Techniques for tracking amphibians: The effects of tag attachment, and harmonic direction finding...
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Amphibia-Reptilia 28 (2007): 367-376 Techniques for tracking amphibians: The effects of tag attachment, and harmonic direction finding versus radio telemetry Jodi J.L. Rowley ∗ , Ross A. Alford Abstract. To gain information on the microhabitat use, home range and movement of a species, it is often necessary to remotely track individuals in the field. Radio telemetry is commonly used to track amphibians, but can only be used on relatively large individuals. Harmonic direction finding can be used to track smaller animals, but its effectiveness has not been fully evaluated. Tag attachment can alter the behaviour of amphibians, suggesting that data obtained using either technique may be unreliable. We investigated the effects of external tag attachment on behaviour in the laboratory by observing 12 frogs for five nights before and five nights after tag attachment, allowing one night to recover from handling. Tag attachment did not affect distance moved or number of times moved, indicating that the effects of tag attachment are unlikely to persist after the first night following attachment. We then compared harmonic direction finding and radio-telemetry using data collected in the field. We fitted rainforest stream frogs of three species with tags of either type, located them diurnally and nocturnally for approximately two weeks, and compared movement parameters between techniques. In the field, we obtained fewer fixes on frogs using harmonic direction finding, but measures of movement and habitat use did not differ significantly between techniques. Because radio telemetry makes it possible to locate animals more consistently, it should be preferred for animals large enough to carry radio tags. If harmonic direction finding is necessary, it can produce reliable data, particularly for relatively sedentary species. Introduction Information on the spatial behaviour and move- ment patterns of individuals is necessary for a complete understanding of species’ ecology. For most amphibian species, patterns of move- ment and habitat use are poorly known, espe- cially in habitat away from breeding sites. One of the most valuable techniques for gaining in- formation on the microhabitat use, home range and movement of a species is remotely tracking individuals in the field. The most commonly used method to track amphibians is radio telemetry, but this technique suffers two major drawbacks. Firstly, while the size and weight of radio transmitters have de- creased considerably over time, they are still too heavy to attach to small species or individ- uals. The lightest commercially available trans- mitters weigh approximately 0.7 g when pack- aged and ready for attachment. If the rule that School of Marine and Tropical Biology, James Cook University, Townsville Queensland, 4811, Australia ∗ Corresponding author; e-mail: Jodi.Rowley@gmail. com animals should carry no more than 10% of their body mass (Richards, Sinsch and Alford, 1994) is followed, the smallest frog that can be radio tracked will weigh 7 g. Other authors have sug- gested a more conservative 5% limit (Kenward, 1987; White and Garrott, 1990), which would preclude tracking animals weighing less than 14 g. Secondly, battery lifetime limits the dura- tion of tracking; this is particularly true for the smallest transmitters (i.e. <1 g), in which bat- teries last for several weeks at most. Another method for remotely tracking small animals is the harmonic direction finder. The harmonic direction finder is a hand-held de- vice that emits a continuous, unmodulated sig- nal that nonlinear conductors, such as diodes, reflect at twice the original wavelength. The harmonic direction finder detects the reflected signal and transforms it to an audible signal. Therefore, if a harmonic tag is attached to a study animal, its location can be determined us- ing a similar technique to that used in radio telemetry. To date, harmonic direction finding has been used on carabid beetles (Mascanzoni and Wallin, 1986; Wallin and Ekbom, 1988; Hockmann et al., 1989; Lövei et al., 1997), © Koninklijke Brill NV, Leiden, 2007. Also available online - www.brill.nl/amre
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Transcript of Techniques for tracking amphibians: The effects of tag attachment, and harmonic direction finding...
Amphibia-Reptilia 28 (2007) 367-376
Techniques for tracking amphibians The effects of tag attachmentand harmonic direction finding versus radio telemetry
Jodi JL Rowleylowast Ross A Alford
Abstract To gain information on the microhabitat use home range and movement of a species it is often necessary toremotely track individuals in the field Radio telemetry is commonly used to track amphibians but can only be used onrelatively large individuals Harmonic direction finding can be used to track smaller animals but its effectiveness has not beenfully evaluated Tag attachment can alter the behaviour of amphibians suggesting that data obtained using either techniquemay be unreliable We investigated the effects of external tag attachment on behaviour in the laboratory by observing 12 frogsfor five nights before and five nights after tag attachment allowing one night to recover from handling Tag attachment didnot affect distance moved or number of times moved indicating that the effects of tag attachment are unlikely to persist afterthe first night following attachment We then compared harmonic direction finding and radio-telemetry using data collectedin the field We fitted rainforest stream frogs of three species with tags of either type located them diurnally and nocturnallyfor approximately two weeks and compared movement parameters between techniques In the field we obtained fewer fixeson frogs using harmonic direction finding but measures of movement and habitat use did not differ significantly betweentechniques Because radio telemetry makes it possible to locate animals more consistently it should be preferred for animalslarge enough to carry radio tags If harmonic direction finding is necessary it can produce reliable data particularly forrelatively sedentary species
Introduction
Information on the spatial behaviour and move-ment patterns of individuals is necessary fora complete understanding of speciesrsquo ecologyFor most amphibian species patterns of move-ment and habitat use are poorly known espe-cially in habitat away from breeding sites Oneof the most valuable techniques for gaining in-formation on the microhabitat use home rangeand movement of a species is remotely trackingindividuals in the field
The most commonly used method to trackamphibians is radio telemetry but this techniquesuffers two major drawbacks Firstly while thesize and weight of radio transmitters have de-creased considerably over time they are stilltoo heavy to attach to small species or individ-uals The lightest commercially available trans-mitters weigh approximately 07 g when pack-aged and ready for attachment If the rule that
School of Marine and Tropical Biology James CookUniversity Townsville Queensland 4811 AustralialowastCorresponding authore-mail JodiRowleygmail com
animals should carry no more than 10 of theirbody mass (Richards Sinsch and Alford 1994)is followed the smallest frog that can be radiotracked will weigh 7 g Other authors have sug-gested a more conservative 5 limit (Kenward1987 White and Garrott 1990) which wouldpreclude tracking animals weighing less than14 g Secondly battery lifetime limits the dura-tion of tracking this is particularly true for thesmallest transmitters (ie lt1 g) in which bat-teries last for several weeks at most
Another method for remotely tracking smallanimals is the harmonic direction finder Theharmonic direction finder is a hand-held de-vice that emits a continuous unmodulated sig-nal that nonlinear conductors such as diodesreflect at twice the original wavelength Theharmonic direction finder detects the reflectedsignal and transforms it to an audible signalTherefore if a harmonic tag is attached to astudy animal its location can be determined us-ing a similar technique to that used in radiotelemetry To date harmonic direction findinghas been used on carabid beetles (Mascanzoniand Wallin 1986 Wallin and Ekbom 1988Hockmann et al 1989 Loumlvei et al 1997)
copy Koninklijke Brill NV Leiden 2007 Also available online - wwwbrillnlamre
368 JJL Rowley RA Alford
snails (Loumlvei et al 1997 Janszligen and Plachter1998 Stringer and Montefiore 2000 StringerParrish and Sherley 2004) insects (Roland etal 1996 Williams Li and Gao 2004) snakes(Webb and Shine 1997 Engelstoft Ovaska andHonkanen 1999) juvenile toads (Leskovar andSinsch 2002 2005) and small hylid frogs (Pel-let et al 2006)
Harmonic direction finding has three mainadvantages over radio telemetry First becausethe harmonic tag needs no battery it can beextremely lightweight (Riley et al 1998) andcan be used on animals as small as bees andmoths (Roland et al 1996) Second it has rel-atively long functional life because it does notrely on a battery for power Tags can there-fore function for as long as they remain at-tached to the animal Third harmonic tags canbe made extremely inexpensively (Langkildeand Alford 2002) which is useful when thereis a high rate of tag loss There are howeverseveral disadvantages to the technique Perhapsthe most obvious of these is that the reflectedsignal from all tags is the same so that indi-vidual tagged animals must be identified in an-other way once they are found This is a parti-cular problem when frogs are detected using theharmonic direction finder but cannot be visu-ally located Further detection range is typicallymuch shorter than for radio telemetry (ie tensof meters versus hundreds of meters Langkildeand Alford 2002) This may be especially truein field sites that are rugged or densely vege-tated because rocky terrain can reflect either orboth of the signals emitted by the detector or thetags and vegetation absorbs radio waves at thefrequencies used (Sizun 2005)
Regardless of technique a major assump-tion of tracking is that the attachment of thetracking device does not influence the behav-iour of the animal (Richards Sinsch and Al-ford 1994) This assumption is difficult to testas it is often impossible to collect comparablebehavioural information from control individu-als in the field There have been a number ofattempts to assess the impact of tracking de-
vices on the behaviour of small animals suchas birds bats and fish but the results of thesestudies have been mixed While some authorshave found no detectable effect of tracking de-vice attachment (Sodhi et al 1991 Neudorfand Pitcher 1997 Powell et al 1998) othershave found marked effects on behaviour such asmovement (Gessaman and Nagy 1988 Bridgerand Booth 2003) Although tracking amphib-ians in the field is increasingly widespread theeffect of tracking device attachment on amphib-ians remains largely unknown Langkilde andAlford (2002) demonstrated that the activitylevels of the adult hylid frogs Litoria lesueuriwere affected by the attachment of tags on thefirst night after their attachment but potentiallong-term effects of tag attachment on anuranbehaviour remain unknown
