EFFECTIVE SAMPLING AREA: A QUANTITATIVE METHOD FOR
SAMPLING CRAYFISHPOPULATIONSIN FRESHWATERMARSHES
BY
CHARLES A. ACOSTAI) and SUE A. PERRY
SouthFlorida Natural ResourcesCenter,EvergladesNational Park, 40001 StatcRoad 9336,
Homestead.
Florida33034,U.S.A.
ABSTRACT
Wc uscd mark-rcc:rpturctechniquesto estimatethe attractionsampling area of baited traps fbr
nronitoring density of thc crayfish Pntcamharusalleni in the freshwatermarshesof the Florida
Everglades.We successfullyapplieda permanentvisible tag suitablefor massor individual rnarking
of crayfish. In laboratory mesocosms,males and f'emalesand juveniles and adults enteredbaited
wire trapswith sirnilarfiequency,reflectinga lack ofage- or sex-specificbias in trapping.In flooded
marshhabitat,we releasedmarked crayfish among a circular array of baited traps set at a specilic
radialdistancefiom the releasepoint and dctcrminedrecaptureproportionsover 48 h. We then used
the methodologyof Turchin & Odenaal (1996) to estimatethe efl'ectivesarnplingarea basedon
the proportionsof crayfish recapturedover various radial distances.In flooded marshes,the mean
proportionof recapturesdeclinedfiom 0.59 in trapswith a l-m samplingradiusto 0.02 in trapswith
a 2[3-msamplingradius.A log-linearregressionmodel provided the best fit to the capturedata,and
the eil-ectivesampling erreaof baited traps was estimatedas 56.3 mt. The efl'ectivesampling area
servesas a translationcoefhcientthat can be usedto calculateactual density of crayiish in a given
areafrom mark-recapturetrappingdata.
RESUME
Nous avons utilisds des techniquesde recaptured'individus marqudespour estimer les zones
d'attraction de pidges appitds pour le controle de densitd de I'dcrevisse Procambarus alleni
dans les marais d'eau douce des Evergladesde Floride. Nous avons appliqud avec succbsune
marque permanente,visible, convenantpour le marquageen masseou individuel des 6crevisses.
En laboratoire,meleset f'emelles,juvinileset adultes,pdndtraientdansles pibgesen grillage appAtds
avecla rn6mefidquence,refldtantl'absenccde biais relatif au sexeou i I'ige dans la capture.Dans
I'habitatde maraisinondd,nous avonsrellchd les dcrevissesmarqudesparmi une aire circulairede
pidgesappitds placdsir unc distanceradiale spdcifiquedu point de relAchement,et ddtermindles
proportionsde recapturesur 48 h. Nous avonsalors utilisd la mdthodologiede Turchin & Odenaal
( I 996) pour estimerla zoned'dchantillonnageefl'ectifd'aprdsles proportionsd'dcrevissesrecaptur6s
sur diversesdistancesradiales. Dans les rnarais inondds, la proportion moyenne dc recapturcs
l.) Fax: 30-5-242-7836;
e-mail:[email protected]
BrillNV.Leiden.
2(XX)
G) Koninkliikc
Clrustaceana
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C ] t I A R I - E SA . A C O S - I A& S I J E A . P E R R Y
ddcroissaitde 0,59, pour les pidgesdans un rayon d'dchantillonnagede I m, ir 0,02 pour les pidges
dans un rayon de 28 m. Un moddle de rdgressionlogarithmiquelindaire fburnissait le meilleur
ajustementaux donndesde capture,et la zone d'dchantillonnageeffectif des pidges appdt6sdtait
estimdeI56,3 m2. La zone d'dchantillonnageefl'ectifseft comme un coefficientde traductionqui
peut etre utilisd pour calculer la densitdrdelle d'6crevissesdans une zone ddterminded'aprbs les
donndesde recaptured'individus marquds.
