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Applied Animal Behaviour Science

journal homepage: www.elsevier.com/locate/applanim

Validation and welfare assessment of flipper-mounted time-depth recordersfor monitoring penguins in zoos and aquariumsGrace Fuller⁎, Matthew R. Heintz, Stephanie AllardCenter for Zoo and Aquarium Animal Welfare and Ethics, Detroit Zoological Society, 8450 W Ten Mile Rd Royal Oak, MI 48067, USA

A R T I C L E I N F O

Keywords:Data loggersBio-loggingGentoo penguinMacaroni penguinRockhopper penguinKing penguin

A B S T R A C T

The time that penguins devote to aquatic behaviors likely has important implications for their welfare in zoosand aquariums. For decades, field researchers have used time-depth recorders (TDRs) to understand the behaviorof penguins at sea. However, zoos and aquariums have rarely used these tools, and wearing devices can po-tentially affect animals negatively by causing discomfort or imposing energetic costs. We evaluated the long-term behavioral responses of 27 penguins (n= 8 king penguins, Aptenodytes patagonicus; n= 3 gentoo penguins,Pygoscelis papua ellsworthi; n= 8macaroni penguins, Eudyptes chrysolophus; and n=8 southern rockhopperpenguins, Eudyptes chrysocome) before, during, and after wearing TDRs in an ABA study design. Our novelmethod involved affixing the TDRs to a custom-designed cradle and securing them on the penguins using flipperbands, which the penguins were accustomed to wearing for identification. The experiment was repeated fourtimes, and we used a total of 399.5 h of behavioral observations to evaluate the effects of the TDRs on locomotor,comfort, and social behaviors. We also conducted observations with a second set of penguins (two of eachspecies) naïve to wearing TDRs to evaluate their acute responses following application of the devices. Finally, weconducted validation tests to assess the accuracy of TDRs in a freshwater pool. Penguins observed immediatelyafter the devices were applied to their flipper bands for the first time showed little device-directed behavior.However, there were some individual differences, suggesting that zoos and aquariums should carefully monitorinitial behavioral responses to TDRs. In the long term, wearing TDRs had few effects on the behavior of thepenguins. The penguins displayed almost no device-directed behavior, and there were few statistically sig-nificant differences in their behavior across the three study conditions. Seasonal changes and penguin weightlikely explained the increase in movement king penguins demonstrated after wearing TDRs (F2,58= 4.34,p= 0.02). King penguins also showed a small increase in agonistic behavior while wearing TDRs (F2,73 = 3.81,p= 0.03), a difference that may have been related to mating competition during the breeding season. Ourresults indicate that these flipper-mounted TDRs had few effects on the penguins, while providing valuableinformation about 24-hour use of aquatic resources in their freshwater habitats.

1. Introduction

Penguins are adapted for life as aquatic foragers, and their aquaticbehaviors may both indicate and affect their welfare. Wild penguinsspend much of their lives at sea; for example, macaroni penguins(Eudyptes chrysolophus) go the entire winter without returning to land(Green et al., 2005). Many species-appropriate behaviors, such as por-poising, only take place in the water (Clarke, 2003), and swimming inflocks may be an important social behavior (Mori, 1999). For penguinsliving in the care of humans, pool size and use are correlated with re-duced risks for health problems like pododermatitis (Erlacher-Reidet al., 2012) and with greater hatching success (Blay and Cote, 2001).These trends suggest that the ability to monitor pool use may be very

informative about the welfare of penguins living in zoos and aquariums(hereafter abbreviated as ‘zoos’).

Traditional methods for observing behavior can be limited by thedifficulty of identifying individual penguins swimming quickly under-water (Clarke, 2003), as well as visibility constraints due to habitatdesign. Data loggers, including devices that measure temperature,pressure, and acceleration, have been employed for decades to monitorthe aquatic behavior of penguins in situ but are less widely used in zoos.With the ability to monitor the timing, duration, and depths of swim-ming bouts automatically and continuously, these devices have greatpotential to provide information about the welfare of penguins living inthe care of humans.

Despite their widespread use, only around 15% of studies have

https://doi.org/10.1016/j.applanim.2019.01.002Received 4 July 2018; Received in revised form 24 December 2018; Accepted 3 January 2019

⁎ Corresponding author.E-mail address: gfuller@dzs.org (G. Fuller).

Applied Animal Behaviour Science xxx (xxxx) xxx–xxx

0168-1591/ © 2019 Elsevier B.V. All rights reserved.

Please cite this article as: Fuller, G., Applied Animal Behaviour Science, https://doi.org/10.1016/j.applanim.2019.01.002

Table1

Subjectcha

racteristic

sand

observationtim

elines.For

long

-term

mon

itoring

subjects,agesa

rebasedon

thefirstdate

time-depthrecorders(TD

Rs)w

eredeployed:A

pril25

,201

5.Weigh

tswereaveraged

acrosseach

ofthe

timeperiod

s(tw

oto

four

fore

achpeng

uin)

that

theeff

ectsof

theTD

Rswereassessed.Seven

TDRs

wererotatedam

ongsubjects.T

wodate

spansa

regivenfore

achtim

eperiod

,because

nota

llmem

bersof

agivenspecies

couldalwaysweara

tTDRat

theexactsam

etim

e.Dates

refle

ctthemaxim

umtim

eindividu

alsworethedata

loggers(som

etim

escaretakerscouldno

trem

ovethem

allo

nthesameday).D

eploym

entd

ates

werematched

fore

achsubjecta

ndseason

acrossstud

yyears.Fo

robservatio

nsof

acuterespon

sestoTD

Rapplication,

exacta

gesa

ndmostrecentw

eigh

ts(taken

betw

eenOctob

er–Decem

ber2

018)

areprovided.M

=male;F=

female.