Our study had two aims First to determinewhether the changes in activity level detectedby Langkilde and Alford (2002) persist afterthe first night following tag attachment usingthe same model species Second to compare ra-dio telemetry and harmonic direction finding interms of both proportion of fixes obtained andmeasures of movement and habitat use by col-lecting data in the field using both techniques ondifferent individuals of three species of rainfor-est stream frogs
Materials and methods
Effect of tracking device attachment on movement
Adult Litoria lesueuri (see next section) were captured inthe field returned to the laboratory on the day of captureand immediately placed into one of the 270 times 130 times 130cm glass terraria used by Langkilde and Alford (2002)They were allowed to acclimate for 24 hours and then theirbehaviour was videotaped for one half hour from 1930 to2200 hours each night for five nights (nights 2-6) They werethen removed from the terrarium and a tag adjusted to weigh5 of their body weight was fitted Tags were constructedusing Germanium diodes (40 V 50 mA Germanium AMDetector Device number 1N60 7 mm long 2 mm diameter)and were fitted to frogs via an elastic waistband Antennaswere made using stainless steel wire and were 13 cm inlength Antenna length was decided on after an extensiveseries of trial-and-error studies in an open study-site Wechose the length that gave the greatest detection range but
Tracking amphibians 369
that did not hinder frog movement For further details ontag assembly see Langkilde and Alford (2002) After beingreturned to the terrarium frogs were allowed to acclimateto the presence of the tag for 24 hours Their behaviour wasthen videotaped as before for the next five nights (nights 8-12) We were able to carry out this experiment on two frogssimultaneously and we replicated it six times on a total ofnine male and three female frogs Because we performed sixtemporal replicates it seems very unlikely that any outsidefactors causing temporal variation in frog behaviour forexample subtle changes in the temperature of the laboratoryor effects of moon phase could be confounded with theeffects of our experimental treatment any such effectsshould appear as noise in the data Videotapes were analysedfollowing the methods of Langkilde and Alford (2002)and summarized behaviour as distance moved (cm) andnumber of times moved totalled across nights 2-6 (beforetag attachment) and nights 8-12 (after tag attachment) Thedata were highly variable and the raw data were stronglyskewed so we transformed both variables to log10(X + 1)before analysis We analysed the differences between days8-12 and 2-6 for each individual using paired-difference t-tests
Comparison of techniques
The study was conducted at five sites all in tropical rain-forests in northern Queensland Australia Birthday CreekPaluma State Forest (146o10prime02primeprimeE 18o58prime54primeprimeS) PythonCreek (145o35primeE 17o46primeS) an unnamed creek (ldquolowerTullyrdquo 145o41primeE 17o48primeS) in Tully Falls Forest Reserve anunnamed creek in Kirrama State Forest (145o52primeE 18o11primeSlsquoKirramarsquo) and Frenchman Creek Wooroonooran NationalPark (145o55primeE 17o20primeS) All sites are relatively undis-turbed rainforest streams The creek beds are composed ofrocks ranging from small pebbles to large boulders (of over10 m in diameter) All streams contained pools and rifflesand in addition most sites contained a number of small (ap-proximately 1-3 m high) waterfalls Two surveys one inthe dry season (May-September) and one in the wet season(October-April) were carried out at each site except Birth-day Creek where only a wet season survey was performedSurveys lasted approximately 16 days
During surveys frogs of three species were tracked theStoney Creek Frog Litoria lesueuri (see below) the GreenEyed Tree Frog Litoria genimaculata and the WaterfallFrog Litoria nannotis All three species are large to me-dium sized hylid frogs (tracked frogs ranged from 42-64 mmsnout-vent-length and 6-29 g in weight) and exhibit sexualsize dimorphism with females larger then males Recentlythe taxonomy of the Litoria lesueuri group has been re-vised (Donnellan and Mahony 2004) Two species L jung-guy and L wilcoxii occur in sympatry in the region mayhybridise and are morphologically indistinguishable (Don-nellan and Mahony 2004) We therefore continue to referto them as Litoria lesueuri Frogs were tracked using radiotelemetry or harmonic direction finding Only frogs weigh-ing more than 11 g were tracked via radio telemetry Ra-dio transmitters were models BD-2N and BD-2NT (Holo-hil Systems Ltd Ontario Canada) they weighed approx-imately 067 g including harness and had a battery life of
approximately 3 weeks The harness was a waistband madeof silicone rubber capillary tubing with an outside diameterof 1 mm Upon attachment the tubing was trimmed so that itencircled the waist of the frog and a fine cotton thread waspassed through the tubing and tied to secure the packageto the frog with excess thread then trimmed This attach-ment approach minimizes restrictions on frog movementand does not produce localized irritation in frogs when fit-ted correctly If the frog cannot be relocated at the end ofthe study the cotton thread will eventually break allowingthe package to fall off Frogs that were too small to be ra-dio tracked and a number of larger frogs were tracked us-ing harmonic direction finding Harmonic tags were con-structed in the same manner as in the laboratory studybut were attached using silicone waistbands The assem-bly weighed approximately 027 g Antennas were paintedwith two bands of colour to allow individual identificationwhen we could visually locate frogs Both types of trackingdevices were fitted in situ and frogs were released at theirpoints of capture after less than five minutes Frogs wearingeither tracking device did not carry harnesses and tags thatweighed more than 6 of their total body weight
Frogs fitted with radio transmitters were tracked usingTelonics TR-4 Tracking Receivers (wet season 2004 only)or Habit Research HR2500 Osprey VHF Receivers with athree-element folding Yagi antennae (AF Antronics WhiteHeath Illinois USA) Frogs fitted with harmonic tags weretracked using a RECCO R5 transmitter-receiver (ReccoRescue Systems Lidingouml Sweden) This system consists ofa hand-held aerial and associated electronics that act as boththe transmitter and receiver Maximum detection range forthe harmonic tags was 40 m (Langkilde and Alford 2002)
We attempted to determine the location of each frogonce during each day (0700-1900) and once each night(1900-0700) during each survey period When using radiotelemetry we began tracking at the location where eachfrog was last found If no signal could be detected at thispoint we walked 300-500 m in each direction away fromthat site trying to reach elevated positions for maximumdetection range If no signal could be picked up after this(15-45 mins depending on terrain and vegetation type) webegan searching for the next frog When using harmonicdirection finding we walked slowly in parallel lines up anddown each side of the stream and approximately 10 m intothe forest on each side of the stream moving the harmonicdirection finding machine at all times making sure to coverall directions (maximising our chances of detecting frogslocated both in the stream and in the canopy) For any frogswe had not yet found (after approximately 1-3 h) we thensearched at and around (20 m radius) the location where itwas last found If no signal could be picked up after this (5-10 mins) we moved on to searching for the next frog Therewere a number of instances where we detected a frog usingharmonic direction finding but could not visually locate andtherefore identify the individual (ie when the frog was inthe canopy) On these instances it was often possible totentatively identify the individual by making the assumptionthat of the frogs not located during that survey it wasthe individual previously located nearest to this locationWe confirmed all such tentative identifications via later
370 JJL Rowley RA Alford
sightings In the process of searching for individual frogswe never noticeably disturbed other tracked frogs primarilydue to the large size of each study site and scattered spatialdistribution of most individuals Although search effort washighly variable from day to day we spent approximatelythe same total number of person-hours using each techniqueduring each survey period
When frogs were located using either technique we re-corded their location as distance along the stream (m) hor-izontal distance from the stream (m) and height abovestream (m) allowing us to calculate their distance movedper day We used these variables because they are impor-tant aspects of the habitat use of amphibians and theycan be compared to determine whether they are differ-entially biased by the tracking technique used To avoidpseudoreplication and biasing our results to frogs that werelocated more often we used individuals as replicates andanalysed means or proportions for each animal Due towell-documented differences in behaviour between sexes(eg Bellis 1965 Dole and Durant 1974 Miaud Sanuyand Avrillier 2000) and our bias towards tracking malesvia harmonic direction finding (due to their smaller bodysize) we performed Mann Whitney tests separately for eachsex and species combination We also examined whetherfrog body weight differed with tracking device for each sexand species combination We used Bonferroni adjustmentsto control Type I error rates Boxplots were used to visu-alise the results In boxplots bold horizontal lines repre-sent the median boxes indicate the locations of upper andlower quartiles bars encompass values up to 15 interquar-tile range open circles represent values more than 15 in-terquartile ranges from the nearest quartile and stars indi-cate data values more than 3 interquartile ranges from thenearest quartile
Results
Effect of tracking device attachmenton movement
Both movement parameters were highly vari-able and changes between nights 2-6 to nights8-12 also varied greatly among individuals(fig 1) For both parameters the median changewas a very slight decline following tag at-tachment (fig 1) however the changes fromnights 2-6 to 8-12 for both movement parame-ters were not significantly different from zero(log10(number of moves) t11 = 0630 P =0542 log10(total distance moved) t11 = 1060P = 0312)
