Author manuscript, published in "European Journal of Wildlife Research 57, 2 (2010) 355-362" DOI : 10.

1007/s10344-010-0440-7

1Estimation of the Iberian lynx (Lynx pardinus) population in the Doana area, SW Spain, using

%capture-recapture analysis of camera-trapping data

+Short Title: Estimation of Iberian lynx population in the Doana area 1 >! !arrote" , # $ere% de &yala" ,$ $ereira' , ( #obles' , ) !u%man" , ( * !arc+a" , , - Iglesias", *

:.er/0s" , I (a1ardo2 , , Sim3n4 , * 5 6arroso4

= ?1 Direccin General para la Biodi ersidad! "inisterio de "edio #mbiente$ <% &ar'ue (acional de Doana! )r*anismo #utnomo de &ar'ues (acionales! "I"#"$

peer-00629072, version 1 - 5 Oct 2011

1;+ Dele*acin &ro incial de ,uel a! -onse.er/a de "edio #mbiente! 0unta de #ndaluc/a$ 111 &ar'ue (atural de Doana! -onse.er/a de "edio #mbiente! 0unta de #ndaluc/a$

1+-orrespondence 11Germ2n Garrote$ &resent address: 3ertebrate Biolo*y and -onser ation 4-" 5esearch Group$ 6aculty of

1>Biolo*y$ -omplutense 4ni ersity of "adrid ! Spain$

1:Email: *erman*78ocplanet$com$ &hone: 9+1 :+;1%+:<=

1#BST5#-T % +

The Iberian lynx @Lynx pardinusA has a hi*hly restricted *eo*raphic distribution! limited e en 8ithin

1the Iberian &eninsula$ The last national sur ey reported less than %;; remainin* indi iduals! distributed in >t8o isolated areas B #ndC.arB-ardea and Doana B and in conse'uence! the Iberian lynx 8as listed by the :I4-( as D-ritically Endan*eredE$ In this study 8e estimate the Iberian lynx population siFe in the Doana =area usin* captureBrecapture analysis of cameraBtrappin* data$ # model 8ith different capture probability for ?each indi idual @"hA yielded an estimate of %: Iberian lynxes @SEG>$%:A more than one year old$ It is <considered that a small slant in the estimation of the number of indi iduals could exist due to the presence of peer-00629072, version 1 - 5 Oct 2011 1;dispersers inside the study area that 8ere not detected$ )ur study sho8s: 1A a reduction in number since the 111<?;s @1> indi idualsA! and fallin* belo8 the theoretical threshold of *enetic iability! %A chan*es in the 1%speciesH spatial distribution in this area! and +A as for other carni ore species! photo*raphic captureBrecapture 1+methods are applicable for estimatin* the siFe of Iberian lynx populations
11 1>Iey8ords: Lynx pardinus! Iberian lynx! cameraBtrappin*! captureBrecapture! population estimates! Doana

1I(T5)D4-TI)( % +

Ineffecti e carni ore sur ey methods limit the ability of mana*ers and researchers to maJe

1appropriate research conclusions and mana*ement recommendations @,eilbrun et al$ %;;:A$ # techni'ue that >estimates density @Kancia et al$ 1<<1A! detects chan*es o er time @Gibbs %;;;A! and considers the 8elfare of :indi idual animals @Gibbs %;;;L "urray and 6uller %;;;L &eterson et al$ %;;+A 8ould *reatly enhance the =ability to monitor and mana*e populations$
?

The use of camera traps to detect elusi e mammals! such as carni ores! has pro en to be hi*hly

<efficient @-utler and S8ann 1<<<A! and some recent studies ha e pro en the *reat potential that this method peer-00629072, version 1 - 5 Oct 2011 1;can pro ide for estimatin* population siFes of secreti e! but indi idually reco*niFable animals$ &opulations of 11ti*er @Panthera tigris; Iaranth and (ichols! 1<<?A! leopard @P. pardusL ,enschel and 5ay %;;+A! sno8 1%leopard @Uncia unciaL 0acJson et al$ %;;:A and ocelot @Felis pardalisL Trolle and IMry %;;+A ha e been 1+successfully estimated usin* captureBrecapture analysis of cameraBtrappin* data$
11

The Iberian lynx @Lynx pardinusA population! limited both to and 8ithin the Iberian &eninsula

1>@"itchellB0ones et al$ 1<<<A! has declined marJedly o er the last century @Graells 1?<=L -abrera 1<11L 1:3al erde 1<:+A$ Durin* the late 1<?;s! a national sur ey estimated a total population siFe of only 1=approximately 1;;; adult indi iduals @5odr/*ueF and Delibes 1<<%A$ This situation 8as mainly due to 8ideB 1?scale e*etation remo al and transformation! humanBcaused mortality and the decline of its main prey! the 1<8ild rabbit @Oryctolagus cuniculusA! due to the impact of the myxomatosis irus @5odr/*ueF and Delibes %;1<<%! %;;+A$ Durin* the late 1<?;s the Iberian rabbit populations 8ere also seriously affected by 5abbit %1,emorrha*ic Disease @5,DL 3illafuerte et al$ 1<<1A! and this could ha e affected lynx populations ia the %%se ere decline of its specialised prey$ Indeed! a national sur ey carried out in %;;% @GuFm2n et al$ %;;1A %+reported an absolute number of less than 1:; indi idual Iberian lynxes for the 8hole of Spain! distributed in %1.ust t8o isolated areas: #ndC.arN-ardea and Doana$ In conse'uence! the species 8as listed by the I4-( as %>D-ritically Endan*eredE @I4-( %;;%! %;;=A$ This has led to the implementation of se eral mana*ement %:measures 8hich aim to stabiliFe the population and in the future! try to re erse this situation @see Simn! %=%;;?A$

