ORIGINAL PAPER

Influence of predation risk and plant structureon vigilance and intermittent locomotionin Microcavia australis (Rodentia, Caviidae)

Paula Taraborelli & Pablo Moreno & Ana Srur &

Carolina Carballido & Stella M. Giannoni

Received: 30 April 2009 /Revised: 10 June 2010 /Accepted: 3 November 2010 /Published online: 14 December 2010# Springer-Verlag and ISPA 2010

Abstract The aim of this study was to analyze and comparevigilance behavior and intermittent locomotion at two sites (ElLeoncito and Ñacuñán, Argentina) that differ in predationrisk, plant structure, and plant resource availability. Subjectswere lesser cavies (Microcavia australis), a social speciesthat is semi-fossorial, diurnal, and native to South America.Continuous focal sampling was conducted during the day, attimes of food shortage, food abundance, and reproductionfrom 2003 to 2005. The proportion of time spent vigilancewas significantly higher at Ñacuñán, where vigilance peakedat midday and reached a minimum in the evening. Thismidday peak of vigilance at Ñacuñán was associated with amidday peak of danger from raptors as indicated by a raptoractivity peak at that time. In contrast, both vigilance andpredator activity at El Leoncito were constant through theday. Records of intermittent locomotion and number andduration of pauses in locomotion were significantly higher at

El Leoncito, a difference that may have been due to the needfor greater vigilance while moving across areas of lessprotective cover at this site.

Keywords Vigilance . Intermittent locomotion . Plantstructure . Predation risk .Microcavia australis

Introduction

Several aspects of rodent behavior and ecology support aninverse relationship between the amount of plant cover andpredatory risk (Ebensperger 2001). Predation risk increasessignificantly in open areas (Lima 1987). Other authorssupport that an increase in the rate of predator attacksresults in an increase in vigilance levels (Lima 1987; Elgar1989; Sundell and Ylönen 2004). Vigilance is a behaviorthat enhances the likelihood that an animal will detect agiven stimulus at a given time (Dimond and Lazarus 1974).Another antipredator behavior is the mode of locomotionemployed by rodents, which plays a vital role in determin-ing their ability to elude predators (Thompson 1985;Djawdan and Garland 1988; Taraborelli et al. 2003a). Thestructural complexity of the habitat may affect movementbehavior by: (1) physically impeding locomotion (Schooleyet al. 1996), (2) making movement more conspicuous andthus riskier (Brillhart and Kaufman 1991; Borruel et al.unpublished data), (3) providing a higher density ofresources, hence favoring lower speeds so that resourceopportunities are not missed (Brownsmith 1977), (4)increasing protection against predators through hidingcover (Thompson 1982; Taraborelli et al. 2003b), (5)increasing visual obstruction, thus reducing the ability todetect predators (Schooley et al. 1996; Ebensperger andHurtado 2005).

P. Taraborelli (*) : P. MorenoGrupo de Investigaciones de la Biodiversidad, Instituto Argentinode Investigaciones de Zonas Áridas, CCT, CONICET,Av. Ruiz Leal s/n, Parque General San Martín, CC 507,CP 5500, Mendoza, Argentinae-mail: paulataraborelli@gmail.com

S. M. GiannoniInstituto y Museo de Ciencias Naturales,Universidad Nacional de San Juan,Av. España 400 Norte,San Juan, Argentina CP 5400

A. SrurDendrocronología-IANIGLA-CCT, CONICET,Mendoza, Argentina CP 5500

C. CarballidoFacultad de Ciencias Exactas y Naturales, UBA,Buenos Aires, Argentina C1428EGA

acta ethol (2011) 14:27–33DOI 10.1007/s10211-010-0087-0

Many animals do not continuously move through theirhabitat, but show an overall pattern of intermittentlocomotion (Pennisi 2000; Vásquez et al. 2002). Intermit-tent locomotion, as is called by MacAdam and Kramer(1998), Pennisi (2000), Kramer and McLaughlin (2001),Vásquez et al. (2002) and Trouilloud et al. (2004), consistsof pauses, lasting from milliseconds to minutes, that breakup movement bursts and enable animals to scan thesurroundings (e.g., Sciurus carolinensis, Tamias striatus,and Octodon degus). Thus, pauses, along with changes inthe duration and speed of moves, form part of a dynamicsystem of intermittent locomotion whereby animals adjusttheir locomotor behavior to changing circumstances(Kramer and McLaughlin 2001).