Figure 1 Changes in behaviour expressed as the differencebetween values of log10 of parameters totalled over nights8-12 following capture with tags attached and over nights2-6 following capture with no tags attached Subtracting thevalue for days 2-6 from that for days 8-12 gives figures forchange that are directly related to actual change the neg-ative median for both parameters indicate that in the indi-viduals observed they decreased slightly following tag at-tachment Neither change approaches statistical significance(see text) Bold horizontal lines represent the median boxesindicate the locations of upper and lower quartiles and barsencompass values up to 15 interquartile range
Comparison of techniques
In total 117 frogs were tracked during the study(table 1) Although a greater number of malesand other smaller individuals were tracked viaharmonic direction finding there was no signifi-cant difference in the weight of frogs tracked viaeither method when each species and sex cate-gory was considered separately (table 1) Theproportion of attempts upon which fixes wereobtained differed significantly between track-ing devices for some classes of individuals Weobtained fewer fixes using harmonic directionfinding for L lesueuri and L nannotis femalesbut not for L genimaculata or L nannotis males(table 1 fig 2) Overall while frogs trackedusing radio telemetry were found on averageon 974 of attempts frogs tracked via har-monic direction finding were located on only668 of attempts This varied among speciesL genimaculata were found 854 of the timeusing harmonic direction finding compared to
Tracking amphibians 371
Tabl
e1
Man
nW
hitn
eyte
sts
for
diff
eren
ces
betw
een
harm
onic
dire
ctio
nfin
ding
and
radi
ote
lem
etry
inpr
opor
tions
offix
esob
tain
eda
vera
gedi
stan
cem
oved
per
day
(m)
aver
age
heig
htab
ove
the
stre
am(m
)an
dav
erag
eho
rizo
ntal
dist
ance
from
the
stre
am(m
)
indi
cate
ssi
gnifi
canc
eat
the
Bon
ferr
oni-
adju
sted
005
leve
l
Spec
ies
Sex
Num
ber
ofin
divi
dual
sTe
sts
for
diff
eren
cebe
twee
nra
dio
tele
met
ryan
dha
rmon
icdi
rect
ion
findi
ngin
w
ithea
chta
gty
peFr
ogbo
dyw
eigh
t(g)
Prop
ortio
nof
fixes
Ave
rage
dist
ance
Ave
rage
heig
htab
ove
Ave
rage
hori
zont
alm
oved
per
day
(m)
stre
am(m
)di
stan
cefr
omst
ream
(m)
Rad
ioH
arm
onic
Man
n-P
Man
n-P
Man
n-P
Man
n-P
Man
n-P
tele
met
rydi
rect
ion
Whi
tney
Whi
tney
Whi
tney
Whi
tney
Whi
tney
findi
ngZ
ZZ
ZZ
Lg
enim
acul
ata
Fem
ale
93
minus04
630
710
minus29
70
09minus1
202
028
2minus1
017
037
3minus0
832
048
2M
ale
015
ndashndash
ndashndash
ndashndash
ndashndash
ndash
Ll
esue
uri
Fem
ale
246
minus03
180
765
minus33
080
002
minus09
850
347
minus11
920
251
minus18
670
065
Mal
e7
25minus2
209
002
5minus3
711
lt0
001
minus24
840
011
minus23
020
020
minus12
770
207
Ln
anno
tis
Fem
ale
193
minus11
280
301
minus27
950
001
minus19
610
053
minus05
260
651
minus08
610
408
Mal
e2
4minus1
97
044
0minus1
174
026
7minus0
926
053
3minus0
939
053
3minus0
939
053
3
372 JJL Rowley RA Alford
Figure 2 Mean proportion of fixes obtained (number of fixes divided by total possible number of fixes for each individual)for Litoria genimaculata (LG) L lesueuri and L nannotis (LN) tracked using harmonic direction finding and radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
582 and 577 of the time for L lesueuri andL nannotis respectively In contrast the pro-portion of fixes for each species during radiotelemetry varied less between 952 and 995Compared to radio telemetry harmonic direc-tion finding typically resulted in a lower av-erage distance moved per day lower averageheight above the stream and lower average hori-zontal distance from the stream for the major-ity of species and sex combinations howeverthese differences were not significant (table 1figs 3-5)
Discussion
While the attachment of tracking devices to am-phibians may result in short-term increases inmovement and activity (Langkilde and Alford2002) the results of our laboratory experimentindicate that this effect can disappear within ashort time Comparing the magnitude of varia-tion among individuals with the magnitude ofthe very small median changes (fig 1) suggeststhat any real effects of tag attachment on be-haviour may disappear after individuals havebeen allowed to acclimate for 24 hours or are
so small compared to levels of variation amongindividuals that they are unlikely to affect theusefulness of observations made using attachedtags As long as data for the period immediatelyfollowing tag attachment are discarded it ap-pears that the effects of tags are unlikely to alterthe movement patterns revealed by tracking am-phibians in the field Our observations of the be-haviour of tagged frogs in the field support thisfinding In all species we studied frogs with at-tached tags appeared to be uninhibited in theirmovement were commonly observed in closeassociation with frogs without tags and wereoften observed calling and in amplexus One in-dividual was observed calling less than 12 h af-ter tag attachment In addition frogs with tagsattached maintained their weight over the track-ing period (JJL Rowley and RA Alford un-publ data)
Although our data revealed no persistent ef-fects of tag attachment on the frequency ofmovement and distances moved by L lesueuriin the laboratory effects of tag attachment can-not be ruled out as there may be subtle effectson behaviour that were not investigated hereThere is also a chance that frog behaviour in our
Tracking amphibians 373
Figure 3 Mean distance moved per day for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
Figure 4 Mean height above stream (m) for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
368 JJL Rowley RA Alford
snails (Loumlvei et al 1997 Janszligen and Plachter1998 Stringer and Montefiore 2000 StringerParrish and Sherley 2004) insects (Roland etal 1996 Williams Li and Gao 2004) snakes(Webb and Shine 1997 Engelstoft Ovaska andHonkanen 1999) juvenile toads (Leskovar andSinsch 2002 2005) and small hylid frogs (Pel-let et al 2006)
Harmonic direction finding has three mainadvantages over radio telemetry First becausethe harmonic tag needs no battery it can beextremely lightweight (Riley et al 1998) andcan be used on animals as small as bees andmoths (Roland et al 1996) Second it has rel-atively long functional life because it does notrely on a battery for power Tags can there-fore function for as long as they remain at-tached to the animal Third harmonic tags canbe made extremely inexpensively (Langkildeand Alford 2002) which is useful when thereis a high rate of tag loss There are howeverseveral disadvantages to the technique Perhapsthe most obvious of these is that the reflectedsignal from all tags is the same so that indi-vidual tagged animals must be identified in an-other way once they are found This is a parti-cular problem when frogs are detected using theharmonic direction finder but cannot be visu-ally located Further detection range is typicallymuch shorter than for radio telemetry (ie tensof meters versus hundreds of meters Langkildeand Alford 2002) This may be especially truein field sites that are rugged or densely vege-tated because rocky terrain can reflect either orboth of the signals emitted by the detector or thetags and vegetation absorbs radio waves at thefrequencies used (Sizun 2005)
Regardless of technique a major assump-tion of tracking is that the attachment of thetracking device does not influence the behav-iour of the animal (Richards Sinsch and Al-ford 1994) This assumption is difficult to testas it is often impossible to collect comparablebehavioural information from control individu-als in the field There have been a number ofattempts to assess the impact of tracking de-
vices on the behaviour of small animals suchas birds bats and fish but the results of thesestudies have been mixed While some authorshave found no detectable effect of tracking de-vice attachment (Sodhi et al 1991 Neudorfand Pitcher 1997 Powell et al 1998) othershave found marked effects on behaviour such asmovement (Gessaman and Nagy 1988 Bridgerand Booth 2003) Although tracking amphib-ians in the field is increasingly widespread theeffect of tracking device attachment on amphib-ians remains largely unknown Langkilde andAlford (2002) demonstrated that the activitylevels of the adult hylid frogs Litoria lesueuriwere affected by the attachment of tags on thefirst night after their attachment but potentiallong-term effects of tag attachment on anuranbehaviour remain unknown
Our study had two aims First to determinewhether the changes in activity level detectedby Langkilde and Alford (2002) persist afterthe first night following tag attachment usingthe same model species Second to compare ra-dio telemetry and harmonic direction finding interms of both proportion of fixes obtained andmeasures of movement and habitat use by col-lecting data in the field using both techniques ondifferent individuals of three species of rainfor-est stream frogs
Materials and methods
Effect of tracking device attachment on movement
Adult Litoria lesueuri (see next section) were captured inthe field returned to the laboratory on the day of captureand immediately placed into one of the 270 times 130 times 130cm glass terraria used by Langkilde and Alford (2002)They were allowed to acclimate for 24 hours and then theirbehaviour was videotaped for one half hour from 1930 to2200 hours each night for five nights (nights 2-6) They werethen removed from the terrarium and a tag adjusted to weigh5 of their body weight was fitted Tags were constructedusing Germanium diodes (40 V 50 mA Germanium AMDetector Device number 1N60 7 mm long 2 mm diameter)and were fitted to frogs via an elastic waistband Antennaswere made using stainless steel wire and were 13 cm inlength Antenna length was decided on after an extensiveseries of trial-and-error studies in an open study-site Wechose the length that gave the greatest detection range but
Tracking amphibians 369
that did not hinder frog movement For further details ontag assembly see Langkilde and Alford (2002) After beingreturned to the terrarium frogs were allowed to acclimateto the presence of the tag for 24 hours Their behaviour wasthen videotaped as before for the next five nights (nights 8-12) We were able to carry out this experiment on two frogssimultaneously and we replicated it six times on a total ofnine male and three female frogs Because we performed sixtemporal replicates it seems very unlikely that any outsidefactors causing temporal variation in frog behaviour forexample subtle changes in the temperature of the laboratoryor effects of moon phase could be confounded with theeffects of our experimental treatment any such effectsshould appear as noise in the data Videotapes were analysedfollowing the methods of Langkilde and Alford (2002)and summarized behaviour as distance moved (cm) andnumber of times moved totalled across nights 2-6 (beforetag attachment) and nights 8-12 (after tag attachment) Thedata were highly variable and the raw data were stronglyskewed so we transformed both variables to log10(X + 1)before analysis We analysed the differences between days8-12 and 2-6 for each individual using paired-difference t-tests
Comparison of techniques
