THE PROTOCOLS FOR KOALA RESEARCH USING RADIO-COLLARS:A REVIEW BASED ON ITS APPLICATION IN A TALL COASTAL

FOREST IN NEW SOUTH WALES AND THE IMPLICATIONS FORFUTURE RESEARCH PROJECTS

SALLY L RADFORD, JEFF MCKEE, ROSS L. GOLDINGAY AND ROD P. KAVANAGH

Radford SL, McKee J, Goldingay RL and Kavanagh RP, 2006. The protocols for koalaresearch using radio-collars: a review based on its application in a tall coastal forest in NewSouth Wales and the implications for future research. Australian Mammalogy 28: 187-200.

In 1996, guidelines were produced for capture and radio-tracking protocols for koala(Phascolarctos cinereus) research within New South Wales (NSW). An integrated projectcommenced in 1998 to examine P. cinereus ecology and health status in Pine Creek StateForest. This project utilised intensive clinical and pathological assessment protocols oncaptured P. cinereus in combination with radio-tracking and ecological investigations. Themethods used in this project were referred to the NSW Koala Research Committee (KRC) forreview in mid 1999 due to the political profile of the study area. The KRC assessed the projectprotocols and reviewed the original guidelines incorporating some of the protocols used in thePine Creek project. The outcome is a new set of protocols for P. cinereus research within NSWwhich are more explicit and restrictive than those applied to P. cinereus research elsewhere orto research on other species. In their current form the new guidelines require a substantialinvestment in time, equipment, personnel and finance; factors that may deter or restrict future,comprehensive ecological research on P. cinereus populations. They inadequately provide forsome practices we believe important in minimising the invasiveness of P. cinereus capture. Wepropose amendments to the guidelines in the areas of personnel required, behaviouralassessment, capture methods, processing safety and tracking frequency. We suggest that theseamendments will render the guidelines more accessible to a broader range of projects, andeasier to apply under field conditions while preserving the intent to maintain P. cinereuswelfare and research best practice.

Key words: Phascolarctos cinereus, capture, radio-tracking, handling.

SL Radford, School of Environmental Science and Management, Southern Cross University,PO Box 157, Lismore, NSW 2480, Australia. Current address: NSW NPWS, PO Box 2228,Jindabyne, NSW 2627, Australia. J McKee, Genomics Research Centre, School of HealthSciences, Griffith University, Gold Coast MC, Qld 9726, Australia. RL Goldingay, School ofEnvironmental Science and Management, Southern Cross University, PO Box 157, Lismore,NSW 2480, Australia. RP Kavanagh, State Forests of NSW, Forest Research and DevelopmentDivision, PO Box 100, Beecroft, NSW 2119, Australia. Manuscript received 4 February 2004;accepted 15 May 2005.

THE koala (Phascolarctos cinereus) has been thesubject of extensive research involving the use ofradio-tracking, particularly in Victoria (Lee et al.1991). However, P. cinereus research becamecontroversial in New South Wales (NSW) during theearly 1990s when some animal deaths appeared to beassociated with radio-collaring. One study occurredin the south-east forests of NSW where P. cinereus isuncommon (Jurskis and Potter 1997; Lunney et al.1997; Jurskis et al. 2002). This led to thedevelopment of a set of guidelines to be followed byfuture P. cinereus radio-collaring projects in NSW(Bali and Delaney 1996).

Another P. cinereus research project, which alsobecame embroiled in the politically-charged debatesurrounding government decisions about major land-use changes, was the Pine Creek Koala Project. TheState Forests of NSW (SFNSW) licence to harvesttimber in Pine Creek State Forest (PCSF) waswithdrawn by the NSW National Parks and WildlifeService (NPWS) in 1995 following complaints bymembers of a local community environmental group(Woodford 1995; SFNSW 2000). For the licence tobe re-instated, SFNSW was required to prepare amanagement plan for the forest that would allow forsustainable harvesting while maintaining a viable P.

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cinereus population (SFNSW 2000). The PCSFKoala Management Plan was formulated followingextensive consultation and was subsequentlyapproved and signed jointly by NPWS and SFNSW(SFNSW 2000). The Plan identified the need foradditional information about the ecology of P.cinereus within the forest and interactions between P.cinereus ecology and harvesting operations. A Ph.D.project, funded by SFNSW, was established toaddress the key research issues identified by the Plan.This project began in late 1998 and utilised P.cinereus capture and radio-tracking in theinvestigation of ecology, population dynamics andhealth status. Fieldwork for the research projectended in October 2002. In July 2003, a large portionof PCSF was gazetted as part of Bongil BongilNational Park in accordance with the NSW Premier’spre-election promises (National Parks Estate Act2003; Totaro 2003). As this study was completedbefore the gazettal, the study area is referred to asPCSF throughout this paper.

Prior to commencement of the project, scientificresearch permits for the research were gained fromNPWS and SFNSW. Animal Care and EthicsCommittee (ACEC) approval was also gained fromSouthern Cross University and SFNSW. Additionalapproval was also required from the NSW KoalaResearch Committee (KRC) because the projectinvestigated P. cinereus ecology in a wild-livingpopulation. The project proposal was submitted to theKRC in January 1999 and was given interim approvalin April 1999 pending submission of progress reportsfollowing each capture session.

In October 1999, a complaint was submitted tothe KRC alleging that the practices of the projectwere in conflict with the guidelines set out by Baliand Delaney (1996). The grievance proceduresrequired the attendance of the research scientists at ameeting to review the project’s protocols. Thesuccessful defence of the Pine Creek Koala Projecthighlighted the ambiguity in the requirements andresulted in a review of the Bali and Delaneyguidelines (1996) by the KRC. The outcome was anew set of prescriptive protocols for application to allresearch projects based on capture and radio-trackingof P. cinereus in NSW (NSW Koala ResearchCommittee 2000).