&opulation estimates in the Doana area sho8ed that the number of indi iduals also declined @5au et

%al$ 1<?>L &alomares et al$ 1<<1L 6erreras %;;1L GuFman et al$ %;;1A as in the rest of its distribution ran*e and +for the same factors mentioned abo e$
1

&re ious censuses in the Doana area 8ere based on intensi e searches for si*ns of lynx presence

>@tracJs and droppin*sA in order to estimate the population @&alomares et al$ 1<<1L GuFman et al$ %;;1A$ The :authors assumed a direct relationship bet8een the index of si*ns abundance and lynx numbers$ &alomares et =al$ @1<<1A estimated there 8ere 1> @1;B>;A indi iduals @excludin* cubs still tended by their motherA in the ?Doana area in the late 1<?;s! 8hile GuFm2n et al$ @%;;1A estimated +:B1% lynxes there in %;;%$
<

These methods pro ided a *ood approximation of the population siFe$ ,o8e er! considerin* that the

peer-00629072, version 1 - 5 Oct 2011

1;Iberian lynx is the most endan*ered feline in the 8orld! it is necessary to obtain as ri*orous and accurate 11estimates as are possible! 8ith methods capable of 'uicJly detectin* population chan*es and thus allo8in* the 1%adoption of emer*ency mana*ement measures 8hen re'uired$
1+

The aim of the present study 8as to determine 8hether the use of cameraBtrappin* techni'ues is

11applicable to the Iberian lynx! a species 8ith a ery limited population and restricted distribution area! as 8ell 1>as 8hether this method can also be applied to estimate its population usin* captureBrecapture analysis$
1:

These conclusions are crucial for establishin* an ade'uate monitorin* pro*ram 8hich 8ill allo8 the

1=desi*n and adoption of further conser ation measures$

1? 1<"#TE5I#KS #(D "ET,)DS %;-Study area$ %1

The study area is located in SO Spain! includin* Doana (ational &arJ! Doana (atural &arJ and

%%the peripheral Fone @6i*$ 1A$ The area is bordered on the south and 8est by the #tlantic )cean! to the east by %+the Guadal'ui ir 5i er! and to the north by the allu ial plain of the 5i er Tinto and the intensi ely culti ated %1hi*h *round of #l.arafe @#non 1<?<A$
%>

The area is *enerally flat! but 8ith some undulations in the north! and the eastern third is lar*ely

%:seasonallyBflooded marshland$ The climate is subBhumid "editerranean 8ith mild! 8et 8inters and hot! dry %=summers and the annual rainfall is bet8een >;; and 1;;;mm @5i asB"artineF 1<?=A$

Se en e*etation units can be distin*uished: "editerranean scrub! Eucalyptus spp$ plantations! pine

%plantations! forested pastureland! marsh! beaches and dunes! and culti ated land$ )utside the protected areas! +irri*ated a*riculture and coastal tourism ha e de eloped to a lar*e de*ree o er the last t8o decades! 8ith a 1correspondin* considerable increase in human impact$
>

In most of the (ational &arJ! human access is restricted to researchers and 8ardens! and huntin* is

:strictly forbidden$ -on ersely! outside the (ational &arJ boundaries! le els of human access depend on land =o8ners! and *ame huntin* is fre'uent$
? <-Camera trapping.

peer-00629072, version 1 - 5 Oct 2011

1;

The field8orJ 8as undertaJen bet8een (o ember %;;% and 6ebruary %;;+ by 1 teams of %B1 people

11each$ &hoto*raphs 8ere taJen usin* +> mm cameras 8ith a data re*ister and automatic flash$ The cameras 1%8ere modified to allo8 acti ation ia an external %>x%> cm pressure plate! positioned 1=; cm a8ay! and 1+tri**ered 8hen stepped on by an animal$ Kynx urine obtained from capti e animals 8as used as the lure! and 11placed on an inert support >;cm abo e the *round and ad.acent to the pressure plate$ This attractant 8as 1>replaced e ery + days @%$> mlP isitA accordin* to pre ious studies about the efficiency of this lure in attractin* 1:lynxes @Garrote et al$ %;;1A$ #ttractants are often deployed by researchers at cameraBtrap sites to encoura*e 1= isits by carni ores @Trolle and IMry %;;+L QielinsJi and Iucera 1<<>A$ #s lon* as the effort and baitin* 1?patternPprotocol is standardiFed! the use of such attractants does not ha e any ma.or samplin* implications 1<and poses no statistical problem for captureBrecapture estimates @,enschel and 5ay %;;+! and see Trolle and %;IMry %;;+A$
%1

The entire area potentially used by Iberian lynx 8as sur eyed inside both the (ational and (atural

%%&arJ boundaries @6i* 1A! co erin* all but the marsh! beach! dunes! culti ated land and pastures$ In the %+peripheral areas the cameras 8ere placed at those sites 8here si*ns had been detected 8ithin the pre ious %1year @scats! tracJs! road casualtiesA$ The main areas inside the (ational &arJ not included in this study 8ere %>marshlandsL inside the 8estern (atural &arJ! the areas excluded 8ere temporary pools @the #balario la*oonsA %:containin* 8ater durin* our study$ (either of these habitats 8ere used by lynx 8ithin both the (ational and %=(atural &arJs$

>

The distance bet8een cameraBtraps 8as 1;;B?;;m! producin* a density of R1 traps per 1>; ha! the

%smallest occupied home ran*e siFe Jno8n for any *i en a*eBsex class @an adult female lynx breedin* in a +hi*h rabbit density situationL 6erreras et al$ 1<<=L &alomares et al$ %;;1A$ -onse'uently! indi iduals of other 1a*eBsex classes 8ill be exposed to a *reater number of traps @)tis et al$ 1<=?L Iaranth and (ichols %;;%A$ In >order to obtain an ade'uate number of lynx captures! the cameraBtrap locations 8ere chosen to maximiFe :capture probabilities @Iaranth and (ichols 1<<?A$ Each camera remained continuously acti e durin* the =entire sur ey period for each blocJ @see statistical methodsA$
?