The study was conducted at five sites all in tropical rain-forests in northern Queensland Australia Birthday CreekPaluma State Forest (146o10prime02primeprimeE 18o58prime54primeprimeS) PythonCreek (145o35primeE 17o46primeS) an unnamed creek (ldquolowerTullyrdquo 145o41primeE 17o48primeS) in Tully Falls Forest Reserve anunnamed creek in Kirrama State Forest (145o52primeE 18o11primeSlsquoKirramarsquo) and Frenchman Creek Wooroonooran NationalPark (145o55primeE 17o20primeS) All sites are relatively undis-turbed rainforest streams The creek beds are composed ofrocks ranging from small pebbles to large boulders (of over10 m in diameter) All streams contained pools and rifflesand in addition most sites contained a number of small (ap-proximately 1-3 m high) waterfalls Two surveys one inthe dry season (May-September) and one in the wet season(October-April) were carried out at each site except Birth-day Creek where only a wet season survey was performedSurveys lasted approximately 16 days
During surveys frogs of three species were tracked theStoney Creek Frog Litoria lesueuri (see below) the GreenEyed Tree Frog Litoria genimaculata and the WaterfallFrog Litoria nannotis All three species are large to me-dium sized hylid frogs (tracked frogs ranged from 42-64 mmsnout-vent-length and 6-29 g in weight) and exhibit sexualsize dimorphism with females larger then males Recentlythe taxonomy of the Litoria lesueuri group has been re-vised (Donnellan and Mahony 2004) Two species L jung-guy and L wilcoxii occur in sympatry in the region mayhybridise and are morphologically indistinguishable (Don-nellan and Mahony 2004) We therefore continue to referto them as Litoria lesueuri Frogs were tracked using radiotelemetry or harmonic direction finding Only frogs weigh-ing more than 11 g were tracked via radio telemetry Ra-dio transmitters were models BD-2N and BD-2NT (Holo-hil Systems Ltd Ontario Canada) they weighed approx-imately 067 g including harness and had a battery life of
approximately 3 weeks The harness was a waistband madeof silicone rubber capillary tubing with an outside diameterof 1 mm Upon attachment the tubing was trimmed so that itencircled the waist of the frog and a fine cotton thread waspassed through the tubing and tied to secure the packageto the frog with excess thread then trimmed This attach-ment approach minimizes restrictions on frog movementand does not produce localized irritation in frogs when fit-ted correctly If the frog cannot be relocated at the end ofthe study the cotton thread will eventually break allowingthe package to fall off Frogs that were too small to be ra-dio tracked and a number of larger frogs were tracked us-ing harmonic direction finding Harmonic tags were con-structed in the same manner as in the laboratory studybut were attached using silicone waistbands The assem-bly weighed approximately 027 g Antennas were paintedwith two bands of colour to allow individual identificationwhen we could visually locate frogs Both types of trackingdevices were fitted in situ and frogs were released at theirpoints of capture after less than five minutes Frogs wearingeither tracking device did not carry harnesses and tags thatweighed more than 6 of their total body weight
Frogs fitted with radio transmitters were tracked usingTelonics TR-4 Tracking Receivers (wet season 2004 only)or Habit Research HR2500 Osprey VHF Receivers with athree-element folding Yagi antennae (AF Antronics WhiteHeath Illinois USA) Frogs fitted with harmonic tags weretracked using a RECCO R5 transmitter-receiver (ReccoRescue Systems Lidingouml Sweden) This system consists ofa hand-held aerial and associated electronics that act as boththe transmitter and receiver Maximum detection range forthe harmonic tags was 40 m (Langkilde and Alford 2002)
We attempted to determine the location of each frogonce during each day (0700-1900) and once each night(1900-0700) during each survey period When using radiotelemetry we began tracking at the location where eachfrog was last found If no signal could be detected at thispoint we walked 300-500 m in each direction away fromthat site trying to reach elevated positions for maximumdetection range If no signal could be picked up after this(15-45 mins depending on terrain and vegetation type) webegan searching for the next frog When using harmonicdirection finding we walked slowly in parallel lines up anddown each side of the stream and approximately 10 m intothe forest on each side of the stream moving the harmonicdirection finding machine at all times making sure to coverall directions (maximising our chances of detecting frogslocated both in the stream and in the canopy) For any frogswe had not yet found (after approximately 1-3 h) we thensearched at and around (20 m radius) the location where itwas last found If no signal could be picked up after this (5-10 mins) we moved on to searching for the next frog Therewere a number of instances where we detected a frog usingharmonic direction finding but could not visually locate andtherefore identify the individual (ie when the frog was inthe canopy) On these instances it was often possible totentatively identify the individual by making the assumptionthat of the frogs not located during that survey it wasthe individual previously located nearest to this locationWe confirmed all such tentative identifications via later
370 JJL Rowley RA Alford
sightings In the process of searching for individual frogswe never noticeably disturbed other tracked frogs primarilydue to the large size of each study site and scattered spatialdistribution of most individuals Although search effort washighly variable from day to day we spent approximatelythe same total number of person-hours using each techniqueduring each survey period
When frogs were located using either technique we re-corded their location as distance along the stream (m) hor-izontal distance from the stream (m) and height abovestream (m) allowing us to calculate their distance movedper day We used these variables because they are impor-tant aspects of the habitat use of amphibians and theycan be compared to determine whether they are differ-entially biased by the tracking technique used To avoidpseudoreplication and biasing our results to frogs that werelocated more often we used individuals as replicates andanalysed means or proportions for each animal Due towell-documented differences in behaviour between sexes(eg Bellis 1965 Dole and Durant 1974 Miaud Sanuyand Avrillier 2000) and our bias towards tracking malesvia harmonic direction finding (due to their smaller bodysize) we performed Mann Whitney tests separately for eachsex and species combination We also examined whetherfrog body weight differed with tracking device for each sexand species combination We used Bonferroni adjustmentsto control Type I error rates Boxplots were used to visu-alise the results In boxplots bold horizontal lines repre-sent the median boxes indicate the locations of upper andlower quartiles bars encompass values up to 15 interquar-tile range open circles represent values more than 15 in-terquartile ranges from the nearest quartile and stars indi-cate data values more than 3 interquartile ranges from thenearest quartile
Results
Effect of tracking device attachmenton movement
Both movement parameters were highly vari-able and changes between nights 2-6 to nights8-12 also varied greatly among individuals(fig 1) For both parameters the median changewas a very slight decline following tag at-tachment (fig 1) however the changes fromnights 2-6 to 8-12 for both movement parame-ters were not significantly different from zero(log10(number of moves) t11 = 0630 P =0542 log10(total distance moved) t11 = 1060P = 0312)
Figure 1 Changes in behaviour expressed as the differencebetween values of log10 of parameters totalled over nights8-12 following capture with tags attached and over nights2-6 following capture with no tags attached Subtracting thevalue for days 2-6 from that for days 8-12 gives figures forchange that are directly related to actual change the neg-ative median for both parameters indicate that in the indi-viduals observed they decreased slightly following tag at-tachment Neither change approaches statistical significance(see text) Bold horizontal lines represent the median boxesindicate the locations of upper and lower quartiles and barsencompass values up to 15 interquartile range
Comparison of techniques
In total 117 frogs were tracked during the study(table 1) Although a greater number of malesand other smaller individuals were tracked viaharmonic direction finding there was no signifi-cant difference in the weight of frogs tracked viaeither method when each species and sex cate-gory was considered separately (table 1) Theproportion of attempts upon which fixes wereobtained differed significantly between track-ing devices for some classes of individuals Weobtained fewer fixes using harmonic directionfinding for L lesueuri and L nannotis femalesbut not for L genimaculata or L nannotis males(table 1 fig 2) Overall while frogs trackedusing radio telemetry were found on averageon 974 of attempts frogs tracked via har-monic direction finding were located on only668 of attempts This varied among speciesL genimaculata were found 854 of the timeusing harmonic direction finding compared to
Tracking amphibians 371
Tabl
e1
Man
nW
hitn
eyte
sts
for
diff
eren
ces
betw
een
harm
onic
dire
ctio
nfin
ding
and
radi
ote
lem
etry
inpr
opor
tions
offix
esob
tain
eda
vera
gedi
stan
cem
oved
per
day
(m)
aver
age
heig
htab
ove
the
stre
am(m
)an
dav
erag
eho
rizo
ntal
dist
ance
from
the
stre
am(m
)
indi
cate
ssi
gnifi
canc
eat
the
Bon
ferr
oni-
adju
sted
005
leve
l
Spec
ies
Sex
Num
ber
ofin
divi
dual
sTe
sts
for
diff
eren
cebe
twee
nra
dio
tele
met
ryan
dha
rmon
icdi
rect
ion
findi
ngin
w
ithea
chta
gty
peFr
ogbo
dyw
eigh
t(g)
Prop
ortio
nof
fixes
Ave
rage
dist
ance
Ave
rage
heig
htab
ove
Ave
rage
hori
zont
alm
oved
per
day
(m)
stre
am(m
)di
stan
cefr
omst
ream
(m)
Rad
ioH
arm
onic
Man
n-P
Man
n-P
Man
n-P
Man
n-P
Man
n-P
tele
met
rydi
rect
ion
Whi
tney
Whi
tney
Whi
tney
Whi
tney
Whi
tney
findi
ngZ
ZZ
ZZ
Lg
enim
acul
ata
Fem
ale
93
minus04
630
710
minus29
70
09minus1
202
028
2minus1
017
037
3minus0
832
048
2M
ale
015
ndashndash
ndashndash
ndashndash
ndashndash
ndash
Ll
esue
uri
Fem
ale
246
minus03
180
765
minus33
080
002
minus09
850
347
minus11
920
251
minus18
670
065
Mal
e7
25minus2
209
002
5minus3
711
lt0
001
minus24
840
011
minus23
020
020
minus12
770
207
Ln
anno
tis
Fem
ale
193
minus11
280
301
minus27
950
001
minus19
610
053
minus05
260
651
minus08
610
408
Mal
e2
4minus1
97
044
0minus1
174
026
7minus0
926
053
3minus0
939
053
3minus0
939
053
3
372 JJL Rowley RA Alford
Figure 2 Mean proportion of fixes obtained (number of fixes divided by total possible number of fixes for each individual)for Litoria genimaculata (LG) L lesueuri and L nannotis (LN) tracked using harmonic direction finding and radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
