MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 496: 85–98, 2014doi: 10.3354/meps10592

Published January 27

INTRODUCTION

Regulation of heart rate (ƒH) underlies the oxygenstore management and dive capacity of seabirds andmarine mammals. The reduction in cardiac outputassociated with a decline in ƒH during forced submer-sion results in: (1) decreased organ blood flow andperfusion-dependent O2 consumption, (2) decreasedblood flow to locomotory muscle and a decline inblood-to-muscle O2 transfer, and (3) decreased pul-monary blood flow and blood oxygen uptake fromthe lung (Scholander 1940, Irving et al. 1941, Ponga-nis et al. 2011). The decrease in peripheral blood flowassociated with a diving bradycardia conserves theblood O2 store and maximizes breath-hold capacity

(Scholander 1940, Irving et al. 1941). A decrease inpulmonary flow similarly conserves the respiratoryO2 store and additionally preserves the respiratoryO2 fraction, which, in turn, optimizes oxygenation ofany blood passing through the lung, thus maintain-ing arterial oxygen saturation longer and maximizingbreath-hold capacity (Andersson et al. 2002).

Although severe bradycardia occurs in forced sub-mersions (the classic dive response), the diving ƒH

response in free-ranging animals is often less intenseand more variable. For example, ƒH decreases frompre-dive levels during dives of king penguins Apteno -dytes patagonicus and macaroni penguins Eudypteschrysolophus at sea, but it does not decline belowresting levels on land, nor does it approach levels

© Inter-Research 2014 · www.int-res.com*Corresponding author: awright@ucsd.edu

Heart rates of emperor penguins diving at sea:implications for oxygen store management

Alexandra K. Wright*, Katherine V. Ponganis, Birgitte I. McDonald, Paul J. Ponganis

Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093-0204, USA

ABSTRACT: Heart rate (ƒH) contributes to control of blood oxygen (O2) depletion through regula-tion of the magnitude of pulmonary gas exchange and of peripheral blood flow in diving verte-brates such as penguins. Therefore, we measured ƒH during foraging trip dives of emperor pen-guins Aptenodytes forsteri equipped with digital electrocardiogram (ECG) recorders and timedepth recorders (TDRs). Median dive ƒH (total heartbeats/duration, 64 beats min−1) was higherthan resting ƒH (56 beats min−1) and was negatively related to dive duration. Median dive ƒH indives greater than the 5.6 min aerobic dive limit (ADL; dive duration associated with the onset ofa net accumulation of lactic acid above resting levels) was significantly less than the median diveƒH of dives less than the ADL (58 vs. 66 beats min−1). ƒH profile patterns differed between shallow(<50 m) and deep dives (>250 m), with values usually declining to levels near resting ƒH in shal-low, short-duration dives, and to levels as low as 10 beats min−1 during the deepest segments ofdeep dives. The total number of heartbeats in a dive was variable in shallow dives and consistentlyhigh in deep dives. A true bradycardia (ƒH below resting levels) during segments of 31% of shal-low and deep dives of emperor penguins is consistent with reliance on myoglobin-bound O2 storesfor aerobic muscle metabolism that is especially accentuated during the severe bradycardiasof deep dives. Although ƒH is low during the deepest segments of deep dives, the total numberand distribution of heartbeats in deep, long dives suggest that pulmonary gas exchange andperipheral blood flow primarily occur at shallow depths.

KEY WORDS: Aerobic dive limit · Diving physiology · Electrocardiogram · ECG · Emperor penguin · Gas exchange · Heart rate · Oxygen store management · Peripheral perfusion

Resale or republication not permitted without written consent of the publisher

Contribution to the Theme Section ‘Tracking fitness in marine vertebrates’

Mar Ecol Prog Ser 496: 85–98, 2014

observed in simulated dives (Kooyman et al. 1973,Ponganis et al. 1997, 1999a, Green et al. 2003, Frogetet al. 2004). In terms of muscle blood flow and oxygendelivery, this ƒH pattern during the penguin’s divehas been considered a trade-off between the classicdive response of forced submersions and the exerciseresponse of flighted birds and terrestrial mammals(Butler 1988, Green et al. 2003). Higher ƒH in divingking and macaroni penguins than in forced submer-sions should also enhance pulmonary blood flow andlung-to-blood O2 transfer, thus contributing to rapidutilization of the respiratory O2 store.