The aim of this paper is to review the KRCguidelines, which is the current reference documentfor NPWS research permits, in relation to the fieldexperiences obtained from implementing these

protocols in the Pine Creek Koala Project.

METHODSStudy sitePine Creek State Forest is located 18 km south ofCoffs Harbour on the mid north coast of NSW (Fig.1). The forest covers an area of 5,890 ha fromBundagen Beach inland to Bellingen and is bisectedby the Pacific Highway. This forest has had anextensive history of logging extending back to 1881and recent surveys (Newman and Partners 1996;Smith and Andrews 1997) have indicated that allareas within the boundaries of the forest have beenimpacted by harvesting. The study area covered theforest west of the Pacific Highway; a 4,418 haportion.

ProtocolsThe project protocols were adapted from Bali andDelaney (1996) to suit tall, moist forest habitat and inaccordance with the regulations regarding P. cinereusresearch as required by NPWS and the KRC. Inaddition, stringent post-capture handling andassessment protocols were used on all animals inorder to obtain detailed health, morphological andreproductive profiles for the capture samplefollowing Kavanagh and Barrott (2001). These datawere integrated with the habitat, home range and landuse data that were collected concurrently.

Capture protocolsCapture by flaggingPrior to the commencement of any capture, the safetyof such a capture for the animal and the capture teamwas assessed. During designated capture sessions, acapture team of four people (2 arboreal flaggers, 1terrestrial flagger, 1 catcher) used the flaggingmethod for most captures. Flagging encouragesdownward movement of the animal by waving abrightly coloured cloth attached to an extendablefibreglass pole above the animal’s head. The height(> 40 m) and complexity of the habitat (multi-layered, vines) within this forest resulted in anadaptation of the typical practice of flagging (Baliand Delaney 1996). During opportunistic captures,the capture team consisted of two to four people (1arboreal flagger, 1-2 terrestrial flaggers, 1 catcher)and again used the flagging method. Noosing was notemployed in this study to capture any animals,although it is commonly employed in other projects(Bali and Delaney 1996).

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Fig. 1. Map showing location of Pine Creek State Forest on the mid north coast of NSW.

Capture by trapTrapping was employed to catch collared P. cinereuswhose transmitter batteries were due for renewal andwhen the target animals were located in treesunsuited for flagging or when previous captureattempts of the target animal had been unsuccessful.A trap (Fig. 2) was only employed where the groundsurrounding the target tree was relatively flat andunobstructed and where there was not another treecrown within reach or stem within jumping distancefor the koala. The trap was designed and built byWildcare; a wildlife care and research organizationin Queensland, and was a modification of a standardcage trap (Fig. 3). The trap (dimensions: 80 cmlength × 40 cm width × 60 cm height) consisted of atimber floor and side walls. The roof was 25 mm ×80 mm weld mesh, as was the top-hinged swing door.The rear wall of the trap was thick Perspex providingthe appearance of an opening and escape route fromthe enclosure. A treadle, depressed when crossed bythe koala, triggered the trap. This ensured that thekoala would be well inside the trap before the doorswung closed. Once triggered, the door was heldlocked in place by a dropped locking bar. The fencewas a sheet of galvanised metal (13 m long × 90 cmhigh) supported by hooked steel posts, enclosing thetree containing the animal, forming a funnel into the

trap. Once set, the trap was checked at intervals of≤ 2 h and was never set for ≥ 24 h at a time.

Handling and processing protocolA mobile disease ecology unit was established withineach operational area to anaesthetise and assess eachanimal after capture during capture sessions. Animalswere restrained in clean ventilated calico drawstringbags and transported from the capture site to thedisease ecology unit by vehicle or on foot (maximum15 min transport time). After an initial examinationall P. cinereus were anaesthetised withisofluorane/oxygen by mask induction with aportable gas anaesthetic machine. Whileanaesthetised, animals were scored for condition,age, reproductive status and underwent astandardised clinical and morphometric assessment.Blood (10 ml) was sampled from each animal via thecephalic vein and was stored cool for complete bloodcount, biochemical analysis, serology and DNAextraction. Microbiological swabs were collectedfrom each eye, the pharynx and the cloaca. Extrainvestigative samples were taken from animals withabnormalities as required. Each koala was tagged(Daltons) in each ear and fitted with a fixed plasticcollar supporting a metal canister radio transmitter(Titley 150-151 MHz). All radio-collars were

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Fig. 2. A schematic diagram of the trap including the cage trap and the galvanised steel surrounds with support posts.

Fig. 3. A schematic diagram of the design of the koala cage trap.

Surrounds

Tree

Trap

Supportpost

PerspexEnd Treadle

Trigger

400 mm800 mm

Main Access Door

600 mm

Trigger Mechanis m

Trap Door

Locking Bar

RADFORD ET AL.: KOALA RADIO-COLLAR PROTOCOLS 191

applied loosely enough to allow the collar to comeoff over the head and the ear tags if sufficient tensionwere applied. During the procedure vital signs weremonitored and recorded every 5 min. P. cinereus (n =70) were anaesthetised for a maximum of 62 min(mean = 36 min). Before each animal was processedall surfaces coming into contact with the animalwere freshly prepared. Processing site surfaces incontact with koalas were replaced, disposable itemsdiscarded and fixed equipment was cleaned and colddisinfected with 70% ethanol or chlorhexidine.Clinical operators used disposable coveralls andgloves and all personnel handling animals washedbetween captures.