#ll lynxes photo*raphed 8ere indi idually identified throu*h a comparison of distin*uishin* natural

<body marJin* @spotsA! as made in other species such as ti*ers! leopards and ocelots @Iaranth and (ichols peer-00629072, version 1 - 5 Oct 2011 1;1<<?L ,enschel and 5ay %;;+L Trolle and IMry %;;+A$
11 1%-Statistical methods. 1+

The study area 8as di ided into t8o blocJs @east and 8estA 8hich 8ere sampled se'uentially @8ith a

111;Bday *ap bet8een them to allo8 for camera relocationA for the same total time period @(G +; daysA$ 1>-apture histories 8ere de eloped for each lynx older than a year identified by the cameraBtrappin*$ -ubs 8ere 1:not included in the analysis! because they could ha e lo8er capture probabilities @Iaranth and (ichols 1<<?A$ 1=The capture history consisted of a strin* of ones and Feros indicatin* 8hether the indi idual 8as camera 1?trapped @1A or not @;A durin* each Dtrappin* occasionE$ The capture history data of the first samplin* day! in 1<each of the t8o blocJs 8ere combined to form one samplin* occasion @Iaranth and (ichols %;;%L Soisalo %;and -a alcanti %;;:A$ The same procedure 8as used for each of the remainin* days 8ithin the +;Bday %1samplin* period$
%%

The capture histories data 8ere analysed usin* the "#5I soft8are @Ohite and Burnham 1<<<A!

%+de eloped to implement closedBpopulation captureBrecapture models$ The "#5I pro*ram produces %1abundance estimates from = models that differ in their assumptions about capture probability$ Indi idual %>hetero*eneity! beha ioural response and time are used as the sources of ariation in the capture probabilities$
%:

"odel ";! assumes a constant capture probability across all occasions and animals$ "odel "t @timeA

%=assumes that capture probability aries bet8een occasions$ "odel "b @beha iourA assumes that capture

1probability differs for animals that ha e! or ha e not been captured pre iously$ "odel "h @hetero*eneityA

%assumes that each animal had its o8n probability of bein* captured$ In addition "#5I allo8s estimation +under 1 models that are pair8ise combinations of these sources of ariation in capture probability @"odels 1"bh! "th! "tb! "tbhA$
>

To identify an ade'uate model for estimation! 8e used the *oodnessBofBfit test! bet8eenBmodel test!

:and the model selection al*orithm @)tis et al$ 1<=?L 5exstad and Burham 1<<1A pro ided in "#5I$
=

These models are desi*ned for closed populations! so assume no chan*es durin* the study$ To ensure

?that our population 8as closed! the best approach 8as to maJe the period of study as short as possible @)tis et <al$ 1<=?A$ Thus! 8e only use the first thirty days from each phase of camera trappin* for the analysis! and the peer-00629072, version 1 - 5 Oct 2011 1;total sur ey period 8as conse'uently =; days$ This 8as a short trappin* period to assume that the population 11stayed stable o er the study period @Iaranth and (ichols 1<<?L Trolle and Iery %;;+L Sil er et al %;;1A$
1%

The area sampled! and the area occupied by lynx 8as defined by an outer buffer strip e'ual to the

1+oneBhalf of the mean maximum distance Iberian lynx tra elled bet8een cameraBtrap stations placed and 11bet8een camera trap stations 8ith Iberian lynx photo*raph! respecti ely @Iaranth and (ichols %;;%A$
1> 1:5ES4KTS 1= 1?

Durin* the study period >1+ trappin* stations 8ere installed for +; days each! %?; in the east blocJ

1<and %:+ in the 8est blocJ$ The total cameraBtrappin* effort lead to 1:%<; cameraBtrappin* ni*hts$ T8enty %;different Iberian lynx @< males and 11 femalesA 8ere photo*raphed a total of 1%< times at 11: different %1camera stations$ Some indi iduals 8ere recaptured multiple times and at multiple camera stations 8ithin 1 %%sur ey day$ Because closedBpopulation captureBrecapture models consider only 1 recapture per Dtrappin* %+occasionE! a total of ?= positi e trappin* occasions 8ere considered for the total of 1%< captures @Table 1A$
%1

The number of trappin* occasions for each indi idual aried from 1 N 1< @Table 1A! indicatin* a

%>notable indi idual ariation in capture probability$ Except for one female! all of those captured had been %:photo*raphed pre iously in earlier sur eys undertaJen since 1<<<! helpin* the tasJ of a*ein* and sexin* each$
%=

The cumulati e cur e of indi iduals DcapturedE durin* the sur ey stabilised after %; days @6i*$ %A$

1This si*nifies that no ne8 indi iduals 8ere photo*raphed after day %;$ Gi en this information! 8e deduce that

%the len*th of the sur ey 8as ade'uate for the aims of our study$
+

The resultin* population siFe estimate 8as %: Iberian lynx @SEG>$%:A more than one year old$ The

1model selection al*orithm in "#5I selected the model "h! 8ith a different capture probability for each >indi idual$ The estimated capture probability per occasion and indi idual 8as ;$111>! and the estimated :probability of catchin* a lynx at least once durin* the entire study period is *i en by the ratio of total number =of animals cau*ht to the estimated population siFe! %;P%:G ;$== @Iaranth and (ichols 1<<?A$
?