SubjectGroup

Species

Num

berof

Males

Num

bero

fFem

ales

Body

Weigh

t(kg)

mean±

SD(range)

orexact

Age

(y)mean±

SD(range)or

exact

TDRDeploym

entD

ates

(MM/D

D/Y

Y;four

deployments

arelistedin

order)

Long

-term

Mon

itoring

King

(Aptenodytespatagonicus)

44

13.4

±2.0(11.7–18

.2)

17.8

±7.6(5.1

–27

.1)

16/8/15

–6/25

/15;

7/7/15

–7/24

/15

212

/4/15–12

/22/15

;1/2/16–1/19

/16

312

/6/16–12

/22/16

;1/3/17–1/18

/17

46/8/17

–6/28

/17;

7/8/17

–7/23

/17

Gentoo(Pygoscelispapuaellsworthi)

21

5.4±

1.1(4.4

–6.5)

1.3±

0.03

(1.3

–1.4)

17/7/15

–7/24

/15

21/2/16

–1/20

/16

31/2/17

–1/18

/17

47/8/17

–7/23

/17

Macaron

i(Eudypteschrysolophus)

44

3.9±

0.2(3.6

–4.1)

13.1

±11

.2(0.9

–30

.4)

14/25

/201

5–5/10

/201

5;5/14

/15–5/29

/15

210

/27/15

–11

/13/15

;11/17

/15–12

/3/15

310

/27/16

–11

/11/16

;11/15

/16–11

/30/16

44/26

/17–5/10

/17;

5/12

/17–5/28

/17

Rockho

pper

(Eudypteschrysocome)

44

2.5±

0.4(1.8

–3.2)

16.3

±11

.8(4.7

–30

.4)

15/14

/15–5/29

/15;

6/8/15

–6/26

/15

211

/17/15

–12

/3/15;

12/4/15–12

/23/15

311

/15/16

–11

/30/16

;12/6/16

–12

/22/16

45/12

/17–5/28

/17;

6/8/17

–6/27

/17

Acute

Respon

seto

TDRs

King

11

18.0

(M)

17.2

(M)

11/20/18

(M)

10.6

(F)

26.0

(F)

11/26/18

(F)

Gentoo(P.p.papua)

11

6.1(M

)6.3(F)

10.9

(M)

6.0(F)

11/19/18

(M)

11/20/18

(F)

Macaron

i1

13.8(M

)3.7(F)

17.5

(M)

14.5

(F)

11/19/18

(M)

11/16/18

(F)

Rockho

pper

11

2.6(M

)2.2(F)

17.5

(M)

32.9

(F)

11/26/18

(M)

11/16/18

(F)

G. Fuller et al. Applied Animal Behaviour Science xxx (xxxx) xxx–xxx

2

examined the impacts—such as physical injury, behavioral changes, orcompromised energetics—of wearing devices on penguins in a fieldsetting (Vandenabeele et al., 2011). Ropert-Coudert et al. (2007b)equipped Adélie penguins (Pygoscelis adeliae) with either large or smalldevices and used the data to predict that penguins without devicesshould be able to swim deeper, further, and faster than conspecificswearing back-mounted data loggers. Their results suggest there areenergetic costs of wearing technology, which may be greater underconditions of food scarcity. Wilson et al. (2015) found that the impactsof devices on Magellanic penguins (Spheniscus magellanicus) dependedon their body condition, which depended on prey abundance. There-fore, penguins that are provisioned in zoos are presumably less likely tosuffer negative energetic effects from wearing devices (Hawkins, 2004).

Energetic costs of attached devices on wild penguins largely varybased on the size or placement of devices (Ropert-Coudert et al.,2007a), and behavioral and physiological impacts likely do as well. Forexample, southern rockhopper penguins (Eudyptes chrysocome) thatwore larger GPS devices had increased levels of circulating corticos-terone after dives compared to conspecifics wearing smaller loggers(Ludynia et al., 2012). Traditionally, researchers have followed the “5%rule,” recommending that devices not exceed this percent of bodyweight (Barron et al., 2010). However, device size can also be measuredby surface area, which seems to influence balance and dive parametersmore than overall mass (Wilson et al., 2004). Logger placement canminimize these influences, and the current standard practice in fieldstudies is to mount devices on the lower back using tape (Wilson et al.,1997).

Some zoos may have concerns about the effects of tape on feathercondition or the extensive handling required to attach devices in thismanner. As an alternative, Simeone et al. (2002) conducted a studywith a small number of zoo-housed Humboldt penguins (Spheniscushumboldti) evaluating ankle-mounted data loggers. One of the penguinsthey studied initially pecked at the device, but this behavior declinedover time (Simeone et al., 2002). However, demographic differencesbetween the experimental and control groups precluded any conclu-sions about the effects of data loggers on their activity budgets(Simeone et al., 2002).

We used a within-subjects study design to evaluate the effectivenessand welfare implications of time-depth recorders (TDRs) mounted onflipper bands for four species of penguins living at the Detroit Zoo inRoyal Oak, MI, USA. Previous field studies have used back-mounteddevices for some of the species we studied (king penguins, Schefferet al., 2016; macaroni and eastern rockhopper penguins, Whiteheadet al., 2016), but to our knowledge, this is the first study to evaluateTDRs on flipper bands for any penguin species in a zoo setting. TheTDRs use conductivity to assess wet/dry state and are generally used inseawater, but we predicted they would function effectively in a fresh-water pool. These penguins were already accustomed to wearing flipperbands for identification purposes, so we expected the devices to havenegligible impacts on their behavior. We predicted that the penguinsmight initially investigate or peck at the TDRs but would quickly be-come accustomed to them and would show few, if any, responses towearing TDRs in the long term. We examined social interactions as wellas self-directed and locomotor behaviors that could indicate discomfortor physical impacts of wearing TDRs. We predicted that any impacts ofwearing devices would be more evident in smaller species. Finally, weanticipated that the devices would provide valuable insight into the 24-hour lives of penguins in the zoo’s care.

2. Materials and methods

2.1. Subjects, housing, and study design

The data used for this analysis were collected as part of a studyevaluating changes in behavior and use of space in penguins aftermoving to a new habitat. The study penguins resided at the Detroit Zoo,

and the study was approved by the Detroit Zoological Society’s SeniorLeadership in Animal Welfare and Management Committee. At thebeginning of the study, the penguins lived in a mixed flock of ap-proximately 60 penguins representing four species: king (Aptenodytespatagonicus), gentoo (Pygoscelis papua ellsworthi), macaroni (Eudypteschrysolophus), and southern rockhopper (Eudyptes chrysocome) pen-guins. For the first year of the study, the penguins resided in thePenguinarium, a facility opened in 1968 that included a ring-shapedfreshwater pool 1.8m deep containing 132.5 kL of water, approxi-mately. For the remaining time, the penguins occupied the PolkPenguin Conservation Center (penguin center), which opened to thepublic in 2016. A group of 20 P.p. papua was added to the flock after themove to the penguin center, bringing the total colony up to approxi-mately 80 individuals. The penguin center features a 1234.0 kL fresh-water pool with a depth of 7.6m. The pool has an open design thatincludes an artificial kelp forest and simulated wave motion. A channelin the back of the habitat allows the penguins to swim continuouslywithout ever having to reverse direction, unless they choose to do so.