In contrast, in emperor penguins Aptenodytesforsteri diving at an isolated dive hole, dive ƒH oftendeclined below levels of birds resting on ice andeven reached levels recorded during simulateddives, especially in dives beyond the previouslymeasured 5.6-min aerobic dive limit (ADL; diveduration associated with the onset of a net accumula-tion of lactic acid above resting levels) (Kooyman1989, Ponganis et al. 1997, 1999a, Meir et al. 2008).These lower ƒH values, especially in longer dives,imply a greater reliance on muscle O2 stores inemperor penguins than in other penguin species.Indeed, myoglobin desaturation profiles in divingemperor penguins revealed that the large muscle O2

store is utilized and often depleted, although at vari-able rates and in variable patterns (Williams et al.2011). The low ƒH values observed in emperor pen-guins diving at an isolated dive hole likely con-tributed to the slow venous O2 depletion observed indives as long as 22 min and to maintenance of arterialoxygen saturation during most of the dive, includingdives as long as 10 min (Meir & Ponganis 2009).

Regarding O2 store management of emperor pen-guins at sea, especially during their long, deep dives,the question remains as to whether a trade-offoccurs, analogous to that of king and macaroni pen-guins, between elevated ƒH values characteristic ofthe exercise response and depressed ƒH values spe-cific to the classic dive response. Or does a classicdive response with more extreme bradycardia pre-dominate, as with emperor penguins at the isolateddive hole? Lower ƒH values would conserve respira-tory and blood O2 at the potential expense of muscleO2 depletion and the subsequent onset of glycolysis,while higher ƒH values could lead to longer mainte-nance of aerobic muscle metabolism but more rapiddepletion of respiratory and blood O2 stores.

We investigated ƒH responses during dives ofemperor penguins making foraging trips to sea dur-ing the chick-rearing period. Specifically, we used anelectrocardiogram (ECG) recorder to measure ƒH and

a time depth recorder (TDR) to record the dive profilein order to: (1) examine the relationship betweendive ƒH (total heartbeats during the dive/dive dura-tion) and dive duration, (2) investigate how ƒH fluctu-ated throughout the course of dives of varyingdepths, and (3) examine the ƒH profile of dives of dif-ferent depths to evaluate the potential for variation inthe number of heartbeats, an index of cumulativecardiac output, during different segments of thesedives.

We suspected that, because both the diving air vol-ume and the total number of wing strokes during adive increased with maximum dive depth in emperorpenguins (Sato et al. 2011), the total number of heart-beats during early descent and throughout thecourse of the dive would increase in deeper divesdespite an overall lower dive ƒH in order to accommo-date greater pulmonary gas exchange. A greaternumber of heartbeats, especially during the gradualdecline in ƒH typical of descent, could also potentiallyincrease muscle O2 delivery during that segment ofthe dive. Therefore, we hypothesized that: (1) dive ƒH

would negatively correlate with dive duration, (2)dive ƒH of dives >ADL would be less than resting ƒH,and (3) the total number of heartbeats would begreater in deeper dives throughout the total dive andduring the gradual decline in ƒH during descent.

MATERIALS AND METHODS

In November 2010 and 2011, emperor penguinswere captured at the sea-ice edge as they de -parted on foraging trips from the Cape Washingtonbreeding colony (74° 40’ S, 165°28’ E), equipped withECG recorders, TDRs, and VHF transmitters, andthen released. Upon return from foraging trips, pen-guins were recaptured to recover the devices. Allprocedures were approved under a University ofCali fornia San Diego Animal Subjects CommitteeProtocol (S02153) and a US Antarctic Treaty Permit(2011−016).