The use of pauses may enable animals to increasepredator detection (MacAdam and Kramer 1998; Kramerand McLaughlin 2001; Trouilloud et al. 2004). Pauseswould last a longer time in open habitats, high-risk areas,and would play an antipredator role because they wouldenhance efficiency in detecting predators and in the abilityto escape (Vásquez et al. 2002). Pauses may also help preybecome more cryptic and reduce the capture ability ofpredators when they are more likely to perceive and/orattack moving prey (Curio 1976) and may provide cavieswith chances to acquire orientation cues for moving acrossthe habitat (Dyer 1998). From a physiological viewpoint,pausing may serve as a resting stage (Weinstein and Full1992). Pauses, aside from providing direction-finding cuesor physiological recovery, may also contribute to informa-tion processing and enhanced predator detection (Dukas1998).

The purpose of this study was to assess the influence ofpredator abundance and plant structure on vigilance andintermittent locomotion in the rodent Microcavia australis(Rodentia, Hystricognate, Caviidae, common name: lessercavy). M. australis is a semi-fossorial herbivore native toSouth America, with diurnal habits, a burrowing rodentexhibiting a group social structure with low levels ofaggressiveness (Rood 1967). It dwells specifically in aridshrub areas and sandy scrublands (Olrog and Lucero 1986;Canevari and Fernández Balboa 2003). Groups are com-posed of several females, one or few males, plus the youngand juveniles (Rood 1967 and 1972). In the Central Monte,the social groups were formed by three to six cavies(Taraborelli and Moreno 2009). Rood (1972) and Taraborelliand Moreno (2009) assert that the mating system in thisspecies is promiscuous, that females mate indiscriminatelywith any male, and cavies show absence of sexualdimorphism. This cavy displays its behavioral patterns inthe burrow area, under the cover provided by trees and/orshrubs where predation risks are lower (Rood 1967; Tognelliet al. 1995). Each group is associated with a burrow and thegroups are permanent, not transitory (Taraborelli 2006). The

fact that cavies congregate underground during the night andmaintain stable associations confirms that this species nestscommunally and suggests that nesting associations representdistinct social units (Ebensperger et al. 2006). Groups of M.australis are not organized according to hierarchies (pers.obs.). When confronted with predators, the cavies react witha higher frequency of vigilance behavior and by fleeingtowards the burrow and/or by hiding in galleries, but not byrepelling the predators (Taraborelli et al. 2008). The caviesnever emit alarm calls in response to the presence of apredator but simply respond with an alert posture (Taraborelli2006, 2008). Therefore, the objective is to analyze andcompare vigilance behavior and intermittent locomotion ofM. australis in two populations located on two sites (ElLeoncito and Ñacuñán, Argentina) differing in predationrisk, plant structure, and plant availability. A specificobjective is to record predators on both sites. One proposedprediction is that on sites with wide open areas (El Leoncito)the number of records of intermittent locomotion andpausing events will be higher. The other prediction is thatvigilance will be used in response to predation risk andtherefore, on both sites, vigilance time will increase withhigher predation risk.

Materials and methods

Study sites

The study was conducted in a population of M. australis inthe Monte semiarid desert, in the Man and BiosphereReserve of Ñacuñán (34° 2’ S, 67° 58’ W, 12,300 ha,540 m asl) in the central-west of Mendoza (Argentina,Ojeda et al. 1998). The climate is warm–dry semiarid; meanannual precipitation is 329.4 mm, with 50% occurring inthe summer months (Cabrera 1976; Estrella et al. 2001).The mesquite plant community is the most extensive andcomplex, composed of three plant layers, the tree layer, theshrub layer, and the very species-rich herb layer (Roig1971). Total plant cover is 54.3% (Taraborelli 2006).Potential predators are diurnal and nocturnal raptors,carnivores, and reptiles (Contreras and Roig 1979; Ojedaet al. 1998).