After informal pilot testing with a subset of individuals, 27 penguins(Table 1) wore time-depth recorders (TDRs) for about a two-weekperiod, four times: twice in the Penguinarium and twice in the penguincenter. We rotated seven TDR units among the 27 subjects. Sometimescaretakers could not remove devices from penguins who stayed in thepool, so those penguins wore the TDRs for extra days. The meanduration wearing TDRs per deployment was 15.8 ± 1.21 (SD) days,with a maximum of 20 days. In each habitat, one of the sessions oc-curred roughly during the breeding season, while the other occurredduring the non-breeding season (October - February). The penguinswere housed on an Arctic light cycle, so the breeding season for themacaroni and rockhopper penguins occurred roughly from March toJuly, while the breeding season for the king penguins occurred fromJune to August. The gentoo penguins were not yet mature and had notestablished a breeding season. The exact dates an individual penguinwore a TDR were matched between the two habitats, and penguins didnot wear TDRs during their annual molt. A geriatric female rockhopperpenguin died midway through the study, and data for this individualare only available from the two seasons in the Penguinarium. A kingpenguin who incubated an egg during the study period and a rock-hopper penguin that moved to another zoo each wore a TDR threetimes: twice in the Penguinarium and once in the penguin center.

We regularly collected observational data on these 27 penguins(Table 1) between January 2015 and July 2017 for a study examiningthe effects of moving to a new habitat on their behavior, use of space,and other indicators of welfare. We retrospectively used a subset ofthese behavioral data around times that the penguins wore TDRs toinvestigate the behavioral impacts of these devices using an ABA studydesign. We compared behavior for two weeks prior to wearing a TDR(A: before condition); for two weeks while wearing a TDR (B: TDRcondition); and for two weeks after wearing a TDR (A: after condition)using a within-subjects design.

2.2. Behavioral observations

Observational data were collected on focal penguins during eachphase of the ABA study using instantaneous scan sampling of activity atone-minute intervals and all-occurrences of brief event behaviors(Altmann, 1974). The ethogram of behaviors used in this study is listedin Table 2. Each observation was ten minutes in duration, and ob-servations were balanced across two-hour time periods between 8:00and 16:00 h. Our aim was to observe each of the 27 penguins once perday, Monday through Friday, although it was not always possible toobserve each penguin every day. During two-hour shifts, observers re-corded data on six to seven randomly selected focal penguins. Ob-servers recorded data on the penguins in the order they were listed toavoid any selection bias for observing birds more readily visible orengaged in more conspicuous behaviors. If the behavior of the penguin

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was not visible for more than five scans, the observer conducted asecond observation during the same two-hour time period. Observersrecorded data on paper check sheets or using the ZooMonitor program(Ross et al., 2016) on tablets (iPad Air (MD785LL/B) and iPad Air 2(MNV72LL/A), Apple Inc., Cupertino, CA, USA).

A total of 32 observers collected data for this study. Each observerpassed a three-part reliability test, which included an identification testfor all focal penguins, a multiple-choice test covering the ethogram, andthree observations scored in tandem with one of the principal in-vestigators. All observers maintained reliability above 90% based onthe mean percent difference calculated on tandem observations, andthis criterion was reassessed quarterly.

2.3. Acute responses to TDR application

To characterize the initial responses of penguins to wearing TDRs inmore detail, we conducted an additional 17 h of observations using thesame ethogram as for the long-term study. We used the same samplingmethod, except individual observations were one hour in duration ra-ther than ten minutes. From each species, the first two authors observedtwo individuals that had never before worn a TDR (Table 1), watchingeach naïve penguin continuously for two hours after caretakers appliedTDRs to their flipper bands. An additional third hour of observation wasconducted on the male rockhopper penguin.

2.4. Observational data summary and analysis

To assess acute responses to wearing TDRs, we analyzed rates ofdevice-directed behavior exhibited by the penguin wearing the TDR ordirected at the TDR from a conspecific. We report these results de-scriptively.

We used a total of 399.5 h of observational data to analyze long-term impacts of wearing TDRs: 113.3 h for king, 48.2 h for gentoo,127.3 h for macaroni, and 110.7 h for rockhopper penguins. Time ob-served per individual per TDR condition (before, during, or afterwearing the TDR) ranged from 2.5 to 7.0 h, with an average of4.9 ± 0.9 (SD) h of observation per individual for a given condition.We combined sessions in which behavior was not visible on more thanfive scans with follow-up sessions within the same two-hour timeperiod. Additionally, on the rare occasion that a penguin was observedfor two complete observations during the same period on the same day,we combined those sessions as well. Thus, the total number of visiblescans in an observation ranged from 5 to 20. To account for this, weused the total number of visible scans to calculate the percent of timeperforming scan behaviors and to estimate the duration of observationsfor calculating rates of all-occurrence behaviors. We focused on

analyzing behaviors that logically might be affected by wearing TDRs.We present full activity budgets in Fig. 2a–d; however, we did notstatistically analyze feeding, because the penguins were mostly hand-fed. In addition, we analyzed allopreening and agonistic behaviors,which often occurred as short events, using all-occurrence data ratherthan scans.

We completed statistical analyses for each species separately usingSPSS v. 25 (IBM Corporation, Armonk, NY, USA). We elected to analyzeeach species separately, because we wanted to focus on welfare impactsat the individual and species level, rather than emphasizing cross-spe-cies comparisons. We compared counts of target behaviors using gen-eralized linear mixed models (GLMMs) with Poisson distributions andlog link functions. We offset models by ln(total number of visible scans)to account for differences in observation length and penguin visibility.We performed model-building using a top-down approach, removingnon-significant fixed factors from the following options: TDR condition(before, TDR, and after), age, sex, and body weight. When age, sex, orweight was a significant predictor, we tested for interactions betweenthese predictors and TDR condition. We always retained TDR condition(along with other significant predictors) in final models whether or notit was significant, because of its importance to the study question. Wewere unable to test for the effects of sex, age, and weight on the gentoopenguins due to the small sample size.