Instrument deployments

Under 0.5% bupivacaine local anesthetic (3−5 mlper bird), 2 subcutaneous ECG electrodes wereinserted dorsally, with one right of midline at thelevel of the axilla and the other left of midline abovethe pelvis in manually restrained, hooded emperorpenguins. The electrodes were connected to a cus-tom-built digital ECG recorder (3991 BioLog, UFI) in

86

Wright et al.: Emperor penguin heart rates at sea

an underwater cylindrical housing (215 g, 16 × 3 cm),secured to the feathers of the mid-back with 5 minepoxy glue (Loctite; Henkel Corp.) and steel cableties. ECG signals were recorded for 48 h at a sam-pling rate of 50 Hz. ECG recording was programmedto start 4 d after deployment of the recorder in orderto collect data during the mid-portion of the foragingtrip. Additionally, all birds were equipped with anMk9 TDR (Wildlife Computers; sensitive to 0.5 m,30 g, 6.7 × 1.7 × 1.7 cm) to record depth at a samplingrate of 1 Hz, and a VHF transmitter (Model MM130,ATS) to facilitate recapture.

Data processing and statistics

The ƒH and dive data were processed, graphed, andstatistically analyzed using Origin (ver. 8.6, Origin-Lab), Microsoft Excel, R software (R DevelopmentCore Team 2012), MATLAB (The MathWorks), andJMP (ver. 10.0.2, SAS Institute). TDR data were ana-lyzed in MATLAB using a custom-written dive analy-sis program (IKNOS; Y. Tremblay unpubl.) andInstrument Helper (Wildlife Computers), which cal-culated a zero offset correction at the surface andidentified dives on the basis of a minimum depth andduration. Dives were defined as submergences of≥5 m and ≥1 min. Dive depth categories were desig-nated as shallow (<50 m), intermediate (50−250 m),and deep (>250 m). ECG and TDR data were syn-chronized and a custom peak detection program (K.Ponganis) was utilized to mark R-wave peaks fromthe digital ECG records and calculate R-R intervals inOrigin. All peaks were visually confirmed in order toensure marking accuracy. The number of dives ana-lyzed for individual birds was dictated by the clarityof the ECG signal. Portions of the ECG record thatwere difficult to decipher were omitted (n = 48 diveswith ƒH data gaps; all gap durations were <5% ofdive duration).

A custom R script was used to determine dive ƒH

and total dive heartbeats. Dive ƒH for each dive wascalculated from the total number of heartbeats foreach dive divided by the dive duration. In dives witha gap in the ECG record (<5% of dive duration), thegap duration was subtracted from the dive durationin the calculation of the overall dive ƒH. Pre- andpost-dive ƒH values were calculated from the totalnumber of heartbeats during the final and initialminute prior to and following a dive, respectively.Lowest resting ƒH values were determined for indi-vidual birds over a period of 1 h. Resting periodswere selected during long surface intervals at least

1 h after or before a dive bout, when the birds werepresumably at rest.

Total number of heartbeats during a dive and thenumber of heartbeats from the start of a dive to thetime that instantaneous ƒH was consistently belowresting ƒH were determined through visual inspec-tion of ƒH profiles for each dive. Dives with ƒH datagaps resulting from brief periods of indecipherableECG signals were omitted from this analysis.

Mean ƒH values at 30 s intervals were also ana-lyzed by dividing depth profiles of dives into 7 cate-gories of dive depth (0−25, >25−50, >50−100, >100−150, >150−250, >250−400, and >400 m). Instanta-neous ƒH for 30 s periods was determined using acustom R script and calculated as the mean of allinstantaneous ƒH values within a 30 s period. Diveswith ƒH data gaps resulting from brief periods ofindecipherable ECG signals were excluded from thisanalysis.