582 and 577 of the time for L lesueuri andL nannotis respectively In contrast the pro-portion of fixes for each species during radiotelemetry varied less between 952 and 995Compared to radio telemetry harmonic direc-tion finding typically resulted in a lower av-erage distance moved per day lower averageheight above the stream and lower average hori-zontal distance from the stream for the major-ity of species and sex combinations howeverthese differences were not significant (table 1figs 3-5)
Discussion
While the attachment of tracking devices to am-phibians may result in short-term increases inmovement and activity (Langkilde and Alford2002) the results of our laboratory experimentindicate that this effect can disappear within ashort time Comparing the magnitude of varia-tion among individuals with the magnitude ofthe very small median changes (fig 1) suggeststhat any real effects of tag attachment on be-haviour may disappear after individuals havebeen allowed to acclimate for 24 hours or are
so small compared to levels of variation amongindividuals that they are unlikely to affect theusefulness of observations made using attachedtags As long as data for the period immediatelyfollowing tag attachment are discarded it ap-pears that the effects of tags are unlikely to alterthe movement patterns revealed by tracking am-phibians in the field Our observations of the be-haviour of tagged frogs in the field support thisfinding In all species we studied frogs with at-tached tags appeared to be uninhibited in theirmovement were commonly observed in closeassociation with frogs without tags and wereoften observed calling and in amplexus One in-dividual was observed calling less than 12 h af-ter tag attachment In addition frogs with tagsattached maintained their weight over the track-ing period (JJL Rowley and RA Alford un-publ data)
Although our data revealed no persistent ef-fects of tag attachment on the frequency ofmovement and distances moved by L lesueuriin the laboratory effects of tag attachment can-not be ruled out as there may be subtle effectson behaviour that were not investigated hereThere is also a chance that frog behaviour in our
Tracking amphibians 373
Figure 3 Mean distance moved per day for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
Figure 4 Mean height above stream (m) for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
Tracking amphibians 369
that did not hinder frog movement For further details ontag assembly see Langkilde and Alford (2002) After beingreturned to the terrarium frogs were allowed to acclimateto the presence of the tag for 24 hours Their behaviour wasthen videotaped as before for the next five nights (nights 8-12) We were able to carry out this experiment on two frogssimultaneously and we replicated it six times on a total ofnine male and three female frogs Because we performed sixtemporal replicates it seems very unlikely that any outsidefactors causing temporal variation in frog behaviour forexample subtle changes in the temperature of the laboratoryor effects of moon phase could be confounded with theeffects of our experimental treatment any such effectsshould appear as noise in the data Videotapes were analysedfollowing the methods of Langkilde and Alford (2002)and summarized behaviour as distance moved (cm) andnumber of times moved totalled across nights 2-6 (beforetag attachment) and nights 8-12 (after tag attachment) Thedata were highly variable and the raw data were stronglyskewed so we transformed both variables to log10(X + 1)before analysis We analysed the differences between days8-12 and 2-6 for each individual using paired-difference t-tests
Comparison of techniques
The study was conducted at five sites all in tropical rain-forests in northern Queensland Australia Birthday CreekPaluma State Forest (146o10prime02primeprimeE 18o58prime54primeprimeS) PythonCreek (145o35primeE 17o46primeS) an unnamed creek (ldquolowerTullyrdquo 145o41primeE 17o48primeS) in Tully Falls Forest Reserve anunnamed creek in Kirrama State Forest (145o52primeE 18o11primeSlsquoKirramarsquo) and Frenchman Creek Wooroonooran NationalPark (145o55primeE 17o20primeS) All sites are relatively undis-turbed rainforest streams The creek beds are composed ofrocks ranging from small pebbles to large boulders (of over10 m in diameter) All streams contained pools and rifflesand in addition most sites contained a number of small (ap-proximately 1-3 m high) waterfalls Two surveys one inthe dry season (May-September) and one in the wet season(October-April) were carried out at each site except Birth-day Creek where only a wet season survey was performedSurveys lasted approximately 16 days
During surveys frogs of three species were tracked theStoney Creek Frog Litoria lesueuri (see below) the GreenEyed Tree Frog Litoria genimaculata and the WaterfallFrog Litoria nannotis All three species are large to me-dium sized hylid frogs (tracked frogs ranged from 42-64 mmsnout-vent-length and 6-29 g in weight) and exhibit sexualsize dimorphism with females larger then males Recentlythe taxonomy of the Litoria lesueuri group has been re-vised (Donnellan and Mahony 2004) Two species L jung-guy and L wilcoxii occur in sympatry in the region mayhybridise and are morphologically indistinguishable (Don-nellan and Mahony 2004) We therefore continue to referto them as Litoria lesueuri Frogs were tracked using radiotelemetry or harmonic direction finding Only frogs weigh-ing more than 11 g were tracked via radio telemetry Ra-dio transmitters were models BD-2N and BD-2NT (Holo-hil Systems Ltd Ontario Canada) they weighed approx-imately 067 g including harness and had a battery life of
approximately 3 weeks The harness was a waistband madeof silicone rubber capillary tubing with an outside diameterof 1 mm Upon attachment the tubing was trimmed so that itencircled the waist of the frog and a fine cotton thread waspassed through the tubing and tied to secure the packageto the frog with excess thread then trimmed This attach-ment approach minimizes restrictions on frog movementand does not produce localized irritation in frogs when fit-ted correctly If the frog cannot be relocated at the end ofthe study the cotton thread will eventually break allowingthe package to fall off Frogs that were too small to be ra-dio tracked and a number of larger frogs were tracked us-ing harmonic direction finding Harmonic tags were con-structed in the same manner as in the laboratory studybut were attached using silicone waistbands The assem-bly weighed approximately 027 g Antennas were paintedwith two bands of colour to allow individual identificationwhen we could visually locate frogs Both types of trackingdevices were fitted in situ and frogs were released at theirpoints of capture after less than five minutes Frogs wearingeither tracking device did not carry harnesses and tags thatweighed more than 6 of their total body weight
Frogs fitted with radio transmitters were tracked usingTelonics TR-4 Tracking Receivers (wet season 2004 only)or Habit Research HR2500 Osprey VHF Receivers with athree-element folding Yagi antennae (AF Antronics WhiteHeath Illinois USA) Frogs fitted with harmonic tags weretracked using a RECCO R5 transmitter-receiver (ReccoRescue Systems Lidingouml Sweden) This system consists ofa hand-held aerial and associated electronics that act as boththe transmitter and receiver Maximum detection range forthe harmonic tags was 40 m (Langkilde and Alford 2002)
We attempted to determine the location of each frogonce during each day (0700-1900) and once each night(1900-0700) during each survey period When using radiotelemetry we began tracking at the location where eachfrog was last found If no signal could be detected at thispoint we walked 300-500 m in each direction away fromthat site trying to reach elevated positions for maximumdetection range If no signal could be picked up after this(15-45 mins depending on terrain and vegetation type) webegan searching for the next frog When using harmonicdirection finding we walked slowly in parallel lines up anddown each side of the stream and approximately 10 m intothe forest on each side of the stream moving the harmonicdirection finding machine at all times making sure to coverall directions (maximising our chances of detecting frogslocated both in the stream and in the canopy) For any frogswe had not yet found (after approximately 1-3 h) we thensearched at and around (20 m radius) the location where itwas last found If no signal could be picked up after this (5-10 mins) we moved on to searching for the next frog Therewere a number of instances where we detected a frog usingharmonic direction finding but could not visually locate andtherefore identify the individual (ie when the frog was inthe canopy) On these instances it was often possible totentatively identify the individual by making the assumptionthat of the frogs not located during that survey it wasthe individual previously located nearest to this locationWe confirmed all such tentative identifications via later
370 JJL Rowley RA Alford
sightings In the process of searching for individual frogswe never noticeably disturbed other tracked frogs primarilydue to the large size of each study site and scattered spatialdistribution of most individuals Although search effort washighly variable from day to day we spent approximatelythe same total number of person-hours using each techniqueduring each survey period
When frogs were located using either technique we re-corded their location as distance along the stream (m) hor-izontal distance from the stream (m) and height abovestream (m) allowing us to calculate their distance movedper day We used these variables because they are impor-tant aspects of the habitat use of amphibians and theycan be compared to determine whether they are differ-entially biased by the tracking technique used To avoidpseudoreplication and biasing our results to frogs that werelocated more often we used individuals as replicates andanalysed means or proportions for each animal Due towell-documented differences in behaviour between sexes(eg Bellis 1965 Dole and Durant 1974 Miaud Sanuyand Avrillier 2000) and our bias towards tracking malesvia harmonic direction finding (due to their smaller bodysize) we performed Mann Whitney tests separately for eachsex and species combination We also examined whetherfrog body weight differed with tracking device for each sexand species combination We used Bonferroni adjustmentsto control Type I error rates Boxplots were used to visu-alise the results In boxplots bold horizontal lines repre-sent the median boxes indicate the locations of upper andlower quartiles bars encompass values up to 15 interquar-tile range open circles represent values more than 15 in-terquartile ranges from the nearest quartile and stars indi-cate data values more than 3 interquartile ranges from thenearest quartile
Results
Effect of tracking device attachmenton movement