Preliminary analyses indicated that the behavior of the penguinsdiffered significantly based on season and habitat. These seasonal dif-ferences meant we were unable to test for the effects of TDR experience(i.e., the number of times the penguin wore the TDR), because testsoccurred in alternating seasons. Because differences in behavior basedon season and habitat were not central to our analysis but greatly im-pacted behavior, we created all the GLMMs using a random interceptand a random slope for Individual ID*TDR condition*Season*Habitat.Due to the smaller number of individuals, we were unable to fit modelsusing the full random slope for gentoo self-directed, inactive, andagonistic behavior. We ran these models using a simpler random slopefor Individual ID*TDR condition. We also followed this approach forrockhopper penguin agonistic behavior, because a model would notconverge for the more complicated random structure. For king pen-guins, we were only able to fit a model for moving using a random slopefor Individual ID*TDR condition*Season. We used a variance compo-nents variance-covariance structure and calculated degrees of freedomusing a Satterthwaite approximation. We made pairwise comparisonsbetween conditions based on estimated marginal means and adjustedfor multiple comparisons using the least significant difference. Forsignificant continuous predictors, we report fixed parameter estimatesrather than marginal means. For all statistical tests, we report sig-nificant effects when p < 0.05 and trends when 0.05 ≤ p < 0.1.

Table 2Penguin ethogram for time-depth recorder (TDR) study. All behaviors were scored using scan sampling, and all-occurrences of behaviors marked * were alsorecorded.

Behavior Operational Definition

Agonistic Behavior* Giving or receiving contact aggression (pecking, wing blows, or gripping and twisting with bill) or noncontact aggression (lunging at another penguin orattempting to peck one without making contact; or pointing the head toward and aggressively vocalizing at another penguin)

Allopreen* Rubbing the head, bill, or flipper on another individual; or “mouthing” another individual; or receiving allopreening from another penguinBathing* Preening or adjustment movements in the water, including tail wags and shaking movementsDevice-Directed* Pecking at, scratching, or manipulating a TDR; making contact with the TDR while preening or scratching in its vicinity; or receiving device-directed

behavior from another penguinFeed Ingesting food, including being fed by keeper, or drinking waterInactive Resting in any position (usually standing or lying); may be moving the head or eyes to observe the surroundings or head may be tucked under the wing

while the penguin is sleepingMove (terrestrial) Moving at any pace by walking or hoppingNot visible Behavior cannot be definitively determinedOther Any other behavior not detailed elsewhere involving vigorous movementSelf-Directed Preening (includes contact between the bill and feathers, rubbing the head over another body part, wing rub on head or neck, scratching with feet) or

adjusting (shaking and stretching movements, including head shake, body shake, tail wag, or rapid wing flap)Swim Moving through the water at any depth using the flippers and feet for propulsion; floating; or porpoising

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2.5. Time-depth recorders

The TDR used in this study was the LAT1800 L (Lotek Wireless, Inc.,Newmarket, ON, Canada). The TDRs were affixed to cradles custom-designed by the manufacturer using epoxy and secured to the penguins’flippers using cable-ties, which the penguins were accustomed towearing for identification purposes (Fig. 1). The LAT1800 L TDR isapproximately cylindrical in shape and measures 36 x 13 x 10mm. Theweight of the TDR in air with the cradle is 14.1 g, which ranges from0.08% to 0.78% of the body weight of the penguins in this study(Table 1). We programmed the TDRs to record pressure and wet/drystate every six seconds for 24 h per day. Each two-week deploymentresulted in 201,600 total data points.

2.5.1. TDR validation testsWe downloaded data from the TDRs using Tag Talk (Lotek Wireless,

Inc., Newmarket, ON, Canada) and exported it into Excel (v. 2016,Microsoft Corporation, Redmond, WA, USA). We explored corre-spondences between observational and TDR data by taking a randomsample of 100 data points when observers recorded that the penguinswere swimming and comparing these to the continuous TDR data bymatching the time stamps from ZooMonitor and TDR data. When thewet/dry state indicated that the unit was wet, we considered this a datamatch; we considered a dry state to be a mismatch. We then comparedpressure readings separately for matches and mismatches for each ha-bitat. We confirmed that the wet/dry (conductivity) sensor registeredwetness in the freshwater pool by experimentally immersing the dataloggers and timing how long it took them to register as dry after beingremoved from the pool. Finally, the penguin center habitat containedpiles of fresh snow, a substrate not present in the Penguinarium. Forthis reason, we also tested whether burying the TDRs in snow registeredas wet on the conductivity sensor. Although it is unlikely that the dataloggers would come into prolonged contact with the snow due to theirattachment location on the penguins, we wanted to ensure this wouldnot result in false readings. We conducted these tests on six of the seven

TDR units employed in these studies, due to the failure of one unit thatwe did not use in further studies. We made comparisons to the nearestminute in each location due to the difficulty of matching the internaltimer on the TDR to the exact second we manipulated the TDRs.

3. Results

3.1. TDR validation tests

When the TDRs were experimentally placed in the pool, each of thesix units registered as wet within the minute they were submerged anddry within the minute they were removed from the pool. When theTDRs were buried in snow for four minutes, the wet/dry sensors re-corded that the devices were dry.

Out of 100 randomly selected data points when observers recordedthe penguins swimming, the wet/dry sensor recorded the TDR as wet 95times and dry 5 times for a 95% match. The percent of mismatches(when observers recorded the penguins as swimming but the wet/drysensor was dry) in the Penguinarium was 3.57% (1 of 28 swims)compared to 12.50% in the penguin center (9 of 72 swims). The TDRsrecorded negative readings for pressure when the penguins were onland or at the water surface. For mismatched data, pressure readingswere always negative, ranging from -0.8 to -0.48 dBar. For matchingdata (when the observers recorded the penguin as swimming and thewet/dry sensor was wet), the data were more variable. Pressure read-ings when observers recorded penguins swimming averaged-0.11 ± 0.43 (SD) dBar (range -0.87 - 0.47 dBar) in the Penguinariumand averaged 1.40 ± 1.63 dBar (range -0.85 – 4.83 dBar) in the deeperpool in the penguin center.