Linear mixed-effects models (JMP) were used toexamine the relationships of dive duration with diveƒH, dive depth with total dive heartbeats, and diveduration with total dive heartbeats. One model wasfitted with dive ƒH as a response variable, dive dura-tion as a fixed effect, and individual as a randomeffect to account for repeated measures. A secondmodel was fitted with total dive heartbeats as aresponse variable, dive depth as a fixed effect, andindividual as a random effect. A third model was fit-ted with total dive heartbeats as a response variable,dive duration as a fixed effect, and individual as arandom effect. An additional model was constructedto assess whether dive ƒH values for dives with dura-tions less than or greater than ADL (5.6 min) (Ponga-nis et al. 1997) were significantly different, with diveƒH as a response variable, dive duration category(< or >ADL) as a fixed effect, and individual as a ran-dom effect. Corrected Akaike’s information criterion(AICc) was used to select the most parsimoniousmodel. All means and medians are listed as means ±SE and median (range).

RESULTS

Data recovery

The ECG signal was indecipherable in 2 of 6 birds,due to obfuscation of the signal by muscle artifactand possibly movement of ECG electrodes ormechanical malfunction. Consequently, simultane-ous measurements of instantaneous ƒH and depthwere recorded from 4 birds (24.6 ± 0.4 kg), resulting

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Mar Ecol Prog Ser 496: 85–98, 2014

in ƒH and depth records for 392 dives ≥1 minin duration.

Resting heart rate profiles

Resting ƒH ranged from 50 to 71 beatsmin−1 (n = 4 birds; Table 1). However, it isunknown whether the lowest resting ƒH

calculated for Penguin 2 was the minimumresting ƒH over a 1 h period because of adearth of resting hours with high signal clar-ity. Excluding Penguin 2, resting ƒH rangedfrom 50 to 64 beats min−1, with a mean of56 ± 4 beats min−1 (n = 3 birds; Table 1). Forthis study, 56 ± 4 beats min−1 was selected asa conservative estimate of resting ƒH for free-ranging emperor penguins.

General description of dive behavior

Dive durations from all dives ranged from1 to 9.42 min, with a grand median of3.08 min (Table 1). Sixty-one percent ofdives were shorter than 4 min (Fig. 1A).Twenty-one percent of dives in the studywere greater in duration than the previously

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Fig. 1. Aptenodytes forsteri. Distributions of (A)dive duration and (B) maximum dive depth, and(C) dive duration versus maximum dive depth ofdives from emperor penguins (EP) at sea. In (C),indi vidual birds are denoted by color (n = 4 birds,

392 dives)

Penguin Body mass No. of Resting ƒH Maximum depth Dive duration Dive ƒH

(kg) dives (beats min−1) (m) (min) (beats min−1)

1 25.0 87 55 127.0 ± 8.2 5.10 ± 0.17 67 ± 1126.0 (15.0−340.0) 5.18 (1.32−8.77) 68 (38−90)

2 24.0 54 71 96.0 ± 7.3 5.04 ± 0.20 68 ± 1100.3 (5.0−246.0) 5.23 (1.32−7.22) 67 (53−91)

5 25.5 247 50 44.1 ± 4.3 2.88 ± 0.11 61 ± 119.0 (6.0−422.5) 2.23 (1.00−9.22) 62 (9−117)

7 24.0 4 64 299.8 ± 89.9 6.96 ± 1.52 64 ± 6364.5 (39.0−431.0) 7.82 (2.80−9.42) 64 (52−76)

Grand meana 24.6 ± 0.4 56 ± 4b 72.3 ± 4.1 3.71 ± 0.10 64 ± 1Grand median (range)a 24.5 (24−25.5) 55 (50−64)b 32.5 (5.0−431.0) 3.08 (1.00−9.42) 64 (9−117)aPooled data (n = 4 birds, 392 dives); bPenguin 2 was excluded from resting ƒH grand mean and median

Table 1. Aptenodytes forsteri. Individual and pooled heart rate (ƒH) data of emperor penguins diving at Cape Washington. Thenumber of dives for each bird was dictated by the clarity of the ECG signal. Maximum depth, dive duration and dive ƒH are

presented as means ± SE and medians (range)

Wright et al.: Emperor penguin heart rates at sea

measured ADL of 5.6 min, and 4% of dives weregreater than 8 min. Maximum depth of all divesranged from 5 to 431 m, with a grand median of32.5 m. The maximum dive depth for each birdranged from 246 to 431 m (Table 1). Most dives wereshallower than 100 m; however, 30% of dives weredeeper than 100 m, and 5% of dives were deeperthan 250 m (Fig. 1B).