To test for a possible differential effect of the attractant on the t8o sexes or on different a*e classes

<8hich could bias the final estimates! the population estimates 8ere made separately for males and females! peer-00629072, version 1 - 5 Oct 2011 1;and for adult and non adult lynxes$ 6ollo8in* the recommendations of Iaranth and (ichols @%;;%A the 11hetero*eneity model @"hA 8as used since this most probably better reflects the beha iours of solitary cats! and 1%8ould pro ide a reasonable model for lynx capture probability @Ielly et al$ %;;?A$ This maJes biolo*ical 1+sense since most cats exhibit some de*ree of territoriality! 8ith home ran*e siFe and trap access aryin* and 11dependin* on the indi idualHs social position and spatial location in the landscape @,enschel and 5ay %;;+L 1>Iaranth and (ichols 1<<?!%;;%L Sil er et al$ %;;1A$ In addition to expectin* hetero*eneity of capture 1:probabilities! the use of "h is preferable! because the .acJBJnife estimator @Burnham and ) erton 1<=<A for 1=this model is robust to de iations from underlyin* model assumptions! and has performed 8ell in simulation 1?studies @)tis et al$ 1<=?L Burnham and ) erton 1<=<A$
1<

The population estimates obtained for lynx more than one year old! 8ere 11 females @SE: %$>:<=A

%;and 1% @SE: +$>1+:A males$ The sum of both estimates coincides 8ith that obtained from the combined matrix %1of males and females$
%%

The population estimates obtained for adult lynxes @S+ yearsA 8ere 1> indi iduals @SE:+$>1+A! and

%+1; indi iduals @SE:%$;>+A for non adults @T+yearsA$ The sum of both estimates is only one lynx less than the %1estimate obtained from the combined matrix$
%>

The mean maximum distances mo ed by indi idual Iberian lynx bet8een successi e captures 8ere

%:%$;1 Jm! pro idin* an outer bufferBstrip 8idth of 1$;% Jm $Thus! the effecti ely sampled area 8as :1?;+ ha$ %=The area occupied by the lynx 8as %>;:= ha$

1 %DIS-4SSI)( +-Iberian lynx population situation. 1

)ur results sho8 that in the Doana area! the total Iberian lynx population siFe is around %:

>indi iduals older than a year! occupyin* %>;:= ha$$ Despite the methodolo*ical differences 8ith the :&alomares et al$ @1<<1A study! 8here 1> indi iduals 8ere reported! a decline in the number of lynxes since the =1<?;s can be seen$
?

# fe8 years after the appearance of 5,D durin* the early 1<<;s! the estimated rabbit population

<decrease 8as about 1;U @3illafuerte et al$ 1<<1A$ #t present! the 8ild rabbit is almost completely absent in peer-00629072, version 1 - 5 Oct 2011 1;=>U of the entire area @GuFman et al$ %;;1A$ This rabbit population crash appears to be the principal cause of 11the lynx decline$
1%

#pproximately half of the Doana lynx population li es in only a 'uarter of its distribution area!

1+precisely 8here the best rabbit populations are located: alon* the northern (ational &arJ boundary and the 118estern limits of the (atural &arJ @GuFm2n et al$ %;;1A$
1>

This situation re eals a ne8 spatial distribution of lynx in the Doana area$ In the 1<?;s!

1:approximately ?;U of all lynx indi iduals 8ere found inside the (ational &arJ boundaries! another 1;U in 1=the ad.acent area! and the rest at some distance from it @&alomares et al$ 1<<1A$ In this study ho8e er! only 1?less than a half of the remainin* lynx indi iduals ha e been detected inside the (ational &arJ! and the species 1<has almost completely disappeared from the southern third of the (ational &arJ$ )nly one photo*raph has %;been obtained in this area! of a female 8hose resident area @8here it is re*ularly detectedA! is located %; Jm %1a8ay$
%%

The theory states that *i en the current estimate obtained! the population is not *enetically iable

%+@SoulM 1<?;L Shaffer and Samson 1<?>A$ In such small and isolated populations! the loss of *enetic ariability %1is accelerated @6ranJlin! 1<?;A! and so maJes them extremely fra*ile$ In fact! a recent study indicated that all %>lynxes necropsied bet8een 1<<? and %;;+ in the Doana area presented some de*ree of immunosuppression %:@&ea et al$ %;;:A and membranous *lomerulopathy! a pro*ressi e disease of immunolo*ical ori*in! 8as %=dia*nosed in all but one of the animals @0imeneF et al$ %;;?A$ The authors postulate a possible *enetic

<

1predisposition to8ards the disease! enhanced by inbreedin* and a possible connection to an immuneBmediated

%systemic disease$
+ 1- pplicability o! Camera-"rap Sur#eys. >

The present study probably represents the lar*est sur ey effort e er applied in a cameraBtrappin*

:study @>1+ camera trapsL 1:%<; trappin* ni*htsA$ #s a result! practically all of the Doana areaHs Iberian lynx =population distribution area 8as sur eyed in little more than % months$
?