3.2. Acute responses to the application of TDRs

Overall, penguins wearing TDRs for the first time performed device-directed behavior at relatively low rates, with a group mean of1.35 ± 0.65 (SE) bouts per hour for their first two hours wearing theTDRs. Both the male gentoo and the female king penguin displayed nodevice-directed behavior at all. The female gentoo, male king, and bothmacaroni penguins performed only one to two device-directed beha-viors each during the entire two-hour period. Their behavior consistedof briefly preening around the TDR or rubbing their head on the area,and, in most cases, contact with the TDR appeared to be incidentalrather than directed towards the device. There was only one instancewhen a conspecific directed behavior towards a focal subject’s TDR,when a macaroni penguin briefly mouthed the female macaroni’s TDR.

The rockhopper penguins displayed the highest rates of device-di-rected behavior. The female rockhopper penguin performed a mean of2.02 ± 2.83 (SD) bouts of device-directed behavior per hour. All ofthese events occurred during her second hour wearing the TDR andmostly consisted of incidental contact with the TDR while preeningnear it. The male rockhopper penguin performed a mean of5.59 ± 0.71 device-directed bouts per hour for the two-hour period,and he was the only individual that was observed nibbling and peckingdirectly at the TDR unit. He was observed for a third consecutive hourand did not display any device-directed behavior during that time.

3.3. Long-term behavioral differences across TDR conditions

We present statistically significant results for TDR condition as afixed factor and do not report statistics for non-significant findings.Penguin age, sex, and weight were sometimes significant as fixed fac-tors in models but not as two-way interactions with TDR condition,with the exception of weight and movement in king penguins. Weconsidered only these interactions pertinent to our research questions,so we do not discuss the role of these other predictors further. Duringthe long-term study, we only observed device-directed behavior a singletime, when a female macaroni penguin briefly scratched and preened

Fig. 1. The time-depth recorders (TDRs) were affixed to custom-designed cra-dles (right middle and lower images). A cable-tie was threaded through thecradle and used to attach the TDR to the top of the penguin’s flipper. Imagesshow rockhopper (top left), king (top middle), macaroni (top right), and gentoo(bottom left) penguins wearing the TDRs. Note the cable-ties with beads usedfor identification purposes on the flippers. The cradle illustration is courtesy ofLotek Wireless, Inc. (Newmarket, ON, Canada).

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around the device. This event occurred during the first period she worethe TDR, but it was several days after the TDR was applied. We did notstatistically analyze device-directed behavior, because we never ob-served it again.

3.3.1. King penguinsThe king penguins showed no significant differences in the amount

of time they spent swimming, inactive, or displaying self-directed be-haviors based on TDR condition (Fig. 2a). The amount of time movingdid vary significantly with TDR condition (F2,58 = 4.34, p = 0.02;Fig. 2a), but the pairwise comparisons between wearing a TDR andbefore (t32 = -0.47, p=0.64) and after (t29 = -1.355, p=0.19) werenot statistically significant. Penguin body weight significantly affectedmovement as a two-way interaction with TDR condition (F2,61= 4.66,p=0.01). Fixed parameter estimates indicated a trend that heavierpenguins moved more after wearing TDRs compared to while wearingthem (b=0.13, p=0.09).

Rates of king penguin agonistic behavior varied significantly basedon TDR condition (F2,73 = 3.81, p = 0.03; Fig. 3a). The king penguinsperformed more agonistic behaviors while wearing TDRs compared tobefore wearing them (t24= 2.14, p= 0.04). Rates of agonistic behaviorincreased from 4.81 ± 1.43 (SE) bouts per hour before wearing TDRsto 7.66 ± 1.59 while wearing TDRs. The difference between afterwearing TDRs compared to while wearing them was not statisticallysignificant (t74 = -0.96, p=0.34). The difference between the beforeand after conditions also was not statistically significant (t62 = -1.55,p=0.13). King penguins showed no differences in rates of allopreening

based on TDR condition, and bathing occurred at rates too low toanalyze statistically.

3.3.2. Gentoo penguinsThe gentoo penguins demonstrated no statistically significant be-

havioral differences based on TDR condition (Fig. 2b). Overall, gentoopenguins spent the most time swimming compared to the other species.

3.3.3. Macaroni penguinsThe macaroni penguins spent the least time swimming of all the

study species, but TDRs did not impact the percent of time they spentswimming or performing any other scan behaviors (Fig. 2c). There wasa trend for rates of agonistic behavior to change with TDR condition(F2,84 = 2.44, p = 0.09; Fig. 3b). Macaroni penguins exhibited a trendto display more agonistic behaviors after wearing TDRs compared towhile wearing them (t80= 1.99, p= 0.05). The difference betweenbefore and during wearing TDRs was not statistically significant(t91= 0.69, p= 0.49), nor was the difference between before and after(t83 = -1.41, p=0.16). Bathing occurred at levels too low to analyzestatistically. Wearing TDRs did not affect rates of allopreening.

3.3.4. Southern rockhopper penguinsRockhopper penguins showed no differences in the amount of time

they spent inactive, performing self-directed behavior, or swimmingbased on TDR condition. However, there was a trend for the amount oftime they spent moving on land to vary based on TDR condition (F2,71= 2.57, p = 0.08; Fig. 2d). There were trends for the rockhopper

Fig. 2. a–d. Activity budgets for four penguin species for two-week periods before, during, and after wearing time-depth recorders (TDRs). Results show the percentof time (mean ± SE) displaying state behaviors for (a) king, (b) gentoo, (c) macaroni, and (d) southern rockhopper penguins. Standard error bars are based on thenumber of penguins in each species (n=8 for all species except gentoo penguins, n= 3). Note that inactive (and for gentoos, swim) behaviors are set to the side toadjust the scale on the main activity budget. No behaviors were statistically significant, but statistical trends (0.05 ≤ p < 0.1) are indicated by ^. Although TDRcondition was significant as a fixed factor for king penguin movement, pairwise comparisons between TDR conditions were not statistically significant.

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penguins to spend less time moving after wearing TDRs compared bothto before (t75 = -1.94, p=0.06) and while (t75 = -1.97, p=0.05)wearing the devices. The difference between the periods before andwhile wearing the TDRs was not statistically significant (t61 = -0.04,p=0.97). The rockhopper penguins also showed no significant changesin rates of allopreening, agonistic behavior, or bathing based on TDRcondition.