Heart rate profiles during diving

All dives exhibited a characteristicpattern of ƒH, with a pre- and post-divetachycardia during surface intervals, re -duced ƒH upon submersion and through -out dives, and anticipatory tachycardia(increase in ƒH coinciding with ascent)prior to surfacing. The pre-dive tachy-cardia (median = 202 beats min−1, range= 109−231 beats min−1) and post-divetachycardia (median = 200 beats min−1,range = 145−226 beats min−1) were both>ƒH at rest (56 beats min−1). Instanta-neous ƒH profiles in 3 dives of varyingdepth are shown in Fig. 2. The ƒH

response was characterized by: (1) pre-and post-dive tachycardia, (2) an abruptpartial decline from pre-dive levels(usually with a transient de crease tobelow resting levels), (3) a progressive,gradual decline in ƒH during earlydescent, sometimes to below resting lev-els, (4) a continuation of lower ƒH valuesduring the bottom phase of the dive, and(5) a gradual increase in ƒH duringascent (Fig. 2, 3). In 27% of dives, diveƒH was below the resting level of 56beats min−1 (Table 2).

Diving heart rate and dive duration

The median dive ƒH was 64 beatsmin−1 (range = 9−117 beats min−1) for alldives (Table 1). The median dive ƒH

for dives shorter than the ADL (79% ofthe dives in this study; 66 beats min−1,range = 9−117 beats min−1) was signifi-cantly greater than the median dive ƒH

of 58 beats min−1 (range = 38−76 beatsmin−1) for dives longer than the ADL (21%of the dives in this study; Tables 2, 3).

Eighteen percent of dives below the ADL had dive ƒH

values less than the resting level of 56 beats min−1,while 45% of dives above the ADL had dive ƒH valuesless than 56 beats min−1 (Table 2). For the previouslyreported ƒH at rest of 73 beats min−1 (Meir et al. 2008)in emperor penguins at the isolated dive hole, dive ƒH

was less than resting ƒH in 76% of dives shorter thanthe ADL and in 98% of dives longer than the ADL.

In dives ≥1 min in duration, there was a significantnegative relationship between dive duration anddive ƒH (Fig. 4, Table 3). However, dive ƒH of dives

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Fig. 2. Aptenodytes forsteri. Instantaneous heart rate (ƒH) and dive depth pro-files from (A) a shallow (27 m, <aerobic dive limit [ADL]) dive of Emperor Pen-guin 1, (B) an intermediate (183 m, >ADL) dive of Emperor Penguin 2, and (C)the deepest (423 m, >ADL) dive of Emperor Penguin 5. In (A), ƒH reaches a min-imum of 52 beats min−1. In (B), ƒH reaches a minimum of 33 beats min−1. In (C),mean ƒH is 17 beats min−1 for over 3 min, reaching a minimum of 8 beats min−1

Mar Ecol Prog Ser 496: 85–98, 2014

less than 2 min in duration or less than 50 m in depthvaried considerably (Fig. 4).

In the analysis of dive ƒH, 12% of dives had a datagap in the ƒH profile. Eighty-one percent of gaps were≤5 s and 75% of all gaps occurred at the start of thedive when wing movement, and thus the potential formuscle artifact, was greatest. Gaps of short durationshould not significantly affect the results or interpre-tation of the data. For example, a dive with a 6 s gapand dive ƒH of 100 beats min−1 would only have an increase in dive ƒH by 2 beats min−1 for a 5 min dive.