Both movement parameters were highly vari-able and changes between nights 2-6 to nights8-12 also varied greatly among individuals(fig 1) For both parameters the median changewas a very slight decline following tag at-tachment (fig 1) however the changes fromnights 2-6 to 8-12 for both movement parame-ters were not significantly different from zero(log10(number of moves) t11 = 0630 P =0542 log10(total distance moved) t11 = 1060P = 0312)
Figure 1 Changes in behaviour expressed as the differencebetween values of log10 of parameters totalled over nights8-12 following capture with tags attached and over nights2-6 following capture with no tags attached Subtracting thevalue for days 2-6 from that for days 8-12 gives figures forchange that are directly related to actual change the neg-ative median for both parameters indicate that in the indi-viduals observed they decreased slightly following tag at-tachment Neither change approaches statistical significance(see text) Bold horizontal lines represent the median boxesindicate the locations of upper and lower quartiles and barsencompass values up to 15 interquartile range
Comparison of techniques
In total 117 frogs were tracked during the study(table 1) Although a greater number of malesand other smaller individuals were tracked viaharmonic direction finding there was no signifi-cant difference in the weight of frogs tracked viaeither method when each species and sex cate-gory was considered separately (table 1) Theproportion of attempts upon which fixes wereobtained differed significantly between track-ing devices for some classes of individuals Weobtained fewer fixes using harmonic directionfinding for L lesueuri and L nannotis femalesbut not for L genimaculata or L nannotis males(table 1 fig 2) Overall while frogs trackedusing radio telemetry were found on averageon 974 of attempts frogs tracked via har-monic direction finding were located on only668 of attempts This varied among speciesL genimaculata were found 854 of the timeusing harmonic direction finding compared to
Tracking amphibians 371
Tabl
e1
Man
nW
hitn
eyte
sts
for
diff
eren
ces
betw
een
harm
onic
dire
ctio
nfin
ding
and
radi
ote
lem
etry
inpr
opor
tions
offix
esob
tain
eda
vera
gedi
stan
cem
oved
per
day
(m)
aver
age
heig
htab
ove
the
stre
am(m
)an
dav
erag
eho
rizo
ntal
dist
ance
from
the
stre
am(m
)
indi
cate
ssi
gnifi
canc
eat
the
Bon
ferr
oni-
adju
sted
005
leve
l
Spec
ies
Sex
Num
ber
ofin
divi
dual
sTe
sts
for
diff
eren
cebe
twee
nra
dio
tele
met
ryan
dha
rmon
icdi
rect
ion
findi
ngin
w
ithea
chta
gty
peFr
ogbo
dyw
eigh
t(g)
Prop
ortio
nof
fixes
Ave
rage
dist
ance
Ave
rage
heig
htab
ove
Ave
rage
hori
zont
alm
oved
per
day
(m)
stre
am(m
)di
stan
cefr
omst
ream
(m)
Rad
ioH
arm
onic
Man
n-P
Man
n-P
Man
n-P
Man
n-P
Man
n-P
tele
met
rydi
rect
ion
Whi
tney
Whi
tney
Whi
tney
Whi
tney
Whi
tney
findi
ngZ
ZZ
ZZ
Lg
enim
acul
ata
Fem
ale
93
minus04
630
710
minus29
70
09minus1
202
028
2minus1
017
037
3minus0
832
048
2M
ale
015
ndashndash
ndashndash
ndashndash
ndashndash
ndash
Ll
esue
uri
Fem
ale
246
minus03
180
765
minus33
080
002
minus09
850
347
minus11
920
251
minus18
670
065
Mal
e7
25minus2
209
002
5minus3
711
lt0
001
minus24
840
011
minus23
020
020
minus12
770
207
Ln
anno
tis
Fem
ale
193
minus11
280
301
minus27
950
001
minus19
610
053
minus05
260
651
minus08
610
408
Mal
e2
4minus1
97
044
0minus1
174
026
7minus0
926
053
3minus0
939
053
3minus0
939
053
3
372 JJL Rowley RA Alford
Figure 2 Mean proportion of fixes obtained (number of fixes divided by total possible number of fixes for each individual)for Litoria genimaculata (LG) L lesueuri and L nannotis (LN) tracked using harmonic direction finding and radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
582 and 577 of the time for L lesueuri andL nannotis respectively In contrast the pro-portion of fixes for each species during radiotelemetry varied less between 952 and 995Compared to radio telemetry harmonic direc-tion finding typically resulted in a lower av-erage distance moved per day lower averageheight above the stream and lower average hori-zontal distance from the stream for the major-ity of species and sex combinations howeverthese differences were not significant (table 1figs 3-5)
Discussion
While the attachment of tracking devices to am-phibians may result in short-term increases inmovement and activity (Langkilde and Alford2002) the results of our laboratory experimentindicate that this effect can disappear within ashort time Comparing the magnitude of varia-tion among individuals with the magnitude ofthe very small median changes (fig 1) suggeststhat any real effects of tag attachment on be-haviour may disappear after individuals havebeen allowed to acclimate for 24 hours or are
so small compared to levels of variation amongindividuals that they are unlikely to affect theusefulness of observations made using attachedtags As long as data for the period immediatelyfollowing tag attachment are discarded it ap-pears that the effects of tags are unlikely to alterthe movement patterns revealed by tracking am-phibians in the field Our observations of the be-haviour of tagged frogs in the field support thisfinding In all species we studied frogs with at-tached tags appeared to be uninhibited in theirmovement were commonly observed in closeassociation with frogs without tags and wereoften observed calling and in amplexus One in-dividual was observed calling less than 12 h af-ter tag attachment In addition frogs with tagsattached maintained their weight over the track-ing period (JJL Rowley and RA Alford un-publ data)
Although our data revealed no persistent ef-fects of tag attachment on the frequency ofmovement and distances moved by L lesueuriin the laboratory effects of tag attachment can-not be ruled out as there may be subtle effectson behaviour that were not investigated hereThere is also a chance that frog behaviour in our
Tracking amphibians 373
Figure 3 Mean distance moved per day for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
Figure 4 Mean height above stream (m) for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
370 JJL Rowley RA Alford
sightings In the process of searching for individual frogswe never noticeably disturbed other tracked frogs primarilydue to the large size of each study site and scattered spatialdistribution of most individuals Although search effort washighly variable from day to day we spent approximatelythe same total number of person-hours using each techniqueduring each survey period
When frogs were located using either technique we re-corded their location as distance along the stream (m) hor-izontal distance from the stream (m) and height abovestream (m) allowing us to calculate their distance movedper day We used these variables because they are impor-tant aspects of the habitat use of amphibians and theycan be compared to determine whether they are differ-entially biased by the tracking technique used To avoidpseudoreplication and biasing our results to frogs that werelocated more often we used individuals as replicates andanalysed means or proportions for each animal Due towell-documented differences in behaviour between sexes(eg Bellis 1965 Dole and Durant 1974 Miaud Sanuyand Avrillier 2000) and our bias towards tracking malesvia harmonic direction finding (due to their smaller bodysize) we performed Mann Whitney tests separately for eachsex and species combination We also examined whetherfrog body weight differed with tracking device for each sexand species combination We used Bonferroni adjustmentsto control Type I error rates Boxplots were used to visu-alise the results In boxplots bold horizontal lines repre-sent the median boxes indicate the locations of upper andlower quartiles bars encompass values up to 15 interquar-tile range open circles represent values more than 15 in-terquartile ranges from the nearest quartile and stars indi-cate data values more than 3 interquartile ranges from thenearest quartile
Results
Effect of tracking device attachmenton movement
Both movement parameters were highly vari-able and changes between nights 2-6 to nights8-12 also varied greatly among individuals(fig 1) For both parameters the median changewas a very slight decline following tag at-tachment (fig 1) however the changes fromnights 2-6 to 8-12 for both movement parame-ters were not significantly different from zero(log10(number of moves) t11 = 0630 P =0542 log10(total distance moved) t11 = 1060P = 0312)
Figure 1 Changes in behaviour expressed as the differencebetween values of log10 of parameters totalled over nights8-12 following capture with tags attached and over nights2-6 following capture with no tags attached Subtracting thevalue for days 2-6 from that for days 8-12 gives figures forchange that are directly related to actual change the neg-ative median for both parameters indicate that in the indi-viduals observed they decreased slightly following tag at-tachment Neither change approaches statistical significance(see text) Bold horizontal lines represent the median boxesindicate the locations of upper and lower quartiles and barsencompass values up to 15 interquartile range
Comparison of techniques
In total 117 frogs were tracked during the study(table 1) Although a greater number of malesand other smaller individuals were tracked viaharmonic direction finding there was no signifi-cant difference in the weight of frogs tracked viaeither method when each species and sex cate-gory was considered separately (table 1) Theproportion of attempts upon which fixes wereobtained differed significantly between track-ing devices for some classes of individuals Weobtained fewer fixes using harmonic directionfinding for L lesueuri and L nannotis femalesbut not for L genimaculata or L nannotis males(table 1 fig 2) Overall while frogs trackedusing radio telemetry were found on averageon 974 of attempts frogs tracked via har-monic direction finding were located on only668 of attempts This varied among speciesL genimaculata were found 854 of the timeusing harmonic direction finding compared to
Tracking amphibians 371
Tabl
e1
Man
nW
hitn
eyte
sts
for
diff
eren
ces
betw
een
harm
onic
dire
ctio
nfin
ding
and
radi
ote
lem
etry
inpr
opor
tions
offix
esob
tain
eda
vera
gedi
stan
cem
oved
per
day
(m)
aver
age
heig
htab
ove
the
stre
am(m
)an
dav
erag
eho
rizo
ntal
dist
ance
from
the
stre
am(m
)
indi
cate
ssi
gnifi
canc
eat
the
Bon
ferr
oni-
adju
sted
005
leve
l
Spec
ies
Sex
Num
ber
ofin
divi
dual
sTe
sts
for
diff
eren
cebe
twee
nra
dio
tele
met
ryan
dha
rmon
icdi
rect
ion
findi
ngin
w
ithea
chta
gty
peFr
ogbo
dyw
eigh
t(g)
Prop
ortio
nof
fixes
Ave
rage
dist
ance
Ave
rage
heig
htab
ove
Ave
rage
hori
zont
alm
oved
per
day
(m)
stre
am(m
)di
stan
cefr
omst
ream
(m)
Rad
ioH
arm
onic
Man
n-P
Man
n-P
Man
n-P
Man
n-P
Man
n-P
tele
met
rydi
rect
ion
Whi
tney
Whi
tney
Whi
tney
Whi
tney
Whi
tney
findi
ngZ
ZZ
ZZ
Lg
enim
acul
ata
Fem
ale
93
minus04
630
710
minus29
70
09minus1
202
028
2minus1
017
037
3minus0
832
048
2M
ale
015
ndashndash
ndashndash
ndashndash
ndashndash
ndash
Ll
esue
uri
Fem
ale
246
minus03
180
765
minus33
080
002
minus09
850
347
minus11
920
251
minus18
670
065
Mal
e7
25minus2
209
002
5minus3
711
lt0