The second population dwells in the arid Monte of ElLeoncito National Park (31º 47´ S, 69º 17´ W; 76,000 ha,2484 m asl), in the southeast of San Juan province (Argentina,Márquez 1999). The climate is cold dry arid, with strongdiurnal, nocturnal, and seasonal temperature ranges (Braccoand Contreras 2000; Márquez and Dalmasso 2003). Meanannual precipitations do not exceed 100 mm, in the form ofsnow and hail in winter, reaching 75 mm, and in the form ofrain and lower than 10 mm in summer (Le Houérou 1999).In the Monte of El Leoncito, there occurs a shrubland of

28 acta ethol (2011) 14:27–33

Larrea nitida with low cover (10%); the herb layer is lowerthan 10 cm in height (Márquez et al. 2000; Márquez andDalmasso 2003). Total plant cover is 21.9% and most of theland is barren (Taraborelli 2006). Similar to the first site,potential predators include carnivores, diurnal, and nocturnalraptors, as well as reptiles (Márquez 1999).

Records of predators

Records of predators were searched and taken from foot-prints, feces, and raptor castings in the study areas. Also,the records were from direct observations during themorning: 8:00–1:00 h, midday, 11:00–14:00 h, afternoon14:00–17:00 h, evening: 17:00-20:00 h. Direct observationswere carried out during 7–11 days at three times of the year(time of food abundance: November–February, food shortage:April–August, and reproduction: September–March) for eachstudy site from 2003 through 2005. And the number of cavieswas gotten from capture, tagging, and recapture, settingHavahart traps (25×30×91 and 18×18×76 cm; Havahart,Lititz, Pennsylvania) and Tomahawk traps (15×15×60 cm;Tomahawk live trap Nº 202/203, Tomahawk, USA). The trapswere set up on activity paths and around burrows (Rood 1972;Hoogland 1995). Subjects were individualized by numberedmetal ear tags (0.6×0.2×0.05 cm; National Bandand Tag Co.Newport, USA), by painting part of the body with innocuouspaint, depending on sex, and by making diverse drawings onthem, for example, circles, squares, vertical or horizontallines, letters, etc. (35 adults at El Leoncito and 11 adults atÑacuñán). Gentian violet was used to paint the cavies; thissubstance is not toxic and is used to cure fungi. Neithertagging nor painting has a negative effect for animal welfare,as corroborated by Hoogland (1981), Cassini (1989), Branch(1993), Meserve et al. (1993), Hoogland (1995), Ebenspergerand Hurtado (2005), and Ebensperger et al. (2006).

The contents of collected feces and raptor castings wereanalyzed in the laboratory under magnifying glass; specieswere identified by their molar teeth using keys foridentifying small mammals, guidebooks, skulls in theIADIZA-CRICYT Collection and photographs (Olrog andLucero 1986; Pearson 1995). The collected feces ofpredators and raptor castings with cavies' bones and hairswere taken as a record of predation. Then, all predationrecords from direct observations, footprints, feces, andraptor castings were associated with time of the day andseason of the year. Predation rates on cavies were calculatedfor each time of the year, and then, we estimated the meanand standard error for all data.

Behavior samplings

Quantification of vigilance behavior and intermittentlocomotion was achieved through focal samplings (focal-

continuous, Altmann 1974; Martin and Bateson 1993;Lehner 1996). Observations were made with binoculars(8×40, Hoken, Wald S.A., China), tape-recorded (usingvoice), and video-taped (Canon ZR-80) from an observa-tion tower 2 m high and 30–50 m away from the burrows.They were taken as of 8:00–13:30 till 14:30–20:30 h(morning, midday, afternoon, evening) over 3–4 days atthree times of the year for each study site from 2003through 2005.

These behaviors were defined as: Vigilance: alert posturethat involves a quadrupedal posture, typically the animal“freezes” with its front legs extended and turns toward thestimulus (Rood 1972; Taraborelli 2006). Intermittentlocomotion: slow or fast moves with the body and headclose to the ground, interrupted every two or three steps byshort pauses where the head adopts an erect position in anattitude of vigilance, and so on (MacAdam and Kramer1998; Pennisi 2000; Kramer and McLaughlin 2001;Vásquez et al. 2002; Taraborelli 2006).