Release protocolKoalas were held for a minimum of 10 min (mean= 27 min) before release to ensure full recovery priorto removal from veterinary supervision. All animalswere released into the tree from which they werecaptured. In this study, release was on approval fromthe attending veterinarian.

Radio-tracking protocolAnimals were tracked daily or alternate days for thefirst two weeks post capture. They were tracked onalternate days or at least a minimum of three timesper week for the next two weeks. Thereafter, trackingwas undertaken once per week, or once per twoweeks after six months of tracking or after a homerange area was identified. In practice, the frequencyof radio-tracking and the sighting of collared animalsvaried depending on weather and terrain. In oneexceptionally wet year all forests in the study areawere inaccessible for several weeks due to floodingand tracking was suspended. Animals frequentingremnant rainforest areas could be located to a definedarea but were often impossible to sight.RESULTSBlood collected during processing was analysed forserum biochemistry and haematology parameters.These values for each animal were compared with adetermined ‘normal range’ calculated from findingsof previous studies (Dickens 1978) and theunpublished reference source of the IdexxLaboratories (formerly Veterinary Pathology

Service). This normal range is somewhat preliminaryas further research is needed to determine this acrossthe distribution of P. cinereus. Levels identified asoutside the normal range vary from slightly excessivein the case of monocytes to extremely variant in thecase of creatinine kinase (CK). An elevated level ofCK was used as an indicator of muscle damage andthe counts of neutrophils, lymphocytes andmonocytes were regarded as indicators of a ‘stresshaemogram’. Less than 11% of animals capturedwere found with elevated CK levels and a similarpercentage was found with stress haemograms in atleast one of the four variables measured (Table 1).Capture duration data were transformed to improvenormality and a multiple regression of the level ofCK within the blood serum against ambienttemperature and the log of capture duration wasperformed. Their relationship was not significant (r2

= 0.01, F = 0.31, p > 0.05, y = 143.6210((log) captureduration) – 2.4688(ambient temp) + 240.8804)indicating that capture duration and ambienttemperature (within the limits of this study) had nosignificant effect on this measure of P. cinereusstress levels. Animals caught with pre-existingconditions were found to have elevated CK levels.The exclusion of these animals from the regression toclarify the impacts of capture on CK levels did notchange the relationship (r2 = 0.04, F = 0.8, p > 0.05, y= 46.4972((log) capture duration) + 0.8456(ambienttemp) + 139.4385). This indicates that either CK wasnot responsive to stress within the short time betweencapture and blood collection, or that the capturedurations and ambient temperatures experienced inthis study were not sufficiently extreme to elevateCK levels. The residuals from both these regressionswere inspected and found to be normally distributedwithout any patterns.

Only three P. cinereus were found with twohaematology parameters outside the normal range.One of these animals, an adult (4 – 7 yr) female, wasdiagnosed with severe keratoconjunctivitis, poorbody condition, poor vision upon capture, wasreluctant to move throughout the capture and wasfound deceased one month later. The second, an adultfemale, was captured from the midst of a loggingoperation, was recaught five months later when

Creatinine Kinase Neutrophils Lymphocytes MonocytesUnits U/L 106/L 106/L 106/L

Normal range 80 - 500 1-7 1-7 0 - 0.6n 65 41 41 38

Count (%) > normal 6 (9.23) 3 (7.32) 1 (2.44) 2 (5.26)Count (%) < normal 1 (1.54) 0 4 (9.76) 0

Table 1. Results of haematology and blood serum biochemistry analyses indicating number (and proportion) of capturedanimals with muscle damage (creatinine kinase (CK)) and components of a stress haemogram as indicated by haematologyand serum parameters falling outside the normal range.

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transport problems prevented blood analysis, and hersignal was lost a month later. It is noteworthy thatthree P. cinereus were caught from the midst of alogging operation and only one was found with thepotential stress indicator of elevated haematologyparameters. The third animal (adult female) wasrecaptured at a later date and remained a part of theradio-tracking study for two years. No animals werefound to have all three parameters (neutrophils,lymphocytes and monocytes) outside the normalrange, resulting in no P. cinereus caught during ourstudy being diagnosed with a ‘stress haemogram’.

There were no strong relationships betweencapture behaviour and outcomes with respect tocapture-related injury, physiological measurementsor haematology parameters (Table 2). The majorityof capture events (88%) involved ‘active’ animals.This was a behavioural response scored duringcapture, defined as an animal that responded well tothe flag and moved readily about the tree. Most of theanimals caught displayed some form of distress(68%) according to the KRC Protocols includingvocalisation, defecation, urination or aggressionduring the capture, transport, processing or releasephase of the capture, with 72% of ‘active’ animalsalso exhibiting ‘distress’. Only 14% of this lattergroup of animals was found to have injuries sustainedduring the capture event, however none of this group

were found with elevated CK levels (Table 2). Infact, the vast majority of animals were not injuredduring the capture process (86%) (Table 2) and thoseinjured sustained only small cuts or bruising. Thoseanimals least active (i.e., not scored as either activeor hyperactive) and displaying none of thebehaviours identified by the KRC as stress indicators(vocalisation, defecation, urination or aggression)(n = 5) resulted in the longest capture durations,suggesting that this group could be more susceptibleto exhaustion and therefore capture-relatedmisadventure. This group also had the highestfrequency of haematology parameters outside thenormal range (Table 2).