Heart rate within dives

For all dives at sea with a complete ECG record(without a ƒH data gap; 344 dives), total number of

dive heartbeats was in the same range as total heart-beats for dives of equivalent duration performed atthe isolated dive hole (Meir et al. 2008) (Fig. 5). Fordives near 5−7 min in duration, total dive heartbeatsranged between 250 and 400 heartbeats (Fig. 5).

In dives ≥1 min in duration, there was a significantrelationship between dive depth and total number ofdive heartbeats (Fig. 6A, Table 3). Total dive heart-beats was variable but increased until 150 m maxi-mum depth, after which total dive heartbeats beganto level off and remained high (Fig. 6A). A significantrelationship was also observed between dive dura-tion and total number of dive heartbeats (Fig. 6B,Table 3).

Instantaneous ƒH reached values consistentlybelow resting ƒH in 31% of dives (dives without gapsin the ƒH profile). The number of heartbeats prior to

90

No. dives Maximum depth Dive duration Dive ƒH % dives with dive ƒH

(m) (min) (beats min−1) below resting ƒH

All dives 392 72.3 ± 4.1 3.71 ± 0.10 64 ± 1 27 32.5 (5.0−431.0) 3.08 (1.00−9.42) 64 (9−117)

Dives < ADL 310 40.4 ± 2.3 2.91 ± 0.07 65 ± 1 18 23.5 (5.0−191.5) 2.58 (1.00−5.57) 66 (9−117)

Dives > ADL 82 192.9 ± 9.3 6.74 ± 0.11 57 ± 1 45 160.5 (83.5−431.0) 6.43 (5.63−9.42) 58 (38−76)

Table 2. Aptenodytes forsteri. Heart rate (fH) data for dives shorter and longer than the aerobic dive limit (ADL; 5.6 min). Maximum depth, dive duration and dive fH are presented as means ± SE and medians (range)

00:36:00 00:38:00 00:40:00 00:42:00

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a a

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Fig. 3. Aptenodytes forsteri. Instantaneous heart rate (ƒH) and dive depth profiles from a deep (301 m) dive of Emperor Penguin5 with prominent features typical of the dive ƒH profile: a, surface interval tachycardia (pre- and post-dive); b, initial sharp partial decline in ƒH, immediately upon submersion, often with transient decrease to below resting levels; c, gradual decline inelevated ƒH during early descent; d, prolonged severe bradycardia during latter descent and near maximum dive depth;

e, slow increase in ƒH during ascent

Wright et al.: Emperor penguin heart rates at sea

reaching resting ƒH (56 beats min−1) wasvariable (2−164 heartbeats), but as depthof dive increased, variability decreased,and values leveled off and remained be -tween 100 and 120 heartbeats in most dives(Fig. 7A). A similar relationship was ob -served between the dive depth and thenumber of heartbeats prior to reaching thepreviously reported resting ƒH (Meir et al.2008) (Fig. 7B).

The profiles of mean instantaneous ƒH

at 30 s intervals of dives in 7 dive depthcategories (Fig. 8) reflected instantaneousƒH profiles. Deeper dives had higherinitial 30 s values, but then had lower ƒH

values throughout the middle portionsof dives.

DISCUSSION

Resting heart rate

The resting ƒH for free-ranging emperorpenguins (56 ± 4 beats min−1) was signifi-cantly less than the resting ƒH determinedfor emperor penguins at the isolated divehole (Meir et al. 2008). Differences in sur-rounding conditions can affect baseline ƒH

and may account for the large disparity ofresting ƒH values observed in free-rangingand captive emperor penguins (Halsey etal. 2008). Resting ƒH for emperor penguinsat the isolated dive hole may have beenelevated due to stress associated with cap-tivity, interactions with other birds, differ-ences in dive and prey types, and longerdiving recovery periods. In addition, thelower resting ƒH values of emperor penguins at sea were the minimum 1 hresting ƒH values found during prolongedsurface intervals. These lower ƒH valuesmay occur during sleep and reflect alower metabolic rate induced by sleep(Stahel et al. 1984, Dewasmes et al. 1989,Halsey et al. 2008). Thus, in our analysesof dive ƒH, we consider the resting ƒH of73 and 56 beats min−1 to represent theupper and lower limits of resting ƒH,respectively (Fig. 7), and, consequently,the upper and lower thresholds for ƒH

associated with a resting level of muscleblood flow.