The estimated a era*e capture probability @;$111>A! and the estimated probabilities of missin* an

<animal @1B"tP(T;$%>A are similar to those obtained from other studies on the ti*er @Iaranth and (ichols peer-00629072, version 1 - 5 Oct 2011 1;1<<?A! .a*uar @Ielly et al$ %;;?A and ocelot @Trolle and IMry %;;+A$
11

#ttractants are commonly used in captureBrecapture population estimates! includin* carni ores

1%@Trolle and IMry %;;+! ,enschel and 5ay %;;+A! deer @-urtis et al$ %;;<A and small mammals @Efford et al$ 1+%;;>A$ ,o8e er! some studies a oid the use of attractants because they can cause hetero*eneity in the 11captures @0acobson et al$ 1<<=A$ The model selection al*orithm identified "h as the most appropriate model! 1>sho8in* the existence of hetero*eneity in capture probabilities bet8een indi iduals *i en the social structure 1:and une'ual access to camera traps$ In addition! based on our data 8e can assume that the attractant used does 1=not produce a si*nificant differential effect neither on sex nor on a*e classes 8hich 8ould lead to chan*es in 1?the estimates$ Besides the effect of the possible ariability bet8een sexes! a*es or indi iduals is ade'uately 1<DbufferedE by applyin* the "h model of indi idual hetero*eneity! 8hich is Jno8n to be robust to iolation of %;underlyin* model assumptions @)tis et al$ 1<=?! Burnham and ) erton 1<=<A$
%1

)ne of the assumptions of captureBrecapture analysis is the absence of *aps in the study area that

%%8ere not sur eyed 8here any indi idual had cero probabilities of bein* captured @Iaranth and (ichols 1<<?A$ %+Thou*h in this study the entire area potentially used by Iberian lynx 8as sur eyed! there exist areas that 8ere %1not co ered in the camera trappin* sur ey$ These areas correspond 8ith open areas @a*ricultural areas or %>8ithout bush co erA or areas 8here rabbit is absent! that are re.ected by lynxes and considered inade'uate for %:the establishment of territories and that are used by dispersal indi iduals only @&alomares et al. %;;;A$ %=#lthou*h the probability that a lynx territory could ha e existed inside these areas that 8ere not sur eyed is

1;

1small! a disperser may ha e used them durin* the study$ This fact could suppose a iolation of the assumption

%and therefore could affect to the final estimation$

+

)ur study sho8s that as 8ith other carni ore species! photo*raphic captureBrecapture methods are

1applicable for estimatin* the abundance of Iberian lynx populations! as they are a fast! effecti e and nonB >in asi e method for establishin* the status of these populations$
:

The deployment of remote cameras offers a helpful means to obtain additional information$ -ameraB

=trappin* maJes it possible to establish the limits of the distribution area! to obtain information about the ?population sex ratio! and occasionally! to detect indi iduals 8ith poor body condition or 8hich are in.ured$ <This permits rapid response action for these indi iduals! if necessary$ peer-00629072, version 1 - 5 Oct 2011
1;

Oith successi e cameraBtrappin* sur eys it 8ould be possible to identify resident lynxes! i$e$ those

11indi iduals detected 8ithin the same area o er successi e seasons and years @,emJer et al$ 1<?1A$ This 1%information is especially important in the case of the females! since monitorin* resident females is the most 1+reliable means for assessin* the trend of a particular population @Iaranth and (ichols %;;%A$
11

There also appears to be a potential for usin* lon*Bterm cameraBtrappin* sur eys to estimate

1>additional population parameters such as sur i al! mortality! recruitment! and dispersal rates for Iberian lynx! 1:by applyin* open captureBrecapture models that are currently a ailable @Seber 1<?%! &ollocJ et al$ 1<<;! 1=Kebreton et al$ 1<<%A$
1?

#dditionally! remote monitorin* reduces ad erse effects that may be caused by more in asi e

1<methods includin* complications due to capture! destructi e marJin* techni'ues! and also reduces %;beha ioural chan*es due to the capture or marJin* process @,eilbrun et al$ %;;:A$
%1

-onsiderin* our results! 8e recommend to conduct sur eys of at least one month len*th @time

%%necessary to stabiliFe the cumulati e cur eA! 8ith a density of 1 trapP1;; ha and co erin* the bi**est area in %+consecuti e sta*es to co er the 8hole study area$
%1 %>-Conclusions %:

11

#s in the rest of its distribution area! the Iberian lynx in Doana has suffered a decline lea in* it in a

%critical situation! compromisin* its lon*Bterm sur i al and placin* it on the ed*e of extinction$ Traditionally! +the ma.ority of the research studies! as 8ell as conser ation 8orJ undertaJen on the Doana population! ha e 1been carried out 8ithin the (ational &arJ boundaries @e$*$ 6erreras et al$ 1<<=L KopeFBBao et al$ %;;?L >&alomares et al$ 1<<:! %;;1A! 8here hi*her le els of protection are present and disturbance to the species is :minimal$ ,o8e er! *i en the ne8 spatial distribution sho8n by the Doana population! the sur i al of the =species inexorably re'uires the implementation of ade'uate mana*ement beyond the (ational &arJ ?boundaries$ #nd this implies continuous monitorin* of its populations throu*hout its entire distribution area$ <This study has re ealed the applicability of cameraBtrap sur eys for maJin* rapid! efficient and nonBin asi e peer-00629072, version 1 - 5 Oct 2011 1;population estimates of the species$ Establishin* a repeated and consistent monitorin* pro*ram employin* 11cameraBtrappin* could be an essential tool to detect population andPor ran*e chan*es and for properly 1%assessin* the effecti eness of conser ation in estments tar*etin* the Iberian lynx$
1+ 11#-I()OKEDG"E(TS 1> 1:

The field8orJ and the economic support 8as possible throu*h the collaboration bet8een the

1=Direccin General de -onser acin de la (aturaleFa @DG-)(#B"I"#"! pro.ect D-ensoBDia*nstico de las 1?&oblaciones de Kince IbMrico en la &en/nsula IbMricaEA! )r*anismo #utnomo de &ar'ues (acionalesB 1<Doana! &ar'ue (atural de Doana! Dele*acin &ro incial de "edioambiente de ,uel a! and T5#GS#$ Oe %;thanJ 0$#$ Blanco D0E! E$ 3ir*s! 0$K$Teller/a and the anonymous re ie8ers for their constructi e comments! %1and also 5amn &MreF de #yala GimMneF! 5icardo BalFola! 0ohn "uddeman and Volanda -ortMs 8ho helped %%8ith the translation$
%+ %15E6E5E(-ES$ %> %:#non @1<?<A &lan (acional de -oordinacin de Doana y su entorno$ -onse.er/a de obras &Cblicas y

%=Transporte$ 0unta de #ndaluc/a! Se illa$

1%

1 %Burnham I&! ) erton O S @1<=<A 5obust Estimation of &opulation SiFe Ohen -apture &robabilities 3ary

+#mon* #nimals$ Ecolo*y :;: <%=B<+:

1 >-abrera # @1<11A 6auna ibMrica$ "am/feros$ "useo (acional de -iencias (aturales! "adrid$ : =-utler TK! S8ann DE @1<<<A 4sin* remote photo*raphy in 8ildlife ecolo*y: a re ie8$ Oildl Soc Bul %=:

?>=1B>?1$
<

peer-00629072, version 1 - 5 Oct 2011

1;-urtis &D! Bold*i B! "attison &"! Boulan*er 05 @%;;<A$ Estimatin* deer abundance in suburban areas 8ith

11infraredBtri**ered cameras$ ,um$ Oildl$ -onf$ +:11:B1%?$

1% 1+ Efford "G! Oarburton B! -oleman "-! BarJer 50 @%;;>A$ # field test of t8o methods for density 11Estimation$ Oildl Soc Bul ++:=+1N=+? 1> 1:6ranJlin I5 @1<?;A E olutionary chan*e in small populations$ In! -onser ation Biolo*y! #n E olutionaryB

1=Ecolo*ical &erspecti e "E Soule W Oilcox B#! Eds$ Sinauer! Sunderland! "# 1+>B11<$
1? 1<6erreras &! #ldama 0! Beltr2n 06! Delibes " @1<<=A Spatial or*aniFation and land tenure system of the

%;endan*ered Iberian lynx @Lynx pardinus$! TemmincJ! 1?%1A$ 0 Qool %1+: 1:+B1?<$
%1 %%6erreras & @%;;1A Kandscape structure and asymmetrical interBpatch connecti ity in a metapopulation of the

%+endan*ered Iberian lynx$ Biol -onser 1;;: 1%>B1+:

%1 %>Garrote G! Garc/a 60! GuFm2n 0(! &ereF de #yala! -! I*lesias -! &ereira &! 5obles 6 @%;;1A$ #plicacin de

%:tMcnicas de autofoto*raf/a en traba.os de conser acin de especies amenaFadas$ El caso del lince ibMrico %=@Lynx pardinusA$ $ 3I .ornadas de la Sociedad Espaola de -onser acin y Estudio de "am/feros$ 3itoriaB

1+

1GasteiF$ % +Gibbs 0& @%;;;A "onitorin* populations$ &a*es %1+N%>% in K$ Boitani and T$I$ 6uller! editors$ 5esearch

1techni'ues in animal ecolo*y$ -olumbia 4ni ersity &ress! (e8 VorJ! (e8 VorJ! 4S#$
> :Graells "& @1?<=A 6auna mastoFoolo*ica ibMrica$ "em 5ea$ #ca$ -iencias X3II$ "adrid$ = ?GuFm2n 0(! Garc/a 60! Garrote G! &MreF de #yala 5! I*lesias -$ @%;;1A$ El lince ibMrico @Lynx pardinusA en

<Espaa y &ortu*al$ -enso dia*nstico de sus poblaciones$ Direccin General para la Biodi ersidad$ "adrid$ peer-00629072, version 1 - 5 Oct 2011
1; 11,eilbrun 5D! Sil y (0! &eterson "0! Te8es "E @%;;:A Estimatin* bobcat abundance usin* automatically

1%tri**ered cameras$ Oildl Soc Bul +1::<N=+$

1+ 11,emJer T&! KindFey 6G! #cJerman BB @1<?1A &opulation characteristics and mo enments patterns of

1>cou*ars in southern 4tah$ 0 Oildl "ana* 1?:1%=>B1%?1

1: 1=,enschel &! 5ay 0 @%;;+A Keopards in #frican 5ainforests: Sur ey and "onitorin* Techni'ues$ O-S Global

1?-arni ore &ro*ram$ Oildlife -onser ation Society$

1< %;I4-( @%;;%A %;;% I4-( 5ed Kist of Threatened #nimals$ I4-(! Gland and -ambrid*e$ %1 %%I4-( @%;;=A %;;= I4-( 5ed Kist of Threatened #nimals$ I4-(! Gland and -ambrid*e$ %+ %10acJson 5"! 5oe 0D! Oan*chuJ 5! ,unter D) @%;;:A$ Estimatin* Sno8 Keopard &opulation #bundance

%>4sin* &hoto*raphy and -aptureB5ecapture Techni'ues$ Oildl Soc Bul +1: ==%B=?1$
%: %=0acobson ,#! Iroll 0-! Bro8nin* 5O! Ioerth B,! -on8ay ", @1<<=A$ InfraredBtri**ered cameras for

11

1censusin* 8hiteBtailed deer$ Oildl Soc Bul %>:>1=N>>:$ % +0imMneF "#! S2ncheF B! &MreF #lenFa "D! Garc/a &! KpeF 03! 5odri*ueF #! "unF! #! "art/neF 6!