The initial core body temperature (CBT) takenfrom each P. cinereus captured was regressed againstthe ambient temperature at the time of capture andthe log of capture duration. There was a highlysignificant relationship (r2 = 0.25, F = 7.82, p =0.0012; Fig. 4), with the relationship described by theequation: y = 0.948 ((log) capture duration) + 0.110(ambient temperature) + 33.770). Ambienttemperature had a stronger relationship with corebody temperature (p = 0.0089), than with that ofcapture duration (log) (p = 0.0114). The residuals ofthe regression were inspected and found to benormally distributed with no internal patterns.

Budget Items 1998-99 1999-00 2000-01 2001-02 2002-03 TotalPersonnel Catching team 20,828.61 18,844.48 16,887.42 8,119.73 $ 64,680.24Veterinary team 13,221.60 14,582.61 7,631.61 4,749.91 $ 40,185.73Opportunistic captures 1,980.00 1,638.20 $ 3,618.20Laboratory work 315.00 2,551.90 556.60 2,725.03 226.05 $ 6,374.58Opportunistic vet services 50.00 526.35 392.75 $ 969.10Capture personnel subtotal 34,365.21 36,028.99 27,581.98 17,625.62 226.05 $ 115,827.85Capture session duration (d) 22 24 12 6 64Opportunistic captures (no.) 9 7 16Koalas caught 19 23 26 9 77Non-capture personnel costs Additional tracking 1,656.00 1,816.00 2,737.00 $ 6,209.00Veterinary post mortems 90.00 243.00 138.60 $ 471.60Post mortem vet lab work 1,003.40 $ 1,003.40Consultant - veg plot work 16,500.00 $ 16,500.00Student costs 7,787.50 16,212.88 17,080.56 30,481.06 13,125.00 $ 84,687.00Total personnel 42,152.71 53,987.87 46,721.54 68,485.68 13,351.05 $ 224,698.85Total other 13,011.94 7,161.98 3,995.91 3,740.17 1,683.22 $ 29,593.23Annual cost per koala 1,868.36 1,685.19 1,060.85 1,958.40 1,643.20 Annual totals $ 55,164.65 $ 61,149.85 $ 50,717.45 $ 72,225.85 $ 15,034.27 $ 254,292.08

Table 3. Expenditure for the Pine Creek Koala Project – an example of implementing the Protocols for Koala Research UsingRadio-collars (NSW Koala Research Committee 2000) in their most extreme, including the number of days for capturesessions, number of opportunistic captures and cost per koala for capture, veterinary and laboratory work. (Other =equipment, maintenance, consumables and travel).

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DISCUSSIONThis project employed resource-intensive methods toexamine home range and habitat variables in relationto forestry practice and their relationship to thehealth, reproductive and nutritional status of thepopulation sample. It was an expensive exercise, withexpenditure exceeding $254,000 (Table 3). Capturesessions utilised four people in the catching team,three support staff including a wildlife veterinarian inthe mobile disease ecology unit, and included two ormore people concurrently radio-tracking in theoperational area. Animals were captured using theflagging or trap methods and then anaesthetised,subject to stringent clinical and morphologicalexamination and sampling procedures. After recoveryand release, animals were closely monitored andassessed for extended periods. The project explored arange of capture, handling and assessment protocolsand was well placed to assess the effects of thoseprocedures. Thus, this project provides a goodplatform from which to examine the implementationof the current KRC guidelines.

We contend that some components of the existingKRC guidelines, if literally applied, are unnecessarilyrestrictive and thus have the potential to limit or deterfuture research. In addition, some areas we considercritical to the safe operation of a field projectinvolving P. cinereus are not addressed. We proposeamendments or modifications to the following areas:

Capture issuesAbandoning capturesThe KRC Protocols identify several signs of “stress”in P. cinereus including vocalising, urination,defecation, and panting (NSW Koala ResearchCommittee 2000). They state that researchers shouldabandon a capture if the koala “cries or exhibits otherperceived high level signs of distress” and the capturecannot be concluded within 2-3 min (NSW KoalaResearch Committee 2000). Abandoning a capturecan be a costly exercise, both in terms of time andresources on the part of the research team and interms of energy expenditure on the part of the animal.Nevertheless it is sometimes necessary to suspend acapture attempt in deference to a perceived risk to theanimal or the capture personnel, or if circumstancessuggest that the attempt is unlikely to succeed.

In assessing risk to the animal we agree that“panting” (hyperventilation with mouth breathing),particularly if observed in combination with highambient temperature (discussed below), reluctance tomove or respond to the flag or uncoordination, is adefinite and reliable indication for aborting a capture.Hyperventilation may indicate impending exhaustion,

hyperthermia or underlying pathology and pursuing ahyperventilating animal may predispose it toexhaustion or misadventure. In addition, reluctance tomove and respond to the flag were characteristicsfound to be potentially indicative of unhealthyanimals as detected by assessment of physiologicaland haematological parameters (Table 2), resulting inlonger and therefore potentially hazardous captures.However, we disagree that urination, defecation orvocalisation during a capture attempt are indicationsto abort a capture or indications that an animal iscompromised beyond its physiological reserves.Firstly, many individuals from disparate taxonomicgroups display these behaviours on threat or captureand they are considered part of the normal repertoireof threat or escape behaviours along with avoidanceand aggression. Indeed, in this study urination and/ordefecation during a capture attempt or immediatelyfollowing capture was so widespread throughout thecaptured population that it was not recorded as acapture anomaly. In our study, 68% of animalsvocalised, urinated, defecated or displayedaggression at some stage during capture, transport,processing or release. When presented for clinicalexamination there was no evidence that these animalswere compromised as a result of the capture orhandling process (Table 2), a finding corroborated byCarrick (1996). Secondly, there is no apparentrelationship between the degree of these behavioursand the level of pursuit or progression to exhaustion.