The duration and frequency of vigilance behavior andintermittent locomotion (moves and pauses) were recordedfor each animal on each sampling date. Number andduration of stops or pauses in intermittent locomotion wererecorded as well. Frequency is the total number ofoccurrences of a behavior (Martin and Bateson 1993). Forcomparing behaviors between sites, rates (frequency ofbehavior/observation period in minutes), and proportions(duration of behavior in minutes/observation period inminutes) were obtained for each site (Martin and Bateson1993). Observations were changed among adult cavies thatwere alone or accompanied by more individuals of thegroup and not repeated for a same individual or group ofcavies. We used only the first observation of eachindividual.

Statistical analysis

The χ2 test was applied to compare the records ofpredators throughout the day at both sites, and Pearsonresiduals (r = f observed – f expected/√f expected) wereused to find differences between said records. TheKruskal–Wallis test was employed to search for differ-ences in predation rates on cavies among the periods ofthe year at both study sites. ANCOVA was used tocompare the mean rates and proportions of behaviors(vigilance, intermittent locomotion, and pauses made perintermittent locomotion event), between sites, times of theyear, and times of the day. ANCOVAwas applied to checkfor differences between sites in the rate of stops perintermittent locomotion. Group size was the covariance.Post hoc tests (Tukey test, p<0.05) were performed amongthe variables considered. Results are expressed as sam-pling mean ± standard error.

acta ethol (2011) 14:27–33 29

Results

Record of predators

The density of cavies was 7.22±0.5 adults/ha at El Leoncitoand 1.91±0.22 adults/ha at Ñacuñán. There were no differ-ences in the predation rate on cavies among the periods of theyear for each site (Ñacuñán: Kruskal–Wallis test, H=1.88,df=2, p=0.501; El Leoncito, Kruskal–Wallis test, H=1.22,df=2, p=0.332). A total of nine groups were defined atNácuñán and 13 at El Leoncito. Social groups were formedby 5–6 individuals at El Leoncito and 3–4 at Ñacuñán.

Predators at Ñacuñán are diurnal raptors all throughoutthe year (Buteo polyosoma, Milvago chimango, 23 totalrecords) with a peak of records at midday, 1.1±0.15raptors/cavy (mean ± standard error), followed by themorning and the afternoon, 0.5±0.1 raptors/cavy, and lowerrecords in the evening 0.3±0 raptors/cavy. And mammaliancarnivores (Lycalopex gymnocercus, Galictis cuja, Con-epatus chinga, Felis catus, seven total records) are the otherpredators, with 0.09±0.05 carnivores/cavy.

Predation risk at El Leoncito is constant throughout theday (χ2=28.27, df=3, p=0.00003). Predators recordedacross the year at El Leoncito are crepuscular and nocturnalmammalian carnivores (25 total records) with 0.21±0.05carnivores/cavy, such as Lycalopex sp. (records of Lycalo-pex culpaeus are the highest) and P. concolor. Diurnalraptors (Athene cunicularia, Geranoaetus melanoleucus,Buteo polysoma, Falco femoralis, Falco sparverius, Circuscinereus, 24 total records) were recorded from the morningto the afternoon, with 0.20±0.09 raptors/cavy.

Small cavies compose about 44% of the diet ofLycalopex sp. and 45% of the diet of P. concolor at ElLeoncito. At Ñacuñán, the cavy was not observed to beincluded in the diet of A. cunicularia or in the diet ofLycalopex sp.

Behavior samplings

The vigilance behavior was observed in cavies located on theedge of the vegetation, under shrubs, and/or trees or in openspaces (Ñacuñán, 11 adults and five pair of individualsobserved, El Leoncito, 28 adults and 23 pairs of individualsobserved). Concerning vigilance proportion between sites,proportion (duration) was significantly higher at Ñacuñán(Ñacuñán 0.19±0.02 min/min, El Leoncito 0.12±0.01 min/min; F1=8.6, p=0.0036, df=1, N=67). A difference invigilance proportion along the day is observed only atÑacuñán, where the peak of vigilance is at midday, followedby the morning and afternoon, and vigilance behavior is lowin the evening; at El Leoncito, vigilance is constantthroughout the day (F3=1.07, p=0.021, df=3, N=67;Fig. 1). Vigilance showed no differences among times of

the year (rate. F2=0.18, p=0.833, df=2; N=67; proportion,F2=0.99, p=0.373, df=2, N=67).