4. Discussion

The TDRs functioned well in a freshwater environment and gener-ated valuable, around-the-clock data on pool use, with minor limita-tions. Rates of device-directed behavior displayed by penguins wearingthe TDRs for the very first time were low, and we observed almost nodevice-directed behavior during long-term use. Behavioral changesbefore, during, and after wearing TDRs largely did not show patternsconsistent with attributing causality in an ABA study design (Saudargasand Drummer, 1996). Consistent with our hypothesis, the smallestspecies (southern rockhopper penguins) showed the strongest reactionto the initial application of the devices. In contrast, the most significantbehavioral changes during long-term use were observed in the largestspecies, the king penguin.

4.1. Validation of TDR data

Direct comparisons of observational to TDR data showed that thetwo methods were in agreement 95% of the time about whether apenguin was in the water. Experimental tests with the TDRs showedthat these errors were not due to delays in the units drying after re-moval from the pool or false positives recorded when penguins were insnow. Instead, the discordant data could have resulted from observererror. The size and complexity of the penguin center made it morechallenging for observers to follow focal penguins compared to thePenguinarium. The greater percentage of data mismatches in the pen-guin center is consistent with this interpretation. Other possibilitiesinclude the sensor not being wet enough while the penguin wasswimming at the pool surface or temporary malfunctioning of the wet/dry sensor, which has been reported in other bio-logging studies(Ropert-Coudert and Wilson, 2004).

Despite this potential limitation, we did find that using the con-ductivity (wet/dry) sensor was more effective for estimating pool usethan the pressure sensor. The pressure sensor recorded a slightly ne-gative value while the penguins were on land and when we experi-mentally placed the TDRs at the pool surface. Although this may be of

little concern in field studies, pressure readings are likely to under-estimate significantly the time spent in the water in zoo settings, wherewater space is shallower and overall more limited. However, the pres-sure sensor also provides information about the depths used in the pool,which can be calculated as 1.0 dBar equal to 1.02m (Fowler, 2013).

4.2. Acute responses to application of TDRs

We predicted that the penguins would initially show behaviors di-rected towards the TDRs such as pecking devices or preening near them,and that these behaviors would decline over time. When TDRs wereapplied to the flipper bands of naïve penguins, they directed relativelylow rates of behavior towards the devices. Additionally, the rockhopperpenguin who performed the highest rates of device-directed behavior(pecking) in these trials completely stopped that behavior in his thirdhour wearing the TDR. These results are consistent with those ofSimeone et al. (2002), who saw low rates of pecking at ankle-mounteddata loggers after they were applied, with no device-directed behaviorsafter the first day wearing the loggers. Attention paid to devices candepend on their color, as in Adélie penguins (Ropert-Coudert andWilson, 2004), or may vary by species; for example, Magellanic pen-guins will bite feathers to remove back-mounted devices (Wilson et al.,1997). Consistent with species differences, the two individuals thatattended most to the devices in this study were both southern rock-hopper penguins, a result that could be related to the fact that theywere the smallest species tested. However, no device-directed behaviorby rockhopper penguins was observed during long-term data collection,suggesting they habituated to wearing the TDRs.

Handling birds to apply devices may have substantial impacts ontheir behavior or health independent of the effects of the technologyitself. However, the penguins in this study were accustomed to regularhandling for health assessments and applying flipper bands. There ismixed evidence for a habituation response to handling in birds. Littlepenguins (Eudyptula minor) repeatedly captured for field research ac-tually showed higher concentrations of corticosterone and more ag-gressive behavior following handling compared to naïve birds (Carrollet al., 2016), suggesting they actually became sensitized to the proce-dure. However, in zoo-housed red-tailed hawks (Buteo jamaicensis),fecal corticosterone concentrations were correlated negatively withboth the duration of handling and exposure to human handling early inlife (Baird et al., 2016). The habituation process may differ for captiveanimals, who are exposed to humans every day, compared to in-dividuals in the wild. In this study, caretakers were able to apply theTDRs to the birds very quickly, usually in less than 30 s. In contrast,

Fig. 3. a–b. Rates (mean ± SE) of agonistic behavior by two penguin species for two-week periods before, during, and after wearing time-depth recorders (TDR).Results show the combined rate per hour of giving and receiving agonistic behavior for king (a) and macaroni (b) penguins. Rates are shown separately for eachhabitat and season (breeding or non-breeding season), but statistical comparisons were made by condition for habitats and seasons combined. Standard errors arebased on n= 8 penguins for each species. Statistical significance (p < 0.05) between pairs of conditions is indicated by * and trends (0.05 ≤ p < 0.1) as ^.

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Ludynia et al. (2012) reported that mounting data loggers on the backsof rockhopper penguins using tape took 10–20 minutes—although thisalso included time required to draw blood and insert passive integratedtransponder (PIT) tags. The process applied in this study was arguablyless invasive and faster and, coupled with their handling experience,likely explains why the penguins showed few behavioral responses towearing the TDRs, even at first.

4.3. Long-term behavioral impacts of TDRs

Using TDRs in a zoo setting requires less consideration of energeticimpacts compared to the wild, given that animals are provisioned andmonitored carefully by caretakers (Hawkins, 2004). For this reason, andbecause the penguins in this study were accustomed to flipper bands,we expected the long-term behavioral effects of wearing the TDRswould be minimal. The data generally supported our predictions.Wearing TDRs did not affect overall activity levels; there were no dif-ferences in time spent inactive based on TDR condition for any of thefour study species. Significant changes in other behaviors occurred insome cases, but generally, it seemed unlikely that the TDRs causedthese changes.

4.3.1. TDR impacts on locomotor behaviorsSimeone et al. (2002) noted that the ankle-mounted data loggers

used in their study sometimes made contact with the substrate whilethe penguins walked, causing some changes in locomotor behavior. Weplaced the devices on flipper bands, so we expected any impact on lo-comotor behavior to affect aquatic rather than terrestrial locomotion.Instead, none of the four study species showed changes in their percentof time swimming based on TDR condition, while two study speciesdisplayed differences in movement on land. In the case of rockhopperpenguins, this difference was a statistical trend showing a linear de-crease in the amount of time spent moving across the three studyconditions, rather than a causal impact of the TDRs.