An additional consideration in assessing the needto abandon a capture attempt is the necessity for thatanimal to be captured. A sick animal requiringtreatment or a collared animal requiring collarremoval may have to endure capture attempts untilsuccessful. In these cases, prematurely abandoning acapture attempt in response to normal escapebehaviour such as “crying” or urination mayrepresent a greater hazard to an animal. Repeatedcapture attempts will increase risk of capture-relatedtrauma, may have cumulative effects or lead tocapture aversion rendering the animal “uncatchable”by conventional methods.

In this study, 12% of all attempted captures wereaborted. The frequency actually declined across thestudy as the team became increasingly skilled athandling the idiosyncrasies of the forest and its'koalas. Most of these were terminated because itbecame clear that the attempt would not succeed orbecause the animal proceeded to a precariousposition from which a fall was likely if provoked.Captures were often unsuccessful when both eyes ofthe target animal were affected by conjunctivitis,when impairment of vision resulted in an inability tosee the flag. In these cases the response to the visual

RADFORD ET AL.: KOALA RADIO-COLLAR PROTOCOLS 195

stimulus of the flag was greatly reduced and captureswere rarely successful. No captures were terminatedbecause the animal was beginning to hyperventilate.In our experience the most significant risk to P.cinereus during capture is trauma due to falls orextended leaps. The likelihood of this occurring isdependent on the habitat, the ability of the capturepersonnel to read the animal’s intent, and ambientconditions. Tall, dense, structurally complex forestsprovide many potential escape routes for an animaland increase the likelihood that it will attempt a high-risk escape manoeuvre. High ambient temperaturespredispose animals to hyperthermia, hyperventilationand a loss of coordination, increasing the risk offalling.

Our results show a correlation between ambienttemperature, capture duration and initial core bodytemperature during capture (Fig. 4), and suggest thatwhen ambient temperatures are > 30°C prolongedcapture attempts should be avoided or aborted if theanimal is recalcitrant. At this temperature range,following extended or athletic captures, koalasexhibit elevated core body temperatures (38–40°C)that may necessitate cooling of the animal.

Fig. 4. Linear regression of first core body temperature(CBT) upon capture versus ambient temperature (AMB) andcapture duration.

We suggest that the KRC guidelines be modifiedto exclude urination, vocalisation and defecation asprimary indicators to abort a capture and to includethe following:1) A capture attempt should be aborted if an animal isat risk of falling resulting in injury, or attempts toinappropriately jump in a manner that is likely tocause it injury.2) A capture should be aborted if an animal pantsexcessively and/or displays progressive exhaustion.

3) Capture attempts on animals that fail to displayany normal threat or escape behaviours, such asavoidance, aggression, urination, defecation orvocalisation should proceed with caution and mayneed to be aborted. The lack of these behaviours mayindicate that the animal is sick, injured or otherwisecompromised.4) Capture attempts by flagging when ambienttemperatures are > 30°C should be avoided or shouldbe aborted if the animal fails to descend readily onthe first attempt. If captures are conducted duringhigh ambient temperatures the animal’s core bodytemperature should be monitored and coolingmethods should be on hand.

Monitoring the effects of captureThe capture of any animal will cause it “stress” andone constant field objective is to minimise this effect.There are several problems with this; to ourknowledge there are no reliable objective directindicators of “stress” in P. cinereus and no way ofdetermining a stress threshold beyond which ananimal will be compromised. Is a capture event anymore or less “stressful” to a koala than competitionbetween males or being chased by a predator? Whatare the outcomes for the individual and thepopulation in each case? However, there are indirectindicators that can be used to monitor and minimisepotential detrimental effects of capture. Anysignificant capture-related stressor that is detrimentalto the animal or the population will have an outcomeobservable as increased morbidity, increasedmortality or reduced fecundity and these outcomesshould be spatio-temporally linked to the captureevent. In this study we monitored a range ofindicators that we considered might reflect the levelsof “stress” associated with capture. These included;capture duration, capture-related injury, capture-related mortality, respiratory rate and CBT onpresentation, haematology and serum CK. Resultsshowed nine animals with small cuts or bruisingassociated with capture (14%); three mortalitieswithin 12 weeks post capture due to predation,chlamydiosis or leukaemia; no animals with stresshaemograms (neutrophilia, lymphocytopenia andmonocytosis); and six animals with elevated CK(9%). When CK levels for the cohort were examinedthere was no correlation with ambient temperatureand capture duration. Serum CK, an enzyme thatrises in the serum as a result of muscle damage, couldbe used as an indicator of capture-induced damage oran indirect “stress” marker. Findings in this studymay indicate either that; despite its labile nature, CKdoes not rise within the short time period betweencapture and collection of blood, or that the stressesexperienced within this study were insufficient toelevate the levels of CK in the blood serum. Further

y = x + 5E-11R2 = 0.2457

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35

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35.4 36.4 37.4

Predicted Y

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work on these parameters will clarify the reliabilityof these markers in capture programs.

While immediate capture-related effects onanimals are relatively easy to monitor, the questionremains as to whether a capture event stresses ananimal in some ill-defined way that may result in adelayed morbidity or mortality. This is a much moredifficult question to address although it could beexamined epidemiologically given a large enoughsample and enough time. If capture events wereresponsible for such a phenomenon a dose-responsemay be expected, with a negative correlation betweencapture duration/difficulty (or capture frequency)and post-capture survival and possibly a negativetrend in condition scores post-capture. If animmunosuppressive mechanism were operating, anincrease in the prevalence of infectious disease ortumours between the start and end of a captureproject might also be expected. If standardisedassessment and monitoring protocols are moreuniversally adopted then it may be possible in thefuture to pool data from a number of capture projectsto effect a sample size that would support this type ofanalysis.