001
minus24
840
011
minus23
020
020
minus12
770
207
Ln
anno
tis
Fem
ale
193
minus11
280
301
minus27
950
001
minus19
610
053
minus05
260
651
minus08
610
408
Mal
e2
4minus1
97
044
0minus1
174
026
7minus0
926
053
3minus0
939
053
3minus0
939
053
3
372 JJL Rowley RA Alford
Figure 2 Mean proportion of fixes obtained (number of fixes divided by total possible number of fixes for each individual)for Litoria genimaculata (LG) L lesueuri and L nannotis (LN) tracked using harmonic direction finding and radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
582 and 577 of the time for L lesueuri andL nannotis respectively In contrast the pro-portion of fixes for each species during radiotelemetry varied less between 952 and 995Compared to radio telemetry harmonic direc-tion finding typically resulted in a lower av-erage distance moved per day lower averageheight above the stream and lower average hori-zontal distance from the stream for the major-ity of species and sex combinations howeverthese differences were not significant (table 1figs 3-5)
Discussion
While the attachment of tracking devices to am-phibians may result in short-term increases inmovement and activity (Langkilde and Alford2002) the results of our laboratory experimentindicate that this effect can disappear within ashort time Comparing the magnitude of varia-tion among individuals with the magnitude ofthe very small median changes (fig 1) suggeststhat any real effects of tag attachment on be-haviour may disappear after individuals havebeen allowed to acclimate for 24 hours or are
so small compared to levels of variation amongindividuals that they are unlikely to affect theusefulness of observations made using attachedtags As long as data for the period immediatelyfollowing tag attachment are discarded it ap-pears that the effects of tags are unlikely to alterthe movement patterns revealed by tracking am-phibians in the field Our observations of the be-haviour of tagged frogs in the field support thisfinding In all species we studied frogs with at-tached tags appeared to be uninhibited in theirmovement were commonly observed in closeassociation with frogs without tags and wereoften observed calling and in amplexus One in-dividual was observed calling less than 12 h af-ter tag attachment In addition frogs with tagsattached maintained their weight over the track-ing period (JJL Rowley and RA Alford un-publ data)
Although our data revealed no persistent ef-fects of tag attachment on the frequency ofmovement and distances moved by L lesueuriin the laboratory effects of tag attachment can-not be ruled out as there may be subtle effectson behaviour that were not investigated hereThere is also a chance that frog behaviour in our
Tracking amphibians 373
Figure 3 Mean distance moved per day for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
Figure 4 Mean height above stream (m) for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
Tracking amphibians 371
Tabl
e1
Man
nW
hitn
eyte
sts
for
diff
eren
ces
betw
een
harm
onic
dire
ctio
nfin
ding
and
radi
ote
lem
etry
inpr
opor
tions
offix
esob
tain
eda
vera
gedi
stan
cem
oved
per
day
(m)
aver
age
heig
htab
ove
the
stre
am(m
)an
dav
erag
eho
rizo
ntal
dist
ance
from
the
stre
am(m
)
indi
cate
ssi
gnifi
canc
eat
the
Bon
ferr
oni-
adju
sted
005
leve
l
Spec
ies
Sex
Num
ber
ofin
divi
dual
sTe
sts
for
diff
eren
cebe
twee
nra
dio
tele
met
ryan
dha
rmon
icdi
rect
ion
findi
ngin
w
ithea
chta
gty
peFr
ogbo
dyw
eigh
t(g)
Prop
ortio
nof
fixes
Ave
rage
dist
ance
Ave
rage
heig
htab
ove
Ave
rage
hori
zont
alm
oved
per
day
(m)
stre
am(m
)di
stan
cefr
omst
ream
(m)
Rad
ioH
arm
onic
Man
n-P
Man
n-P
Man
n-P
Man
n-P
Man
n-P
tele
met
rydi
rect
ion
Whi
tney
Whi
tney
Whi
tney
Whi
tney
Whi
tney
findi
ngZ
ZZ
ZZ
Lg
enim
acul
ata
Fem
ale
93
minus04
630
710
minus29
70
09minus1
202
028
2minus1
017
037
3minus0
832
048
2M
ale
015
ndashndash
ndashndash
ndashndash
ndashndash
ndash
Ll
esue
uri
Fem
ale
246
minus03
180
765
minus33
080
002
minus09
850
347
minus11
920
251
minus18
670
065
Mal
e7
25minus2
209
002
5minus3
711
lt0
001
minus24
840
011
minus23
020
020
minus12
770
207
Ln
anno
tis
Fem
ale
193
minus11
280
301
minus27
950
001
minus19
610
053
minus05
260
651
minus08
610
408
Mal
e2
4minus1
97
044
0minus1
174
026
7minus0
926
053
3minus0
939
053
3minus0
939
053
3
372 JJL Rowley RA Alford
Figure 2 Mean proportion of fixes obtained (number of fixes divided by total possible number of fixes for each individual)for Litoria genimaculata (LG) L lesueuri and L nannotis (LN) tracked using harmonic direction finding and radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
582 and 577 of the time for L lesueuri andL nannotis respectively In contrast the pro-portion of fixes for each species during radiotelemetry varied less between 952 and 995Compared to radio telemetry harmonic direc-tion finding typically resulted in a lower av-erage distance moved per day lower averageheight above the stream and lower average hori-zontal distance from the stream for the major-ity of species and sex combinations howeverthese differences were not significant (table 1figs 3-5)
Discussion
While the attachment of tracking devices to am-phibians may result in short-term increases inmovement and activity (Langkilde and Alford2002) the results of our laboratory experimentindicate that this effect can disappear within ashort time Comparing the magnitude of varia-tion among individuals with the magnitude ofthe very small median changes (fig 1) suggeststhat any real effects of tag attachment on be-haviour may disappear after individuals havebeen allowed to acclimate for 24 hours or are
so small compared to levels of variation amongindividuals that they are unlikely to affect theusefulness of observations made using attachedtags As long as data for the period immediatelyfollowing tag attachment are discarded it ap-pears that the effects of tags are unlikely to alterthe movement patterns revealed by tracking am-phibians in the field Our observations of the be-haviour of tagged frogs in the field support thisfinding In all species we studied frogs with at-tached tags appeared to be uninhibited in theirmovement were commonly observed in closeassociation with frogs without tags and wereoften observed calling and in amplexus One in-dividual was observed calling less than 12 h af-ter tag attachment In addition frogs with tagsattached maintained their weight over the track-ing period (JJL Rowley and RA Alford un-publ data)
Although our data revealed no persistent ef-fects of tag attachment on the frequency ofmovement and distances moved by L lesueuriin the laboratory effects of tag attachment can-not be ruled out as there may be subtle effectson behaviour that were not investigated hereThere is also a chance that frog behaviour in our
Tracking amphibians 373
Figure 3 Mean distance moved per day for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
Figure 4 Mean height above stream (m) for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
372 JJL Rowley RA Alford
Figure 2 Mean proportion of fixes obtained (number of fixes divided by total possible number of fixes for each individual)for Litoria genimaculata (LG) L lesueuri and L nannotis (LN) tracked using harmonic direction finding and radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
582 and 577 of the time for L lesueuri andL nannotis respectively In contrast the pro-portion of fixes for each species during radiotelemetry varied less between 952 and 995Compared to radio telemetry harmonic direc-tion finding typically resulted in a lower av-erage distance moved per day lower averageheight above the stream and lower average hori-zontal distance from the stream for the major-ity of species and sex combinations howeverthese differences were not significant (table 1figs 3-5)
Discussion
While the attachment of tracking devices to am-phibians may result in short-term increases inmovement and activity (Langkilde and Alford2002) the results of our laboratory experimentindicate that this effect can disappear within ashort time Comparing the magnitude of varia-tion among individuals with the magnitude ofthe very small median changes (fig 1) suggeststhat any real effects of tag attachment on be-haviour may disappear after individuals havebeen allowed to acclimate for 24 hours or are
so small compared to levels of variation amongindividuals that they are unlikely to affect theusefulness of observations made using attachedtags As long as data for the period immediatelyfollowing tag attachment are discarded it ap-pears that the effects of tags are unlikely to alterthe movement patterns revealed by tracking am-phibians in the field Our observations of the be-haviour of tagged frogs in the field support thisfinding In all species we studied frogs with at-tached tags appeared to be uninhibited in theirmovement were commonly observed in closeassociation with frogs without tags and wereoften observed calling and in amplexus One in-dividual was observed calling less than 12 h af-ter tag attachment In addition frogs with tagsattached maintained their weight over the track-ing period (JJL Rowley and RA Alford un-publ data)
Although our data revealed no persistent ef-fects of tag attachment on the frequency ofmovement and distances moved by L lesueuriin the laboratory effects of tag attachment can-not be ruled out as there may be subtle effectson behaviour that were not investigated hereThere is also a chance that frog behaviour in our
Tracking amphibians 373
Figure 3 Mean distance moved per day for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
Figure 4 Mean height above stream (m) for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
Tracking amphibians 373
Figure 3 Mean distance moved per day for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
Figure 4 Mean height above stream (m) for female (F) and male (M) Litoria genimaculata (LG) L lesueuri and L nannotis(LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences between techniques datafor each individual were adjusted by subtracting the mean for that species and sex combination obtained via radio telemetryBold horizontal lines represent the median boxes indicate the locations of upper and lower quartiles bars encompass valuesup to 15 interquartile range open circles represent values more than 15 interquartile ranges from the nearest quartile andstars indicate data values more than 3 interquartile ranges from the nearest quartile
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
374 JJL Rowley RA Alford
Figure 5 Mean horizontal distance from stream for female (F) and male (M) Litoria genimaculata (LG) L lesueuri andL nannotis (LN) tracked using harmonic direction finding and radio telemetry In order to illustrate differences betweentechniques data for each individual were adjusted by subtracting the mean for that species and sex combination obtainedvia radio telemetry Bold horizontal lines represent the median boxes indicate the locations of upper and lower quartilesbars encompass values up to 15 interquartile range open circles represent values more than 15 interquartile ranges from thenearest quartile and stars indicate data values more than 3 interquartile ranges from the nearest quartile