INTRODUCTION
A variety of methodshave been used to samplecrayfish populationsin freshwater habitats,but most have a number of associatedlogistical and quantitative
problems.Collectionby hand (e.g.,Hazlettet al., 1979)is generallynot practical in heavily vegetatedhabitats.Throw traps (Jordanet al., 1996)and pull traps
(Kushlan& Kushlan, 1979)havebeenusedto samplecrayfishProcambarusalleni
(Faxon, 1884)in freshwatermarl prairie and slough habitatsin the Florida Everglades.Thesemethodsare labor intensive,do not sampleanimalsin burrows,and
are diflicult to use in heavily vegetatedhabitats.Becausethesemethodssample
only a relatively small area,crayfish density may be underestimatedor overestimated if sampling is not intensiveand the spatial distribution of animals is not
uniform. Baited traps have been used for sampling crayfish populationsin several studies(e.g.,cylindrical wire minnow traps,Momot & Gowing, 1972).The
disadvantageof this methodis that it samplesan unknown areaand gives a relative estimateof densitywith an unknown standarderror.Howi:ver,if the attraction
areathat a trap effectivelysamplesis known, trap samplingcan yield quantitative
estimatesfbr monitoringdensityfluctuationsor for analyzingdispersalpatterns.
Mark-recapturemethodshave been widely usedto quantify animal abundance
in the field (Seber,1982).However,it is not known if trapsthat work by attraction
(e.g., containing bait, pheromones)conform to the restrictive assumptionsof
mark-recapturemodels. For example,most mark-recapturemodels assumethat
all animalsare equally likely to be capturedwithin a given area(Cormack, 1969),
but this assumptioncannot be tested until the sampledarea is known. Turchin
& Odenaal (1996) developeda method of quantifying attraction sampling for
insectsusing mark-recaptureexperimentswith pheromonetraps. They used the
relationshipbetweenthe proportionsof recapturedinsectsover all distancesfrom
the releasepoint to estimatethe effective sampling area.This estimatecan be
used as a translationcoefficientto link recaptureprobabilitiesto actual density
per unit area (Turchin & Odenaal,1996).Their method does not assumethat all
animalswithin a given areaareequally likely to be recapturedor that the estimate
is affectedby animaldistributionas long astrapsarelocatedrandomlywith respect
to distribution(Elkinton & Card6, 1980).
SA M PI-ING FRESIIWATEITCRAYFISH POPULA'I'IONS
421
We used the approachof Turchin & Odenaal(1996) to estimatethe effective
sampling area of baited traps fbr sampling crayfish in flooded freshwatermarl
prairie. We lirst testedfor possibleage- or sex-biasesassociatedwith trap sampling. We then releasedmarkedcray{ishin marshesand measuredrecapturerates
at various distancesfrom releaseto determinethe effective attractionarea of a
baited trap. We assessthe effectivenessof this techniquefor sampling crayfish
populationsin floodedmarshhabitat.
METHODS
experiments,we first testeda permanentvisible
To conductIleld mark-recapture
tag fbr crayfishusing colored elastomerplugs that are implantedunder the clear
exoskeletonof the ventral abdomen.In this procedure,a small amount of liquid
elastomer(< 0.01 ml) is injected under the exoskeleton,and this hardensas a
plug within 24 h (NorthwestMarine Technology,Inc., Shaw Island, Washington,
U.S.A.).This methodhas been used for massor individualmarking of aquatic
organisms(e.g., shrimp, Godin et al., 1995).We held tagged crayfish in the
laboratoryto observetag loss,mortality rates,and molting success.
We conductedexperimentsin laboratorymesocosmsto test fbr samplingbias
associatedwith trapping. Equal numbersof adult and juvenile male and female
crayfishPntcambarusalleni (Decapoda,Cambaridae)were held for 24 h in 2-m
Two wire minnow traps(50 cm long x 20 cm diameterwith
diametermesocosms.
1.5-cmentrancesat eachend) baitedwith shrimp or two unbaitedtraps (with feed
shrimpscatteredaroundthe tank) were placedin the mesocosmsthat containedno
othershelterstructures.Fifteenreplicateswith 6-12 crayfisheachwere conducted
with baited traps and l1 replicateswith unbaitedtraps (eachtotal l14 crayfish).