Capture methodsThe use of a fixed trap to catch P. cinereus is notaddressed in the KRC Protocols. Hasegawa andCarrick (1995) described this method and itsapplication. In this study we used a trap three times,with a 67% success rate, and detected no detrimentaleffects on subsequent examination of animalscaptured by this method. Indeed the issues of trauma,over-exertion, hyperventilation, progressiveincoordination and exhaustion were non-existent withthis method in this small sample. Its shortcomingshowever include its limited application to appropriatetrees and the fact that most animals are trapped atnight, which entails added logistic complexity ifanimals are to be processed and released in a timelyfashion. We propose its inclusion in the guidelines asan adjunct capture method that is ethical, nontraumatic and particularly useful in those cases wherethere is urgency to catch an animal that cannot beflagged. Procedures for ensuring that a trappedanimal is not left unattended for long periods areeasily applied. Alternate methods for capturingkoalas, such as by darting (Lynch and Martin 2003),have also not been addressed by the KRC protocols,indeed there is little opportunity for exploration ofnovel capture techniques.Processing issuesVeterinary involvement The following are excerpts from the Sections 2 and 4of the current KRC guidelines:

“Veterinarians or veterinary assistants will havespecific responsibilities for invasive procedures.” “A veterinarian (experienced with koalas) must be inattendance whenever gaseous (Isoflurane)anaesthesia is to be used. Either gaseous anaesthesiaor sedation is recommended when invasive samplingis required (eg. Chlamydia swabbing and bloodsampling). Sedation will be sufficient for many suchstudies, rather than full anaesthesia, and is potentiallysafer for procedures such as blood sampling.” “All researchers must have a standing arrangementwith at least one veterinarian experienced in thehandling, assessment, sedation, anaesthesia andtreatment of koalas. If there are no veterinarians withkoala experience resident in the area, the veterinarianmust at least have wildlife experience. Any koalasthat die during the course of a radio-tracking programmust (wherever possible) be subjected to postmortem examination by a veterinarian.” (NSW KoalaResearch Committee 2000).

There are several items here that we believecould be modified as these requirements may act tolimit the acceptance of the protocols they hope toencourage. Firstly, the lack of availability ofexperienced koala or wildlife veterinarians may makethese requirements expensive and logisticallyimpossible. We suggest that anaesthesia, postmortem, blood sampling and many invasivediagnostic procedures could be carried out by anyappropriately-trained field worker. This protocolshould be competence-based rather than degree-based which would remove the necessity for aveterinarian to be present for such procedures. In thelong term this provision would simplify theapplication of these techniques and make them moreaccessible to field workers in general, particularlywith respect to financial expenditure. In this study upto 24% of the annual budget was spent on veterinaryexpenses – nearly $42,000 over the term of the study(Table 3). Similarly, the stipulation that gasanaesthesia must only be carried out by a veterinarianmay severely restrict its use. This may be counter-productive as gas anaesthesia is the least invasive,quickest and safest of the chemical restrainttechniques and may be preferable to sedation orinjectable anaesthesia and could be admissible by acompetent researcher. Finally, the current KRCguidelines do not adequately address the potentialinvasive effects of the anaesthetic proceduresthemselves and the fact that provision for theselimitations should be addressed in the research plan,nor do they address handling procedures in theabsence of anaesthesia for non-invasive procedures.We therefore suggest that the guidelines onanaesthesia, post mortem and invasive procedures bemodified along the following lines:

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Section 2, Research Team“Suitably trained personnel will have specificresponsibilities for the health and welfare of animalsand for carrying out anaesthesia, invasive procedures,assessing the effects of capture on the animal andconducting post mortems. This may includeveterinarians, biologists or research personnelexperienced with the species and trained to carry outthe specific procedures to be performed.”Here we believe the demonstration of competence isthe most important criterion.

Similarly, in Section 4 on veterinary involvementwe suggest the following discussion be incorporated:1) General anaesthesia may be useful to collectdetailed morphometric, physiological, health andreproductive status information from animals as itfacilitates a standardised approach, accuracy andprecision.2) In accordance with standard ACEC guidelines,some form of anaesthesia is a requirement whenpainful or invasive procedures are to be carried out.3) General anaesthesia, applied by gaseous orinjectable agents, or local anaesthesia may be carriedout and supervised by a veterinarian, biologist orresearcher who is appropriately trained and endorsedto use those anaesthetic agents in wildlife.4) Prior experience with koala anaesthesia orconsultation with a veterinarian or biologist withkoala anaesthetic experience is strongly advised askoala anaesthesia may be idiosyncratic.5) Gas anaesthesia using an isoflurane (or relatedagent) /oxygen mix delivered by mask orendotracheal tube is preferable to injectable methodsbecause;a) Almost all of the anaesthetic gas is excreted via thelungs whereas injectable agents are metabolised viathe liver and kidneys. Thus, toxic or hangover-likeeffects are less likely with gas agents.b) Induction and recovery times are shorter with gasagents.c) A gas anaesthetic can be readily controlled andtailored to suit the animal and the procedure beingcarried out.d) The presence of an anaesthetic machine for gasdelivery means that appropriate resuscitationequipment is on hand if required.

6) Whether being used electively or as a requirement,a plan for monitoring and minimising thedisadvantages and potential harmful effects of fieldanaesthesia should be incorporated in the researchplan.