13ar*as #! &ea K$ @%;;?A$ "embranous *lomerulonephritis in the Iberian lynx @Lynx pardinusA$ 3et >Immunol Immunopathol 1%1: +1N1+
: =Iaranth I4! (ichols 0D @1<<?A Estimation of ti*er Densities in India usin* photo*raphic captures and

?recaptures$ Ecolo*y =<:%?>%B%?:%$

<

peer-00629072, version 1 - 5 Oct 2011

1;Iaranth I4! (ichols 0D @edsA @%;;%A$ "onitorin* ti*ers and their prey: a manual for researchers! mana*ers

11and conser ationists in tropical #sia$ -entre for Oildlife Studies$ Ban*alore! India$
1% 1+Ielly "0! (oss #0! #rispe K! Di Bitetti "! De #n*elo -D! &a iolo #! Di Blanco VE! "affei K @%;;?A$

11Estimatin* puma densities from remote cameras across three study sites:Boli ia! #r*entina! and BeliFe$ 0 1>"ammal ?<:1;?B11?$
1: 1=Kancia 5#! (ichols 0D! &ollocJ I, @1<<1A Estimatin* the number of animals in 8ildlife 1?populations$ &p$ %1>B%>+$ In: T$#$ BooJhout @ed$A$ 5esearch and mana*ement techni'ues 1<for 8ildlife and habitats$ The Oildlife Society! Bethesda @"d$A$ %; %1Kebreton 0D! Brunham I&! -lobert 0 W #nderson D5 @1<<%A "odelin* sur i al and testin* biolo*ical

%%hypotheses usin* marJed animals: a unified approach 8ith case studies$ Ecol "ono*r :%::=B11?$
%+ %1KopeFBBao 03! 5odrY*ueF #! &alomares 6 @%;;?A$ Beha ioural response of a trophic specialist! the Iberian

%>lynx! to supplementary food: &atterns of food use and implications for conser ation$ Biol$ -onser 111: %:1?>=N1?:=
%=

1>

1"itchellB0ones #0! #mori G! Bo*dano8icF O! IrystufeJ B! 5ei.nders &0,! SpitFenber*er 6! Stubbe 0!

%Thissen 0B"! 3ohraliJ 3! Qima 0 @1<<<A The #tlas of European "ammals$ T$ #nd #$ D$ &oyser +Ktd$PSocietas Europaea "ammalo*ica! Kondon! 4I$
1 >"urray DK! 6uller "5 @%;;;A # critical re ie8 of the effects of marJin* on the biolo*y of ertebrates$ 1>N

::1 K$ Boitani! and T$ I$ 6uller! editors$ 5esearch techni'ues in animal ecolo*y$ -olumbia 4ni ersity &ress! =(e8 VorJ! (e8 VorJ! 4S#$
? <)tis DK! Burnham G! Ohite -! #nderson D5 @1<=?A Statistical inference from capture data on closed animal

peer-00629072, version 1 - 5 Oct 2011

1;populations$ Oildl "ono*r :%: 1B1+>$

11 1%&alomares 6! 5odri*ueF #! Kaffite 5! Delibes " @1<<1A The Status and Distribution of the Iberian Kynx Felis

1+pardina @TemmincJA in -oto de Doana! SO Spain$ Biol -onser >=: 1><B1:<$

11 1>&alomares 6! 6erreras &! 6edriani 0"! Delibes " @1<<:A Spatial relationships bet8een Iberian lynx and other

1:carni ores in an area of southB8estern Spain$ % pp &col ++:>B1+$

1= 1?&alomares 6! Delibes "! 6erreras &! 6edriani 0"! -alFada 0! 5e illa E @%;;;A$ Iberian Kynx in a 6ra*mented

1<Kandscape: &redispersal! Dispersal! and &ostdispersal ,abitats$ -ons$ Biol$ 3ol 11! +: ?;<B?1?$
%; %%&alomares 6! Delibes "! 5e illa E! -alFada 0! 6edriani 0" @%;;1A Spatial ecolo*y of Iberian lynx and

%+abundance of European
%1rabbits in south8ester Spain$ Oildl "ono*r 11?: 1B+>$ %> %:&ea K! Garc/a &! 0imMneF "#! Benito #! &MreF #lenFa "D! S2ncheF B @%;;:A ,istopatholo*ical and

%=immunohistochemical findin*s in lymphoid tissues of the endan*ered Iberian lynx @Kynx pardinusA$ -omp$ %?Immunol$ "icrobial$ Infect$ Dis$ %<:111N 1%:$

1:

1 %&eterson "(! KopeF 55! 6ranJ &#! &eterson "0! Sil y (0 @%;;+A E aluatin* capture methods for urban

+8hiteBtailed deer$ Oildl Soc Bul +1: 11=:N11?=$

: =&ollocJ I,! (ichols 0D! Bro8nie -! ,ines 0E @1<<;A Statistical inference for captureBrecapture experiments$

?Oildl "ono*r 1;=: 1B<=

< 1;5au 05! Beltr2n 06! Delibes " @1<?>A -an the increase of fox density explain the decrease in lynx numbers at