The king penguins did show a U-shaped pattern in movement be-havior, with less movement on land while wearing TDRs compared toboth before and after. Although the overall effect of condition onmovement was statistically significant, pairwise comparisons betweenTDR conditions were not. The difference between during and afterwearing TDRs was only about three percent of the time, so the changein movement may not be of great biological significance either. It seemslikely that two confounding factors may be driving these trends. Theking penguins spent much more time moving in the Penguinariumcompared to the penguin center, and we were not able to fit a model tocontrol for habitat in this analysis. Additionally, there was a significantinteraction between penguin weight and the percent of time spentmoving. Increased body mass predicated more time spent moving afterwearing a TDR compared to while wearing one. Yet, if wearing theTDRs caused a reluctance to move on land, it seems logical to expectthat this would disproportionately affect smaller penguins, for whomthe TDRs were a larger percentage of their body weight. However, weobserved the opposite trend. In general, other studies have not foundthat body weight significantly affects the response to devices (Barronet al., 2010), and our data do not indicate a clear relationship in thiscase. Some of these inconsistencies may be due to limitations in con-trolling for season and habitat statistically resulting from the retro-spective nature of our study design.

4.3.2. TDR impacts on comfort behaviorsComparing activity budgets, there were few differences related to

TDRs in self-directed behavior, which included preening and adjust-ment movements, such as wing flapping. There were no differences inthe percent of time performing these behaviors between TDR conditionsfor any species. There also were no significant changes in bathing be-havior (adjusting or preening in the water) based on TDR condition forthe only species that regularly performed this behavior, the rockhopper

penguin. Additionally, we saw only one instance of device-directedbehavior by penguins during the long-term study. Thus, the penguinsshowed almost no signs of physical discomfort associated with wearingthe TDRs on flipper bands.

4.3.3. TDR impacts on social behaviorsThere were no effects of wearing TDRs on allopreening, the most

common affiliative behavior, in king, macaroni, or rockhopper pen-guins. The gentoo penguins rarely exhibited this behavior, so we wereunable to assess whether TDRs affected affiliative behavior in thisspecies. The data did show relationships between TDR condition andagonistic behavior for two species.

Macaroni penguins engaged in more agonistic behavior afterwearing TDRs compared to while wearing them. It seems unlikely thatthe TDRs caused this trend; instead, it may represent behavioralchanges associated with the breeding season, like the pattern seen forterrestrial movement in the rockhopper penguins. As nest-building be-gins in preparation for breeding, macaroni penguins exhibit a surge intestosterone accompanied by high levels of agonistic behavior relatedto intraspecific competition and nest defense (Williams, 1992). Con-sistent with this interpretation, rates of agonistic behavior were higherfor the macaroni penguins during both breeding seasons compared tothe non-breeding seasons. Rather than peaking at the beginning of thebreeding season, agonistic behavior increased precipitously from Mayto June in both years. Thus, agonistic behavior was at its highest at theend of the breeding season, which coincided with the phase afterwearing TDRs. In contrast, levels of agonistic behavior remained steadythroughout testing during both non-breeding seasons. The evidence issomewhat inconsistent, but there is little reason to suppose that re-moving the TDRs caused the increase in aggressive behavior towardsthe end of the breeding season.

King penguins displayed more agonistic behavior while wearingTDRs compared to before wearing them. Yet, it is unclear how agonisticbehavior was related to the TDRs, because we never observed anypecking or other behavior directed towards devices on conspecifics. Inwild king penguins, territory location (center versus periphery ofcolony) and breeding stage are the major determinants of intraspecificaggression, which increases from incubation to the brooding period(CôTé, 2000). Some of the king penguins in this study produced eggs,but there were no chicks reared during either breeding season. Analysisof individual agonistic behavior showed that the trend we observed waslargely due to increased agonism by two individuals while wearingTDRs during the breeding season in the penguin center. One of theseindividuals was thought to have fertilized a viable egg during this time,and perhaps the increased agonistic behavior was related to matingcompetition. The force behind this trend remains unclear, but rates ofagonistic behavior were generally low in this study and were wellbelow the 13% of the daily activity budget devoted to agonistic beha-viors in defense of territory reported by Viera et al. (2011). We suspectthat this difference was, in fact, due to our inability to completelycontrol for seasonality with our retrospective study design. However,for the sake of caution, future studies should still carefully monitor ratesof agonistic behavior to ensure there are no negative welfare effects.

5. Conclusions

Overall, we found that the TDRs functioned well for recordingaround-the-clock data on the aquatic behaviors of all four penguinspecies in their freshwater habitats at the Detroit Zoo. We observed veryfew changes in behavior that could be linked to the TDRs, even im-mediately following application of the devices. However, we do notmean to suggest that this approach would have the same results inevery setting. In wild animals, potential negative effects of devices aregenerally assessed in relation to energy expenditure, foraging success(e.g., foraging duration or mass of prey consumed), reproductive suc-cess (e.g., clutch size or offspring growth rates), or survival (Barron

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et al., 2010; Hawkins, 2004). We did not test the impact of wearingflipper-mounted TDRs on these measures. Furthermore, even withoutattached devices, flipper bands increase swimming costs and decreasesurvival in wild penguins (Jackson and Wilson, 2002).

Flipper-mounted TDRs are a useful tool for continuously trackingpenguin aquatic behavior as part of an animal welfare monitoringprogram, and we have already applied these methods in several con-texts. We used TDRs to monitor a gentoo penguin recovering from aninfection, as well as to assess circadian entrainment to a new light cyclein recently transferred macaroni penguins. Furthermore, technologicaladvancements continue to improve automated monitoring technolo-gies. There are TDRs equipped with accelerometers that can measureactivity on land as well as in the water (e.g., Yoda et al., 2001), and thecomputational ability to recognize specific behaviors using accel-erometer data is improving (Sakamoto et al., 2009). These technologiescould also be deployed in future studies using our methods for a morecomprehensive means of monitoring penguin welfare in zoos andaquariums.

Acknowledgments

We would like to thank the Detroit Zoological Society bird staff forassisting us with this study and for sharing their expertise. We alsothank the many dedicated volunteers who collected and entered data.

References

Altmann, J., 1974. Observational study of behavior: sampling methods. Behaviour 48,227–265.

Baird, B.A., Kuhar, C.W., Lukas, K.E., Amendolagine, L.A., Fuller, G.A., Nemet, J., Willis,M.A., Schook, M.W., 2016. Program animal welfare: using behavioral and physio-logical measures to assess the well-being of animals used for education programs inzoos. Appl. Anim. Behav. Sci. 176, 150–162.

Barron, D.G., Brawn, J.D., Weatherhead, P.J., 2010. Meta-analysis of transmitter effectson avian behaviour and ecology. Methods Ecol. Evol. 1, 180–187.