Disadvantages and precautions associated withfield anaesthesia include: a risk of morbidity andmortality associated with the anaesthetic agent

especially in animals with cardiopulmonary, hepaticor renal disease; the turnover time for capture,processing and release may be increased, especially ifinjectable anaesthetic agents or inappropriatetechniques are used; a risk of disease transferbetween animals if appropriate decontamination anddisinfection procedures are not used; anaestheticagents may alter some physiological parameters andanaesthetic baselines need to be determined for theseparameters before interpreting data; anaesthetics anddelivery gases can be hazardous to operators ifcarelessly used; an increase in cost per capture eventfor consumables; and the initial cost, maintenancecost and logistic inconvenience of specialisedequipment. With the exception of initial cost, thedisadvantages and risks associated with anaesthesiacan be minimised by sound theoretical and practicaltraining and a disciplined approach to its use in thefield.

We believe that the use of anaesthesia of any typeis unnecessary in situations where captured animalsare simply tagged, radio-collared and/or assessedvisually for reproductive status and morphologywithout the use of invasive techniques.

Potential effects of intensive handling andprocessingOne issue not clearly addressed by the KRCprotocols is that any capture and handling projectprovides an additional, artificial inter- and intra-species interaction. This may be particularlyimportant when dealing with species that arerelatively solitary and with populations that arepredisposed to infectious disease. If appropriateprotocols are not used, a capture team mayinadvertently act as a disease vector between animalsthat would not normally have contact with theorganism, a possibility exemplified by thetransmission paths of bovine leukaemia virus andequine infectious anaemia virus (Rosenberg andJolicoeur 1997). In practice this means that allsurfaces and instruments that come into contact withkoalas should be replaced or disinfected betweencaptures, and handlers should take appropriatemeasures to ensure that their clothing, hands, traps,flags and transport bags do not transfer materialbetween animals. We propose that the KRCguidelines be modified to include a provision that allresearch plans address this issue in the planningstage.

Radio-telemetry issuesFitting radio-collarsThe KRC Protocols state that diseased, ill or koalasin very poor condition should not be radio-collaredunless approval is specifically given for this in the

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ACEC approval (NSW Koala Research Committee2000). Depending on the definitions of ‘diseased’,‘ill’ and ‘injured’ this requirement, if taken literally,would have precluded almost all animals in thisstudy. In this population, during 1999 there wasa 72% prevalence of Chlamydia bacteria and a44% incidence of symptomatic disease(keratoconjunctivitis), a 90% incidence of chronicotitis externa (inflammation and infection of thepinnae), and several animals were diagnosed withsevere illness after examination of clinical pathologyresults post release. Exclusion of animals on thisbasis effectively nullifies any ability to determineactual causes of mortality in a population, to monitorthe course of disease and determine incidence rates orincubation periods or to determine how diseaseaffects habitat utilisation and population stability.Given that disease status is an importantconsideration for many wild (and captive) P. cinereuspopulations and disease ecology has been identifiedas a research priority (Canfield 1990; Hume 1990;Carrick 1996; Martin and Handasyde 1999), it isdifficult to see the value in selecting for only“healthy animals in a tracking study”, particularly inthe absence of any evidence that collaring ill animalsis universally detrimental. Interestingly, a separate 2-year radio-tracking study was conducted in parallelwith this project in adjacent habitat. In the secondstudy the researchers elected to maximise collar timein the field and hence collared only those animalsidentified as ‘healthy’ by prior clinical examination.At the conclusion of both projects the observedmortality rates in each study were 14% per annum forthe study where no selection was applied and 23%per annum where collar selection for healthy animalsonly was applied (B. Ryan, pers. comm.) indicatingthat apparently healthy animals are still susceptible tofatal disease and misadventure. The second study wascentred on the forest immediately adjacent to thePacific Highway bisecting the forest and a number oftheir mortalities were the result of motor vehicleaccidents. The non road-accident rates for each studywere 14% and 15%, respectively (B. Ryan, pers.comm.). This suggests that collaring apparentlyunhealthy animals does not prejudice survival. Wesuggest an alternative guideline:1) that collars should not be fitted to animals thatmay be adversely affected by carrying a collar, suchas those with injuries or abnormalities associatedwith the neck or those whose behaviour or conditionsuggest that a collar burden would be detrimental.2) this decision is probably best assessed on site bythe project officer responsible for the health andwelfare of the animals after reviewing all availableinformation about an animal.

Frequency of radio-trackingThe experience gained through this study is thatweekly radio-tracking should not necessarily be aprescription for all studies, depending on theparticular research question(s). Some studies may bebetter served by intensive tracking periods of up to amonth or more, followed by extended periodswithout tracking of one month or more. Thejustification for ongoing intensive radio-trackingappears to be largely based on the collection ofmortality information should a collared animal die. Itis our experience that the information required toestimate cause of death can only realistically becollected within a short period of time i.e., beforenecrosis begins to alter organ appearance. A goodalternative here would be to use mortality indicatorsbuilt into the transmitter, in combination with regularsignal monitoring to supplement tracking andsighting at wider intervals. This would decrease thetracking work required but increase the likelihood ofdetecting lack of movement associated withmorbidity and cause of death. The KRC Protocolsdescribe the value of a necropsy examination severaldays post mortem as providing information regardingage and sex (NSW Koala Research Committee 2000).However, if the study animal has previously beencaught in a radio-collaring program, this informationshould already have been collected. Therefore, theloss of information after 24-48 h post-mortem wouldindicate that there is little difference betweentracking fortnightly or monthly, for example. TheKRC Protocols also provide a lesser trackingfrequency for recaptures (NSW Koala ResearchCommittee 2000). This frequency is of alternate daysfor two weeks then a return to their previous trackingfrequency (weekly or fortnightly). If this is suitablefor recaptures, and the most significant reason forintensive tracking periods is to monitor impacts ofanaesthesia and collar deployment, then this wouldlikewise be all that is necessary for initial capturesalso. A frequency recommended from theexperiences of this study would be:1) track and visually inspect each animal on the dayfollowing capture and collaring and on each of thenext few subsequent days, at least twice within thenext week, followed by whatever frequency isrequired by the research question.2) assessment of movement patterns and habitat usesuch as animal height relative to tree height andextent of cryptic behaviour must be undertaken at arange of times since capture.