On both sites, intermittent locomotion was observed inindividuals solely when going across open areas and when thecavy was alone or with only one more individual of the group.The intermittent locomotion was recorded in seven adults andfive pairs of cavies at Ñacuñán and 23 adults and 11 pairs ofindividuals at El Leoncito. Records (moves and pauses) weresignificantly higher at El Leoncito (34 and Ñacuñán 12). Onlyat Ñacuñán did the rate of intermittent locomotion vary alongthe day, where the peak of frequency of intermittent locomotionper minute occurred at midday, instead of in the morning andafternoon; on the other hand, at El Leoncito, this rate wasconstant throughout the day (F3=3.4, p=0.0219, df=3, N=46;Fig. 2). But, the proportion of this behavior did not changebetween periods of the day (F3=8.22, p=0.397, df=3, N=46).Moreover, there were no differences in intermittent locomo-tion between times of the year (rate F2=0.44, p=0.644, df=2,N=46; proportion F1=1.03, p=0.362, df=2, N=46).

With respect to the number of pauses per intermittentlocomotion event, the rate was found to be significantlyhigher at El Leoncito (19±1 pauses min−1, Ñacuñán 11±2pauses min−1; F1=1.12, p=0.03, df=1, N=46). Andproportion (duration) of pauses per intermittent locomotionwas also significantly higher at El Leoncito (0.17±0.01minutes/minutes, Ñacuñán 0.13±0.02 minutes/minutes; F1=4.02, p=0.034, df=1, N=46). Then, cavies spent approxi-mately 17% of their time making pauses at El Leoncito and13% of it at Ñacuñán.

Discussion

Antipredator responses in M. australis could be directlyrelated to the risk of predation on each site, as the duration

Ñacuñán

morning midday afternoon eveningPeriod of day

0.1

0.3

Pro

po

rtio

n o

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gila

nce

(m

in/m

in)

a

b

ab

c

a

b

aa

0

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0.4

El Leoncito

Fig. 1 Vigilance proportion (vigilance duration in minutes/minutes ofobservation) along the day at El Leoncito and Ñacuñán. a, b, cindicate significant differences (Tukey test p<0.05)

30 acta ethol (2011) 14:27–33

of the vigilance behavior is significantly higher at Ñacuñán,where the vigilance peak is at midday, followed by themorning and the afternoon, and where vigilance is low inthe evening. At Ñacuñán, the major risk of predation isfrom raptors, predators that overlap with the period ofactivity of cavies, with a peak of records at middayfollowed by the morning and the afternoon, and lowerrecords in the evening. And records of mammaliancarnivores are constant throughout the day (Taraborelli2006). At El Leoncito, both vigilance predation risk areconstant throughout the day. Raptors have been recordedfrom morning to afternoon and mammalian carnivoreswould be overlapping in the early morning and in theevening (Taraborelli 2006). Other studies and a standardmodel of optimal vigilance behavior have found that anincrease in the rate of predator attacks leads to an increasein vigilance (Lima 1987; Sundell and Ylönen 2004).Therefore, vigilance would respond to predation riskbecause vigilance time increases when the number ofpredator records is higher. Then, vigilance proportion couldbe an indicator of predation risk.

Cavies adjusted their locomotion behavior according tothe type of habitat used. Intermittent locomotion wasobserved for adults and juveniles on both sites, when theindividual was alone or with only one more individuals ofthe group and when going across open areas. Lima (1987)described that when distance to the plant cover increases,the likelihood of escaping decreases, since predators preferto attack in open areas. Therefore, the area of dangerincreases with distance from a refuge (Taylor 1998) becausepredation risk per time unit is higher in open places thannear or under shrubs (Djawdan and Garland 1988; Hughesand Ward 1993). At El Leoncito, records of intermittent

locomotion were higher than at Ñacuñán. This could be dueto the fact that open areas at El Leoncito are wider (80%approximately), and to the cavies moving from one burrowto another and in search for food among three to fourpatches of Larrea nitida, whereas cavies at Ñacuñánrestricted their activity to only one burrow under a complexplant structure (tree, shrub, and herb layers; Ebensperger etal. 2006; Taraborelli 2006). At El Leoncito, cavies travellonger distances than they do at Ñacuñán; for example, atEl Leoncito, distances traveled are 10–100 m, whereas atÑacuñán they are 6–17 m (Taraborelli 2006).