Trappedcrayfish were enumerateddaily by sex and maturity. When not being
usedin experiments,crayfish were held in tanks with openedwire minnow traps
that servedas shelterand that may preventthe developmentof trap-shyor trapseekingbehavior.Trap data were analyzedusing a hierarchicallog-linear model
for a multidimensionalcontingencytable with craylish sex (male and female)and
maturity(adultandjuvenile) nestedin trap type (baitedor unbaited).We examined
the likelihood ratio chi square(G2t to evaluatethe fit of the model and the partial
chi squares(X2) for effectsof the individual terms (2ar,1998).
In the marl prairie marshesof eastern EvergladesNational Park, Florida,
U.S.A., we conductedmark-recaptureexperimentswith a single-release-multipletrap designto estimatethe attractionsamplingareaof baited traps.Crayfishwere
marked,held without food for 24 h, and then releasedin the centerof a circular
array of baited wire traps that were checked after 48 h. Preliminary sampling
'12r1
( l l l A R l , E S A . A C O S I A & S I J EA . P E R R Y
showed that crayfish catch in traps is similar after 24 and 48 h but declines
after 72 and 144 h. Since the probability of recapturemay be underestimated
if most animals are taken in the near traps (Elkinton & Cardd, 1980), we
conductedseparateexperimentswith a circular anay of traps set at one of several
experimental
samplingradii (1,4, 8, 16,or 28 m) from the releasepoint and each
trap at twice thosedistancesfrom other traps.Eighteenreplicateswith 20 crayfish
eachwere conductedfbr eachsamplingarray.
To estimatethe effectivesamplingareaof baitedtraps,we adoptedthe approach
of Turchin & Odenaal (1996). The proportions of recapturedcrayfish P were
plotted at each distance r fiom the release point. Regressionanalyseswere
conductedto determinethe relationshipbetweenthe dependentvariable (P) and
the actual,log-transformed,or squareroot-transformedindependentvariable (r).
The besttransformationof radiusr as indicatedby the coefficientof determination
R2 was used,and an empiricalcurvewas fitted to the datato describethe functional
relationshipP(r). This flnction P(r) was then integratedover all radii to calculate
the effectivesamplingarea,a (equationI from Turchin & Odenaal,1996):
a:2t
r
/ r P t r td r
(,
Turchin and Odenaal (1996) point out that the efl-ectivesampling area, a, is
actuallya conversioncoefficientfor estimatingdensityin a given area.
RESULTS
The tagging proceduredid not increasemortality; <27o mortality occurred
in both taggedand untaggedcrayfish held in the laboratoryfor thirty days. The
elastomertag remainedhighly visible in the ventral abdomen,and we observed
no loss of tags during one molt in 49 crayfishor during multiple molts in 17
crayfish.Nevertheless,crayfish could be expectedto lose the elastomertag if it
is placedtoo nearthe exoskeleton.One problem notedwith the procedurewas that
in a few animals the elastomerplug was displacedfrom the original position in
one abdominalsegmentto other segments,probably due to tail-flipping or other
strenuousactivity by the animal immediately after tagging. Crayfish marked by
this methodmust be held in the laboratoryfor 24 h to observethe final position of
the tag.
ln laboratorymesocosms,the presenceof shrimp bait was the only significant
factor in crayfishcaprure(G: 1.846,df 3, P : 0.61).More crayfishentered
baitedtraps (86 crayfish)than unbaitedtraps (28 crayfish)(partial X2 30.93,df l,
P < 0.0001).There were no signilicantdifferencesin the captureof males and
429
SA M PLI NC FRI]SHWATER CRAY FISII POPI.JLAf IONS
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Fig. l. Proportionsofrecaptured crayfish Proc'umbarusolleni as a function ofdistance fiom the
releasepoint. Line showsthe fittcd function P(r) : 0.57 0.22|n r.
females(partial 12 0.035,clf 1, P : 0.85) or adultsand juveniles(partial 12
0.526,df I, P : 0.45).