experiment changed with time over the courseof captivity and further studies should controlfor any possible temporal effects In additionthe affect of tracking device attachment is likelyto vary among species and to depend on the rel-ative size of the transmitter and on the trans-mitter attachment method (Boag 1972 Lanceand Watson 1977 Wanless Harris and Morris1988 Bridger and Booth 2003) The potentialeffects of tag attachment must therefore be care-fully considered in any study
Our comparison of tracking methods indi-cated that when harmonic direction finding isused it is important to consider the limitationsof the method Its principal limitation is that itoften produces a relatively low number of fixesfor each animal The proportions of fixes we ob-tained are comparable to those found in otherstudies using harmonic direction finding (Webband Shine 1997 Williams Li and Gao 2004Leskovar and Sinsch 2005) Although our studyrevealed no significant effect of tracking deviceon the average distance moved by frogs dataobtained using harmonic direction finding maybe biased towards animals that move relatively
short distances since animals that move largedistances often cannot be located (eg Webband Shine 1997 Leskovar and Sinsch 2002Williams Li and Gao 2004 Leskovar and Sin-sch 2005) It also may be biased against ob-taining fixes in highly concealed retreat sitessince its signal strength is greatly reduced bythick vegetation and rocks As we spent approx-imately the same amount of person-hours usingeach technique harmonic direction finding wastypically much less efficient than radio teleme-try Although it is theoretically possible to inten-sively search large areas using this techniquefactors such as difficult terrain and time con-strains often make this impractical
As in several other studies we found that inthe field detection range with harmonic direc-tion finding was considerably lower than thatreported in optimal (flat open) study sites (En-gelstoft Ovaska and Honkanen 1999) In factwhile the maximum detection distance for thediodes used in this study is approximately 40m (Langkilde and Alford 2002) in the fieldthe maximum detection distance recorded was12 m and this was with direct line of sight
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
Tracking amphibians 375
between the harmonic direction finder and thefrog which was located in the canopy Detec-tion distance was often as low as 05 m whenfrogs were under rocks within the stream bankthereby making it necessary to scan aroundevery boulder and in every crevice in order to lo-cate an animal Therefore while the distance be-tween parallel scanning paths when using har-monic direction finding was recommended tobe 4-8 m for toads in relatively open habi-tat (Leskovar and Sinsch 2005) the results ofthis study indicate that in densely vegetated orrocky environments the distance between par-allel scan paths may need to be reduced to aslittle as 1-2 m This makes harmonic directionfinding a laborious and time consuming activ-ity in such environments particularly becausefrogs occur in complex three-dimensional envi-ronments requiring scanning under rocks andup trees
That tagged animals must be identified in an-other way once they are found using harmonicdirection finding was a problem with speciesthat spent time in inaccessible places such asunder boulders or in the canopy While we wereoften able to identify the individual by a processof elimination and the location of individualson previous and subsequent surveys in stud-ies with longer time intervals between locatingfrogs this may not be possible
Our data indicate that realistic and usefulinformation on the behaviour and microhabi-tat selection of several species of frogs can beobtained using either harmonic direction find-ing or radio telemetry They also suggest thatthe choice of tracking device should depend onboth the behaviour of the study species and thenature of the terrain Harmonic direction find-ing is more suitable for animals that are rel-atively sedentary or have small or otherwisewell-defined home ranges In our study the typeof tracking device did not affect the proportionof fixes obtained for L genimaculata a specieswhich tends to remain close to the stream (JJLRowley and RA Alford unpubl data) but hada large impact on the proportion of fixes ob-
tained for the more mobile L lesueuri Therocky nature of our study sites and the tendencyof L nannotis to shelter under large bouldersmeant that fixes often could not be obtained forthis species using harmonic direction findingThe choice of tracking technique should alsobe influenced by study duration with the longfunctional life of harmonic tags making har-monic direction finding more appealing in long-term studies Although radio telemetry was amore reliable and accurate method of obtaininginformation on the spatial ecology of our studyspecies for species that are too small to trackusing radio telemetry harmonic direction find-ing may often be a viable method for obtainingdetailed information on their spatial ecology
Acknowledgements This research was supported by fund-ing from the Australian Department of Environment andHeritage Australian Geographic a subcontract to RAAfrom US NSF IRCEB grant DEB-0213851 (JP CollinsPI) the Society for the Study of Amphibian and ReptilesGrants in Herpetology the Australian Geographic Societyand the Peter Rankin Trust Fund for Herpetology JJLR wassupported by an Australian Postgraduate Research Schol-arship The research was carried out under Scientific Pur-poses Permits (N000125796SAA WISP01715204 andWITK01715604) issued by the Queensland Parks andWildlife Service and was approved by the James Cook Uni-versity Animal Care and Ethics Committee (approvals A672-01 and A863) We are extremely grateful to A Backerand numerous volunteers for assistance in data collectionand R Jehle J Pellet R Puschendorf and an anonymous re-viewer for comments on earlier versions of the manuscript
References
Bellis ED (1965) Home range and movements of thewood frog in a northern bog Ecology 46 90-98
Boag DA (1972) Effect of radio packages on behaviourof captive red grouse J Wildl Man 36 511-518
Bridger CJ Booth RK (2003) The effects of bioteleme-try transmitter presence and attachment procedures onfish physiology and behavior Rev Fish Sci 11 13-34
Dole JW Durant P (1974) Movements and seasonalactivity of Atelopus oxyrhynchus (Anura Atelopodidae)in a Venezuelan cloud forest Copeia 1974 230-235
Donnellan SC Mahony MJ (2004) Allozyme chromos-mal and morphological variability in the Litoria lesueurispecies group (Anura Hylidae) including a descriptionof a new species Aust J Zool 52 1-28
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
Williams DW Li G Gao R (2004) Tracking move-ments of individual Anoplophora glabripennis (Coleop-tera Cerambycidae) adults Application of harmonicradar Environ Entomol 33 644-649
Received September 12 2006 Accepted November 62006
376 JJL Rowley RA Alford
Engelstoft C Ovaska K Honkanen N (1999) The har-monic direction finder a new method for tracking move-ments of small snakes Herp Rev 30 84-87
Gessaman JA Nagy KA (1988) Transmitter loads affectthe flight speed and metabolism of homing pigeonsCondor 90 662-668
Hockmann P Schlomberg P Wallin P Weber R (1989)Die bewegungsmuster und orientierung des laufkaumlfersCarabus auronitens in einem westfaumllischen Eichen-Hainbuchen-Wald (Radarbeobachtungen und Ruumlckfang-experimente) Abh Westfaumll Mus Nat kd 51 7-15
Janszligen B Plachter H (1998) The use of harmonic radarfor search on the mobility of small invertebrates VerhGes Oumlkol 28 217-224
Kenward R (1987) Wildlife Radio Tagging New YorkAcademic Press
Lance AN Watson A (1977) Further tests of radio-marking on red grouse J Wildl Man 41 579-582
Langkilde T Alford RA (2002) The tail wags the frogHarmonic radar transponders affect movement behaviorin Litoria lesueuri J Herpet 36 711-715
Leskovar C Sinsch U (2002) Harmonic radar a novelapproach to track dispersing toadlets (Bufo calamita Bviridis) Zool Anal Complex Syst 105 Suppl V 7
Leskovar C Sinsch U (2005) Harmonic direction find-ing a novel tool to monitor the dispersal of small-sizedanurans Herpetol J 15 173-180
Loumlvei GL Stringer IAN Devine CD Cartellieri M(1997) Harmonic radar mdash a method using inexpensivetags to study invertebrate movement on land N Z JEcol 21 187-193
Mascanzoni D Wallin H (1986) The harmonic radara new method of tracing insects in the field EcolEntomol 11 387-390
Miaud C Sanuy D Avrillier J-N (2000) Terrestrialmovements of the natterjack toad Bufo calamita (Am-phibia Anura) in a semi-arid agricultural landscapeAmphibia-Reptilia 21 357-369
Neudorf DL Pitcher TE (1997) Radio transmitters donot affect nestling feeding rates by female hooded war-blers J Field Ornithol 68 64-68
Pellet J Rechsteiner L Skrivervik AK Zurcher JFPerrin N (2006) Use of the Harmonic direction finderto study the terrestrial habitats of the European tree frog(Hyla arborea) Amphibia-Reptilia 27138-142
Powell LA Krementz DG Lang JD Conroy MJ(1998) Effects of radio-transmitters on migrating woodthrushes J Field Ornithol 69 306-315
Richards SJ Sinsch U Alford RA (1994) RadioTracking In Measuring and Monitoring Biological Di-versity Standard Methods for Amphibians p 155-157Heyer WR Donnelly MA McDiarmid RW HayekLC Foster MS Eds Washington Smithsonian Insti-tution Press
Riley JR Valeur P Smith AD Reynolds DR PoppyGM Loumlfstedt C (1998) Harmonic radar as a means oftracking the pheromone-following flight of male mothsJ Insect Behav 11 287-296
Roland J McKinnon G Backhouse C Phillip D(1996) Even smaller tags on insects Nature 381 120
Sizun H (2005) Radio Wave Propagation for Telecommu-nication Applications Heidelberg Springer-Verlag
Sodhi NS Warkentin IG James PC Oliphant LW(1991) Effects of radiotagging on breeding merlins JWildl Man 55 613-616
Stringer I Montefiore R (2000) Distribution and biologyof the endangered kauri snail Paryphanta busbyi wattiSci Conserv 163 1-42
Stringer IAN Parrish GR Sherley GH (2004) Popu-lation structure growth and longevity of Placostylushongii (Pumonata Bulimulidae) on Tawhiti Rahi IslandPoor Knights Islands New Zealand Pacific ConservBiol 9 241-247
Wallin H Ekbom B (1988) Movements of carabid bee-tles (Coleoptera Carabidae) inhabiting cereal fields afield tracing study Oecologia 77 39-43
Wanless S Harris MP Morris JA (1988) The effectof radio transmitters on the behavior of common murresand razorbills during chick rearing The Condor 90 816-823
Webb JK Shine R (1997) A field study of spatialecology and movements of a threatened snake speciesHoplocephalus bungaroides Biol Conserv 82 203-217
White G Garrott R (1990) Analysis of Wildlife Radio-tracking Data San Diego Academic Press
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Received September 12 2006 Accepted November 62006
