOK J D, BIRDSEY G M, YANG Z, BRUFORDM W & DANPURE C J (2000). Molecular adaption ofalanine: glyoxylate aminotransferase targeting inprimates. Molecular Biology and Evolution 17(3): 387-400.

HOLT W V (2000). Basic aspects of frozen storage ofsemen. Animal Reproduction Science 62: 3-22.

HOLT W V (2000). Fundamental aspects of spermcryobiology: the importance of species and individualdifferences. Theriogenology 53: 47-58.

HYATT A D & CUNNINGHAM A A (2000).Ranaviruses; a threat to amphibians? Getting theJump! on amphibian diseases. InternationalConference on Amphibian Disease (Cairns, Australia).26-30 August 2000.

HYATT A D, GOULD A, COUPAR B, HENGTSBERGERS & CUNNINGHAM A (2000). Ranaviruses; diversityand impact on commercial fisheries and piscine andherpetological wildlife. 6th Australian Conference forElectron Microscopy (ACEM), (Canberra). pp. 99-100.

HYATT A D, GOULD A R, ZUPANOVIK Z,CUNNINGHAM A A, HENGTSBERGER S,WHITTINGTON R J, KATTENBELT J & COUPAR B E H(2000). Comparative studies of piscine and amphibianiridoviruses. Archives of Virology 145: 301-331.

JEPSON P D, BAKER J R, KUIKEN T, SIMPSON V R,KENNEDY S & BENNETT P M (2000). Pulmonarypathology of harbour porpoises (Phocoena phocoena)stranded in England and Wales between 1990 and1996. Veterinary Record 146: 721-728.

KELLY M J & DURANT S M (2000). Viability of theSerengeti cheetah population. Conservation Biology14: 786-797.

KENNEDY S, KUIKEN T, JEPSON P D, DEAVILLE R,FORSYTH M, BARRETT T, VAN DE BILT W G, OSTERHAUS AD M E, EYBATOV T, DUCK C, KYDYRMANOV A,MITROFANOV I & WILSON S (2000). Mass die-off ofCaspian seals caused by canine distemper virus.Emerging Infectious Diseases 6: 637-639.

KIFLAWI M, ENQUIST B J & JORDAN M A (2000).Position within the geographic range, relative localabundance and developmental instability. Ecography23: 539-546.

KILIAN S A R (2000). Assessment of reproduction inthe Amur leopard (Panthera pardus orientalis). MScThesis, University of London.

LAFORTUNE M (2000). Clinical and cardiopulmonaryevaluation of medetomidine, clove oil and propofol inleopard frogs (Rana pipiens). MSc Thesis, Universityof London.

LAWSON B (2000). The geographical distribution,natural history and pathology of parapoxvirus diseasein red squirrels in the UK. MSc Thesis, University of London.

MacDONALD D W, MACE G M & RUSHTON S (2000).British mammals: is there a radical future? InPriorities for the Conservation of Mammalian Diversity- Has the Panda had it’s day?: pp. 177-205. (Eds AEntwistle & N Dunstone). Cambridge University Press,Cambridge.

MACE G M (2000). Summary of the results of thereview of IUCN Red List categories and criteria 1996-2000. In 2000 IUCN Red List of Threatened Species:pp. 57-61. (Ed. C Hilton-Taylor). IUCN, Gland,Switzerland.

MACE G M & BALMFORD A (2000). Patterns andprocesses in contemporary mammalian extinction. InPriorities for the Conservation of Mammalian Diversity- Has the Panda had it’s day?: pp. 27-52. (Eds AEntwistle & N Dunstone). Cambridge University Press,Cambridge.

MACE G M, BALMFORD A, BOITANI L, COWLISHAWG, DOBSON A P, FAITH D P, GASTON K J,HUMPHRIES C J, LAWTON J H, MARGULES C R,MAY R M, NICHOLLS A O, POSSINGHAM H P,RAHBEK C, VAN JAARSVELD A S, VANE-WRIGHT R I& WILLIAMS P H (2000). It’s time to work togetherand stop duplicating conservation efforts. NatureCorrespondence 405: 393.

MAR K U (2000). Life-table analysis of captiveworking Asian elephants (Elephas maximus) ofMyanmar. MSc Thesis, University of London.

MAYER J (2000). Use of the geographic informationsystem to investigate mercury levels in correlation withpost-mortem findings of Aspergillus induced lesions inthe common loon (Gavia immer) in the northeasternUnited States of America. MSc Thesis, University of London.