The meanproportionof recapturesdeclinedfrom 0.585 (SE + 0.03) in traps
I m from the releasepoint to 0.016(SE + 0.007)at the 28 m radius.Regression
analysisindicatedthat the ln transformationof the independentvariabler provided
model
thebestfit (F: 252.2,df l, P < 0.0001;Rz 0.74).The mostparsimonious
of the functional relationshipbetweencrayfish recaptureP and trap radius r was
(fie. l):
P(r):0.57-0.221nr.
Using this P(r) in the Turchin-Odenaalequation,we estimatethe effectivesampling
areaas ct : 56.3 m2. This suggeststhat a shrimp-baitedwire trap would most
efficiently samplecrayfishin a 4 m radiusover 48 h.
DISCUSSION
The autecology of the target species must be consideredin any sampling
scheme.A potentialproblemwith trappingis the developmentof behavioralbiases
43t)
C H A R L F SA . A C O S T ^& S U E A . P E R R Y
associatedwith trap avoidance("trap shy") or trap seeking("trap happy"). Brown
& Brewis (1978) suggestedthat trap samplingfbr the crayfishAustropotamobius
pallipe,s(Lereboullet,l8-58)is strongly biasedby "trap happy" male adultswhen
compared with hand collections. In the laboratory,we found no evidence of
behavioralbias in P. alleni males and f'emalesor adults and juveniles. Our lield
samplingin Evergladesmarl prairie marshesalso indicatesa lack of trappingbias
for all crayfishexceptfor gravid femalesthat may be inactivein burrows (Acosta
& Perry,unpubl.).The coefficientfbr the effectivesamplingareamay needto be
approximatedseparatelyfor unique field conditions (Turchin & Odenaal, 1996).
For example, if water flow is strongly directional, baited traps will sample an
ellipticalareawithin the downstream
chemicalplume.
The probability of recapturingmarked crayfish in baited traps decreasedwith
distance as expected.Baited crayfish traps set in shallow freshwater marshes
appearto efl'ectivelysampleabout 0.01 ha, suggestingthat most crayfish within
6 m receivea strong chemical food signal. Beyond this distance,the probability
of capturerapidly declines.The effectivesamplingareacan be usedto link markrecapturemeasurements
to estimatesof actual densities,and it providesa means
to evaluatesampling designs for field use (Turchin & Odenaal, 1996). A key
factor in the successof our experimentswas the use of a highly visible tag with
little or no tag loss or increasein mortality of crayfish.This method appearsto
have substantialbenefitsover other tagging proceduressuch as those involving
mutilation(seeWeingartner,I 982).
Direct estimationof the attractionsampling area can be made in some cases
(e.g.,for insects,Byers et al., 1989;Elkinton & Cardd, 1980; Schlyter,1992).
Other studieshaveattemptedto estimatesamplingareafrom catch statistics(e.g.,
for lobsters,Evans & Evans, 1996),but such estimatesare impossibleto verify
unlessactualdensitiesare known. The methodologyof Turchin & Odenaal(1996)
usesthe empirical relationshipbetweenthe proportionsof recapturedanimalsand
distanceto quantify the effectivesamplingarea.This approachgives a quantitative
estimateof samplingareawithout many of the restrictiveassumptionsassociated
with mark-recapturemodels.
ACKNOWLEDGEMENTS
We thank our volunteersK. Grenouillou and T. Mueller for their assistance
in the field, and T. Van Lent fbr insightful commentson methods.Funding for
C. Acostawas providedthroughCooperativeAgreementNo. 5280-8-9015from
the EvergladesNational Park, National Park Service, to K. Downum, Florida
InternationalUniversity, Miami, Florida, U.S.A. Referenceto trade namesdoes
not imply U.S. governmentendorsement
of commercialproducts.
S A M P I - I N G F R E S I I W A T E RC R A Y F I S [ I P ( ) P I ] I , A T I O N S
431
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Firstreceived6 April 1999.
Final versionaccepted29 June 1999.