An assessment of movement patterns and habitatuse would elucidate the impacts of capture on thesevariables and may contribute to detecting a decrease

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in a koala’s health status in sufficient time to allowfor recapture and potential treatment.

The tracking intensity required by the KRCProtocols (NSW Koala Research Committee 2000)will likely result in a decrease in the number ofanimals tracked at any one time and therefore greatlyinfluence the overall sample size of the study. Thismay be particularly important for experimentalstudies requiring treatment replication, such as thoseattempting to assess the impacts of managementactivities, including timber harvesting and otherforestry operations. In this study, each trackinglocation was approximately 1 h in duration due to thecomplexity of the habitat and height of the forest,resulting in slow progress of the radio-tracker anddifficulties associated with sighting collared koalas.This limited the number of koalas to 8-10 that couldbe tracked per day. With koalas needing to be trackeddaily post-capture for an extended period of time, themaximum number of animals able to be radio-trackedin accordance with protocols would be 8-10(depending on habitat conditions and geographicalspread of tagged animals) unless extra support wasavailable during the intensive post-capture trackingperiod, a potentially expensive alternative. Over$6,200 was spent in this study on additional supportfor post-capture radio-tracking (Table 3) during thecapture session, as the primary investigators wereoccupied with the capture process. This number isbelow that required to ensure adequate replication oftreatments within most studies. By staggering thecapture sessions, in combination with a decreasedtracking frequency, it may be possible to incorporatea much larger sample of animals in radio-trackingstudies. Any greater frequency of radio-tracking thanthat suggested above will result in major limitationsto the scope of projects. This was the case in thisproject where habitat assessment was unable to beundertaken until radio-tracking had virtually ceased.Projects undertaken in simpler habitats withdecreased time required per tracking event wouldenjoy more flexibility in tracking frequency.However, this should not be justification for settingsuch a high baseline.

Chronology of research permit approvalsThe permit and ethics approval process for this studywas exceptionally arduous, extending from theproject’s conception in 1998 until its completion in2002. The KRC Protocols were established, in part,as a means to protect koala researchers from thevagaries of the political environment surroundingtheir study animal. This was largely unsuccessful forthis study, most clearly seen in the 2002 applicationfor renewal of permits. The final permit renewalapplication was submitted to NPWS in February2002. This submission involved no changes to any

protocols and only one koala remained collared andin need of capture for collar removal in May 2002 tocomplete the study. This renewal was not granteduntil June 2002, by which time, for animal ethicsreasons, the koala had already been caught, the collarremoved, and the animal released.

It is imperative that the process of review ofresearch permits and ethics applications be addressedmore stringently so that researchers working on thisspecies are not discriminated against. Extendedreview times for applications may prevent applicationfor, or acceptance of, grant funds and enrolment ofstudents, limiting further research on this species. Fora species such as P. cinereus, which is identified asthreatened in some parts of its range and over-abundant in southern parts, any procedures thatunnecessarily limit research into its ecology could bedetrimental to the ecosystems which it inhabits.

ConclusionThe highly political profile of P. cinereus leaves itsresearchers susceptible to scrutiny, bias andpersecution. Research protocols to protect the healthand well-being of threatened species or populationsare also a necessary adjunct to ecological research. Itis critical, however, that these protocols are based onsound physiological and ecological knowledge. P.cinereus is a large and robust animal. Furthermore,we should be aware that the political climatesurrounding icon species, such as P. cinereus, has thepotential to unfairly restrict the activities ofresponsible and approved research programs and torender them impossible to undertake on the basis ofthe excessive costs that may be incurred to justify itscontinuance. The KRC Protocols are a strong step inthe protection of koalas as research subjects and theirresearchers in research protocol implementation.However, they are limited by their restrictive andprescriptive nature. It is hoped that they will beavailable for review and improvement as a result oftheir widespread implementation. This study is wellplaced to undertake the first review of theseProtocols, as this was the first implementation ofthem in a field-based investigation of P. cinereuspopulation dynamics and disease ecology. Webelieve that our combined experiences and findingscontribute significantly to this discussion as theyprovide evidence for many aspects of the Protocolsand highlight areas to be improved.

ACKNOWLEDGMENTSThe authors wish to thank and acknowledge theefforts of the catching team, especially Graeme Lloydand Kevin Glover, and the Veterinary Team,including Jon Hanger and Debbie Lloyd. Without thecontinued efforts and support of these people therewould have been no koalas caught and no project

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conducted. They suffered considerable personal costsfor the sake of this project and we thank themimmensely for their efforts and dedication. Weacknowledge the financial support of SFNSW for thesubstantive costs of the project and the contributionsof Southern Cross University School ofEnvironmental Science and Management and theLinnean Society. We also thank the SFNSW NorthCoast Ecology Team, including Paul Meek, AnnaLloyd, Nick Corkish, Brian Tolhurst, Jason Haydock,Garry Sticker, Jamie Bertram and Terry Tweedie, fortheir assistance during the study.

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