MILNER-GULLAND E J, COULSON T N & CLUTTON-BROCK T H (2000). On harvesting astructured population. Oikos 88: 592-602.

NAIQUE S, PORTER R, CUNNINGHAM A A &HUGHES S (2000). Scoliosis in an orang utan. TheBritish Association of Clinical Anatomists Summer2000 Scientific Meeting (St John’s College,Cambridge). 20-21 July 2000.

NETTLETON P F, GILRAY J, THOMAS K, MCINNES C,SAINSBURY A W & GURNELL J (2000). Studies on apoxvirus from the European red squirrel (Sciurusvulgaris). Proceedings of the 5th InternationalCongress of the European Society for VeterinaryVirology, (Brescia, Italy). 27-30 August.

O’KEEFE J (2000). Experimental investigation of thesusceptibility and pathogenesis of West Nile Virus inMallards (Anas platyrhynchos). MSc Thesis, Universityof London.

OWENS I P F & BENNETT P M (2000). Ecological basis ofextinction risk in birds: habitat loss versus humanpersecution and introduced predators. Proceedings of theNational Academy of Sciences USA 97: 12144-12148.

OWENS I P F & BENNETT P M (2000). Quantifyingbiodiversity: a phenotypic perspective. ConservationBiology 14: 1014-1022.

PAUL R E L, COULSON T N, RAIBAUD A & BREY B T(2000). Erythropoietic sex determination in malariaparasites. Science 287: 128-131.

PETTIFOR R A, CALDOW R W G, ROWCLIFFE J M,GOSS-CUSTARD J D, BLACK J M, HODDER K H,HOUSTON A I, LANG A & WEBB J (2000). Spatiallyexplicit, individual based, behavioural models of theannual cycle of two migratory goose populations.Journal of Applied Ecology 37(S1): 103-135.

PETTIFOR R A, NORRIS K N & ROWCLIFFE J M(2000). Incorporating behaviour in predictive modelsfor conservation. In Behaviour and Conservation: pp.198-220. (Eds L M Gosling & W J Sutherland).Cambridge University Press, Cambridge.

PICKARD A R (2000). Reproductive and welfaremonitoring for the management of captive populations.Proceedings of the Zoological Society of LondonSymposium ‘Reproduction and Integrated ConservationScience’ (London). 9-10 November 2000.

PICKARD A R, ABAIGAR T, GREEN D I, HOLT W V &CANO M (2000). Estrogen excretion as a prediction offertility in an exotic ungulate, the mohor gazelle(Gazella dama mhorr). Theriogenology 53: 343.

PICKARD A, DI MARCO F & PANKHURST S (2000).Monitoring stress in mara: preliminary findings offaecal cortisol analysis. 2nd Annual Symposium onZoo Research, Federation of Zoological Gardens ofGreat Britain & Ireland, (Paignton Zoo, Devon). 6-7July 2000: pp. 201-202.

PIZZI R (2000). Investigations of causes of mortalityin British garden birds by post-mortem examination.MSc Thesis, University of London.

PURVIS A, AGAPOW P-M, GITTLEMAN J L & MACE G M(2000). Nonrandom extinction and the loss ofevolutionary history. Science 288: 328-330.

PURVIS A, GITTLEMAN J L, COWLISHAW G & MACE G M(2000). Predicting extinction risk in declining species.Proceedings of the Royal Society of London SeriesB 267: 1947-1952.

PURVIS A, JONES K E & MACE G M (2000).Extinction. BioEssays 22: 1123-1133.

ROSSITER S J (2000). The causes and consequences ofgenetic structure in the greater horseshoe bat(Rhinolophus ferrumequinum). PhD Thesis, University of Bristol.

ROSSITER S J, JONES G, RANSOME R D & BARRATT E M(2000). Parentage, reproductive success and breedingbehaviour in the greater horseshoe bat (Rhinolophus

ferrumequinum). Proceedings of the Royal Society ofLondon Series B 267: 545-551.

ROSSITER S J, JONES G, RANSOME R D & BARRATT E M(2000). Genetic variation and population structure in theendangered greater horseshoe bat Rhinolophusferrumequinum. Molecular Ecology 9: 1131-1135.

SAINSBURY A W, NETTLETON P, GILRAY J & GURNELL J(2000). Grey squirrels have a high seroprevalence to aparapoxvirus associated with deaths in red squirrels.Animal Conservation 3: 229-233.