Blay, N., Cote, I.M., 2001. Optimal conditions for breeding of captive Humboldt penguins(Spheniscus humboldti): a survey of British zoos. Zoo Biol. 20, 545–555.

Carroll, G., Turner, E., Dann, P., Harcourt, R., 2016. Prior exposure to capture heightensthe corticosterone and behavioural responses of little penguins (Eudyptula minor) toacute stress. Conserv. Physiol. 4.

Clarke, A.G., 2003. Factors affecting pool use by captive Humboldt penguins (Spheniscushumboldti). Gilbert, T.C. (Ed.), The Fifth Annual Symposium on Zoo Research,Federation of Zoological Gardens of Great Britain and Ireland, Marwell ZoologicalPark 190–204.

CôTé, S.D., 2000. Aggressiveness in king penguins in relation to reproductive status andterritory location. Anim. Behav. 59, 813–821.

Erlacher-Reid, C., Dunn, J.L., Camp, T., Macha, L., Mazzaro, L., Tuttle, A.D., 2012.Evaluation of potential variables contributing to the development and duration ofplantar lesions in a population of aquarium-maintained African penguins (Spheniscus

demersus). Zoo Biol. 31, 291–305.Fowler, G., 2013. Tag Talk for Lotek Archival Tags (LAT Series) User Manual (Revision

Eight). Lotek Wireless, Inc., Newmarket, ON, Canada.Green, J.A., Boyd, I.L., Woakes, A.J., Warren, N.L., Butler, P.J., 2005. Behavioural flex-

ibility during year-round foraging in macaroni penguins. Mar. Ecol. Prog. Ser. 296,183–196.

Hawkins, P., 2004. Bio-logging and animal welfare: practical refinements. Mem. Natl.Inst. Polar Res., Spec. Issue 58, 58–68.

Jackson, S., Wilson, R.P., 2002. The potential costs of flipper-bands to penguins. Funct.Ecol. 16, 141–148.

Ludynia, K., Dehnhard, N., Poisbleau, M., Demongin, L., Masello, J.F., Quillfeldt, P., 2012.Evaluating the impact of handling and logger attachment on foraging parameters andphysiology in southern rockhopper penguins. PLoS One 7, e50429.

Mori, Y., 1999. A note on swimming group size in captive African penguins (Spheniscusdemersus) in relation to weather conditions. Appl. Anim. Behav. Sci. 62, 359–364.

Ropert-Coudert, Y., Wilson, R.P., 2004. Subjectivity in bio-logging: do logged data mis-lead? Mem. Natl. Inst. Polar Res., Spec. Issue 58, 23–33.

Ropert-Coudert, Y., Knott, N., Chiaradia, A., Kato, A., 2007a. How do different data loggersizes and attachment positions affect the diving behaviour of little penguins? DeepSea Res. Part II-Top. Stud. Oceanogr. 54, 415–423.

Ropert-Coudert, Y., Wilson, R.P., Yoda, K., Kato, A., 2007b. Assessing performance con-straints in penguins with externally-attached devices. Mar. Ecol. Prog. Ser. 333,281–289.

Ross, M.R., Niemann, T., Wark, J.D., Heintz, M.R., Horrigan, A., Cronin, K.A., Gillespie,K., 2016. ZooMonitor [Mobile Application Software]. https://zoomonitor.org.

Sakamoto, K.Q., Sato, K., Ishizuka, M., Watanuki, Y., Takahashi, A., Daunt, F., Wanless,S., 2009. Can ethograms be automatically generated using body acceleration datafrom free-ranging birds? PLoS One 4, e5379.

Saudargas, R.A., Drummer, L.C., 1996. Single subject (small N) research designs and zooresearch. Zoo Biol. 15, 173–181.

Scheffer, A., Trathan, P.N., Edmonston, J.G., Bost, C.-A., 2016. Combined influence ofmeso-scale circulation and bathymetry on the foraging behaviour of a diving pre-dator, the king penguin (Aptenodytes patagonicus). Prog. Oceanogr. 141, 1–16.

Simeone, A., Wilson, R.P., Knauf, G., Knauf, W., Schützendübe, J., 2002. Effects of at-tached data-loggers on the activity budgets of captive Humboldt penguins. Zoo Biol.21, 365–373.

Vandenabeele, S.P., Wilson, R.P., Grogan, A., 2011. Tags on seabirds: How seriously areinstrument-induced behaviours considered? Anim. Welf. 20, 559–571.

Viera, V.M., Viblanc, V.A., Filippi-Codaccioni, O., Côté, S.D., Groscolas, R., 2011. Activeterritory defence at a low energy cost in a colonial seabird. Anim. Behav. 82, 69–76.

Whitehead, T., Kato, A., Ropert-Coudert, Y., Ryan, P.G., 2016. Habitat use and divingbehaviour of macaroni Eudyptes chrysolophus and eastern rockhopper E. chrysocomefilholi penguins during the critical pre-moult period. Mar. Biol. 163, 19.

Williams, T.D., 1992. Reproductive endocrinology of macaroni (Eudyptes chrysolophus)and gentoo (Pygoscelis papua) penguins: I. Seasonal changes in plasma levels of go-nadal steroids and LH in breeding adults. Gen. Comp. Endocrinol. 85, 230–240.

Wilson, R.P., Putz, K., Peters, G., Culik, B., Scolaro, J.A., Charrassin, J.-B., Ropert-Coudert, Y., 1997. Long-term attachment of transmitting and recording devices topenguins and other seabirds. Wildl. Soc. Bull. 25, 101–106.

Wilson, R.P., Kreye, J.M., Lucke, K., Urquhart, H., 2004. Antennae on transmitters onpenguins: balancing energy budgets on the high wire. J. Exp. Biol. 207, 2649–2662.

Wilson, R.P., Sala, J.E., Gómez-Laich, A., Ciancio, J., Quintana, F., 2015. Pushed to thelimit: food abundance determines tag-induced harm in penguins. Anim. Welf. 24,37–44.

Yoda, K., Naito, Y., Sato, K., Takahashi, A., Nishikawa, J., Ropert-Coudert, Y., Kurita, M.,Le Maho, Y., 2001. A new technique for monitoring the behaviour of free-rangingAdelie penguins. J. Exp. Biol. 204, 685–690.

G. Fuller et al. Applied Animal Behaviour Science xxx (xxxx) xxx–xxx

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