11DoanaZ$ 5e $Ecol$ @Terre ieA 1;: 11>B>;$ peer-00629072, version 1 - 5 Oct 2011
1% 1+5exstad E! Burnham I& @1<<1A 4serHs *uide for interacti e pro*ram -#&T45E$ #bundance estimation 11of closed populations$ -olorado State 4ni ersity! 6ort -ollins! -olorado! 4S#$ 1> 1:5i asN"art/neF S @1<?=A "emoria del "apa de Series de 3e*etacin de Espaa$ 1: 1;;;;;$ I-)(#$ "adrid$ 1= 1?5odr/*ueF #! Delibes " @1<<%A$ -urrent ran*e and status of the Iberian Kynx 6elis pardina TemmincJ! 1?%1

1<in Spain$ Biol -onser :1: 1?<B1<:$

%; %15odr/*ueF #! Delibes " @%;;+A &opulation fra*mentation and extinction in the Iberian lynx$ Biol -onser

%%1;<: +%1B++1$
%+ %1Seber G#6 @1<?%A The estimation of animal abundance and related parameters$ Second edition$ "ac"illan!

%>(e8 VorJ! (e8 VorJ! 4S#$

%: %=Shaffer "K! Samson 6B @1<?>A &opulation siFe and extintion: a note on determinin* critical population siFes$

%?#mer (at 1%>: 111B>%$

%<

1=

1Sil er S-! )str KET! "arsh K$I! "affei K! (oss #0! Ielly "0! Oallace 5B! GomeF ,! #yala G @%;;1A The

%use of camera traps for estimatin* .a*uar &anthera onca abundance and density usin* capturePrecapture +analysis$ )ryx +?: 11?B1>1$
1 >Simn "# @%;;?A -urrente status of Iberian lynx in #ndalusia$ &roceedin*s of the III Iberian Kynx

:International Seminar$ #ndalusia Go emment! I4-(PS- -ats Specialist Group$

= ?Soisalo "S! -a alcanti S"- @%;;:A Estimatin* the density of a .a*uar population in the BraFilian &antanal

<usin* cameraBtraps and captureBrecapture samplin* in combination 8ith G&S radioBtelemetry$ Biol -onser peer-00629072, version 1 - 5 Oct 2011 1;1%<: 1?=B1<:$
11 1%SoulM "E$ @1<?;A Thresholds for sur i al: maintainin* fitness and e olutionary potential$ In -onser ation

1+Biolo*y: #n E olutionaryBEcolo*ical &erspecti e! ed$ "$E$ SoulM W B$#$ Oilcox$ Sinauer #ssociates! 11Sunderland! "assachusetts 1>1B:<$
1> 1:Trolle "! IMry " @%;;+A Estimation of ocelot density in the pantanal usin* captureBrecapture analysis of

1=cameraBtrappin* data$ 0 "amm ?1: :;=B:11$

1? 1<3al erde 0# @1<:+A Informacin sobre el lince en Espaa$ "in$ #*ric$ Bol$ Tec$! Ser$ -ine*Mtica! 1$ %; %13illafuerte 5! -al ete -! Gort2Far -! "oreno S @1<<1A$ 6irst epiFooty of 5abbit ,aemorra*ic Disease on free

%%li in* populations at Doana (ational &arJ @SO SpainA$ 0 Oildl Dis +;: 1=:B1=<$
%+ %1Ohite G-! Burnham I& @1<<<A &ro*ram "#5I: sur i al estimation from populations of marJed animals$

%>Bird Study 1::1%;N1+?$

%: %= QielinsJi O0! Iucera TE @1<<>A #merican "arten! 6isher!Kynx! and Ool erine: Sur ey "ethods for Their

1?

1Detection$ 4SD# 6orest Ser ice General Technical 5eport &SO GT5B1>=$

peer-00629072, version 1 - 5 Oct 2011

1<

peer-00629072, version 1 - 5 Oct 2011

1
% +(ig "$B Sur ey area in Doana (ational &arJ @discontinuous lineA! Doana (atural &arJ @continuous lineA and

1peripheral area sho8in* camera trap layout @*rey dotA$ -amera trap 8ith Iberian lynx photo*raph @9A$

%;

25 20 Indi iduals 15 10 5

(ig '-

peer-00629072, version 1 - 5 Oct 2011

0 1 + > = < 11 1+ 1> 1= Days 1< %1 %+ %> %= %<

>-umulati e cur e for photoBidentified Iberian lynx$ Days from the start of cameraBtrappin* @x axisA ersus :photoBidentified indi iduals @y axisA$

%1

Indi/idual IK;1 IK;% IK;+ IK;1 IK;> IK;:

7rapping 8ccasions 1 > > 1 + 1 1 1 + 1 1 > 1< % 1 1> 1% = % 1

&ge #dult #dult #dult #dult #dult #dult #dult #dult #dult #dult #dult #dult Indet$ T+ years T+ years T% years T% years T% years T% years T% years

Sex 6emale 6emale 6emale 6emale 6emale 6emale 6emale "ale "ale "ale "ale "ale 6emale 6emale "ale 6emale 6emale 6emale "ale "ale

peer-00629072, version 1 - 5 Oct 2011

IK;= IK;? IK;< IK1; IK11 IK1% IK1+ IK11 IK1> IK1: IK1= IK1? IK1< IK%;
%

+Table 1$ Summary of cameraBtrappin* results$ (umber of trappin* occasions! a*e and sex of each indi idual

1photo*raphed$

%%