SAINSBURY A W, NETTLETON P, GILRAY J & GURNELL J(2000). Parapoxvirus infection: an emerging disease inred squirrels. Proceedings of the British VeterinaryZoological Society (Cotswold Wildlife Park, UK). 13-14 May.

SAINSBURY A W, NETTLETON P F, GILARY J A, THOMAS K,McINNES C & GURNELL J (2000). Grey squirrels havehigh seroprevalence to a parapoxvirus associated withdeaths in red squirrels. Association of VeterinaryTeachers and Research Workers Annual Conference(Scarborough). April 2000.

SELISKAR A, FLACH E J, LUNA S P L & EATWOOD R(2000). Isoflurane anaesthesia in an Indian rhinoceros(Rhinoceros unicornis). Proceedings of the 7th WorldCongress of Veterinary Anaesthesia, (Berne). 20-23September 2000.

SEMPLE S & McCOMB K (2000). Perception offemale reproductive state from vocal cues in amammal species. Proceedings of the Royal Society ofLondon Series B 267: 707-712.

SMITH A T, BOITANI L, BIBBY C, BRACKETT D,CORSI F, DA FONSECA G A B, GASCON C, DIXON MG, HILTON-TAYLOR C, MACE G, MITTERMEIER R A,RABINOVICH J, RICHARDSON B J, RYLANDS A,STEIN B, STUART S, THOMSEN J & WILSON C(2000). Databases tailored for biodiversityconservation. Science 290: 2073.

STRIKE T & PICKARD A (2000). Non-invasivehormone analysis for reproductive monitoring infemale southern white rhinoceros (Ceratotheriumsimum simum). 2nd Annual Symposium on ZooResearch, Federation of Zoological Gardens of GreatBritain & Ireland (Paignton Zoo, Devon). 6-7 July2000: pp. 191-197.

THURSTON L M (2000). An investigation into sources ofvariation and the genetic basis of boar spermatozoasurvival following cryopreservation. PhD Thesis,University of London.

THURSTON L M, SIGGINS K, MILEHAM A, WATSON P F &HOLT W V (2000). Identification of amplified restrictionfragment length polymorphism (AFLP) markers linked togenes controlling boar sperm viability followingcryopreservation. Journal of Reproduction and FertilityAbstract Series 25.

VAN WYK J W (2000). A retrospective study of thepattern of iron storage in captive members of the orderArtiodactyla. MSc Thesis, University of London.

WANG J (2000). Effects of population structures andselection strategies on the purging of inbreedingdepression due to deleterious mutations. GeneticalResearch 76: 75-86.

WANG J & HILL W G (2000). Marker-assistedselection to increase effective population size byreducing Mendelian segregation variance. Genetics154: 475-489.

WEBER M (2000). Effects of hunting on tropical deerpopulations in South eastern Mexico. MSc Thesis,University of London.

WESCHE P (2000). Isolation of Malasseziapachydermatis from the skin of captive WhiteRhinoceros (Cerathotherium simum simum), BlackRhinoceros (Diceros bicornis michaeli) and Indian(Rhinoceros unicornis). MSc Thesis, University of London.

WILLIAMS D L, MacGREGOR S & SAINSBURY A W(2000). Evaluation of bacteria isolated from infectedeyes of captive, non-domestic animals. VeterinaryRecord 146: 515-518.

Text in bold refers to articles highlighted in theresearch section of the report.

32 publications

© 2001The Institute of ZoologyThe Zoological Society of LondonRegistered charity no. 208728

Thanks to the following for use of the photographson p6/7 Gareth Jones, Bristol University, p8 Richard Cooke, p10 Sue Wilson, World Bank,p11 Seamus Kennedy, Dept. of Agriculture forNorthern Ireland, p13 Tim Coulson, University ofCambridge, p14/15 Ian Owens, Imperial College,London, p17 Josephine Pemberton, University of Edinburgh, p21 Deborah Curtis, University ofSurrey Roehampton, p27 James Gibbs.

Thanks also to Brian Aldrich, Helen Clarke, Guy Cowlishaw, Rob Deaville, Terry Dennett, Sarah Durant, Edmund Flach, Jo Gipps, Rob Hammond, Michael Lyster, Amanda Pickardand Lisa Thurston for photographs.

Edited by Helen F Stanley and Katrine Garn

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