At El Leoncito, the number and duration of pauses perintermittent locomotion event was significantly higher thanat Ñacuñán. Cavies made 19±1 pauses min−1 and spent17% of their time in this stance at El Leoncito. At Ñacuñán,they made 11±2 pauses min−1, with pauses taking 13% oftheir time. For example, gray squirrels approaching a foodsource away from forest cover made 22 pauses min−1 andspent 35% of their time pausing, whereas those carrying anut to a site for hoarding under forest cover made 10 pausesmin−1, which took them 14% of their time. Pausingincreases with early detection of predators (MacAdam andKramer 1998). Longer pausing may increase the efficacy ofantipredator vigilance because it enhances predator detection.During pauses, cavies often adopted a crouching posturewith the head raised in an alert stance. This position mayallow M. australis to visually scan the surroundings,increasing their visual detection of dangerous events, andhence decreasing their reaction time to flee from potentialpredators, as it occurs in other social rodents (Blumstein1998; MacAdam and Kramer 1998; Kramer and McLaughlin2001; Trouilloud et al. 2004). Intermittent locomotion maybe advantageous, therefore, in providing brief periods ofvisual field stability (Kramer and McLaughlin 2001). Thestatic position adopted during pauses may also improvehearing performance in comparison to running behaviorwhen audition may be interfered by the noise generated bythe very movement of the animal (Kramer and McLaughlin2001; Vásquez et al. 2002). MacAdam and Kramer (1998)and Trouilloud et al. (2004) found that S. carolinensis and T.striatus increase their pauses with the head raised whenapproaching situations of higher risk, for instance whenforaging farther from their burrows. Vásquez et al. (2002)reported that the pauses in O. degus lasted longer in openhabitats and high-risk areas. And these interruptions wouldplay an antipredator role since they would improve anti-predator vigilance (Trouilloud et al. 2004).

Pauses might also make prey more cryptic and reducecapture ability if predators are more likely to detect and/orattack moving prey because such motionless periods mayalso reduce the probability that visually or auditorysensitive predators will detect the prey (Curio 1976; Kramerand McLaughlin 2001). Also, Vásquez et al. (2002) noted

morning midday afternoon eveningPeriod of day

Rat

e o

f in

term

itte

nt

loco

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tio

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Fre

q/m

in)

a

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ÑacuñánEl Leoncito

Fig. 2 Rate of intermittent locomotion (frequency of intermittentlocomotion/minutes of observation) along the day at El Leoncito andÑacuñán. a, b indicate significant differences (Tukey test p<0.05)

acta ethol (2011) 14:27–33 31

that it was far more difficult for the predator to detect amotionless degu than a moving one. Therefore, when aloneor with only one more individual of the group, M. australiswould adjust its antipredator behavior (e.g., intermittentlocomotion) according to the type of habitat used, partic-ularly when going across open areas where there aresituations of higher risk.

On the other hand, differences found between popula-tions might have an evolutionary explanation. Sassi(unpublished data) found that analyses of genetic differen-tiation (ISSR markers) for M. australis revealed that thepopulation at Ñacuñán constitutes a group and thatpopulations at El Leoncito compose a different group, sothere could be two separate gene pools, one at Ñacuñán andthe other one at El Leoncito. However, the levels of geneticvariability show that each population would maintain alarge effective size and a high level of intra- and inter-population polymorphism. From the genetic viewpoint,plasticity of this species would depend on the heterogeneityof the environment it has to cope with. In this respect,phenotypic plasticity plays a key role in the ecologicalsuccess of organisms and in the local adaptation of thespecies.

Acknowledgments This study was partially financed by CONICET,PICT Nº 03281, and PIP 02884. The authors wish to express theirthanks to M. C. González, N. Borruel, A.J. Sandobal, M. Martínez,and V. Bauni for their cooperation in the field. Thanks also to N.Horak for the English version of the manuscript and to Dr. R. Ojedafor his contributions in reviewing the manuscript and for the literatureprovided.

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