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Mar Ecol Prog Ser 496: 85–98, 2014

Dive behavior

Dive durations and maximum depths of dives ofemperor penguins in this study (Fig. 1A,B) were typ-ical of those reported in previous studies of free-ranging emperor penguins on foraging trips to seaduring the chick-rearing period (Kooyman & Kooy-man 1995, Kirkwood & Robertson 1997, Wienecke etal. 2007, Sato et al. 2011, Williams et al. 2012) and ofdive durations of emperor penguins at the isolateddive hole (Ponganis et al. 2001, 2007, Meir et al. 2008,Sato et al. 2011, Williams et al. 2011). The tightly cou-pled positive relationship between dive duration andmaximum dive depth (Fig. 1C) during foraging trips

to sea was similar to results from prior studies of free-ranging emperor penguins (Kooyman & Kooyman1995, Sato et al. 2011). Despite the exclusion of divesless than 1 min in duration, the grand median diveduration was 3.08 min (range = 1.00−9.42 min; Table 1),below the ADL of 5.6 min.

Heart rate profiles during dives

Examination of individual ƒH profile patterns re -vealed notable differences between shallow (<50 m)and deep (>250 m) dives. In shallow, short-durationdives, the overall ƒH pattern was similar to that

92

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30

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120 EP 1 Shallow EP 1 Intermediate EP 1 Deep EP 2 Shallow EP 2 Intermediate EP 2 Deep

EP 5 Shallow EP 5 Intermediate EP 5 Deep EP 0 Shallow EP 7 Intermediate EP 7 Deep

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(bea

ts m

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)

Dive duration (mm:ss)Fig. 4. Aptenodytes forsteri. Dive heart rate (ƒH) (total number of heartbeats/dive duration) versus dive duration for emperorpenguins (EP) at sea. Individual birds are denoted by color; dive depth categories (shallow: <50 m; intermediate: 50−250 m;

deep: >250 m) are denoted by symbols (see key; n = 4 birds, 392 dives)

00:00 02:00 04:00 06:00 08:00 10:00 12:00 14:00 16:00 18:00 20:000

100

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Present study Meir et al. (2008)

Tota

l div

e he

artb

eats

Dive duration (mm:ss)

Fig. 5. Aptenodytes forsteri. Total dive heartbeats versus dive duration for the present study of emperor penguins diving at sea(n = 4 birds, 344 dives) and the Meir et al. (2008) study of emperor penguins diving at an isolated dive hole (n = 9 birds, 125 dives)

Wright et al.: Emperor penguin heart rates at sea

observed in other free-ranging penguin species(Green et al. 2003, Froget et al. 2004) and in emperorpenguins making short dives at an isolated dive hole(Meir et al. 2008). The ƒH profile pattern of thesedives was characterized by an initial rapid decreasein ƒH from pre-dive values, followed by a gradualdecline in ƒH throughout the dive to a level some-times below that at rest, and lastly, an increase inƒH during ascent (Fig. 2A). Although shallow, short-duration dives of emperor penguins had ƒH profilepatterns similar in shape to those of free-rangingbirds of other penguin species, the ƒH values duringthese shallow dives were much lower in emperorpenguins than in the other species. Instantaneous ƒH

and overall dive ƒH of these shallow dives were loweron both an absolute and a relative-to-resting basisthan in the other 2 penguin species. Therefore, ifthere is a trade-off between the elevated ƒH of theexercise response and the depressed ƒH of the classicdive response in emperor penguins, the response of

the emperor penguin is much closer to the classicdive response than those of other penguins.

In contrast to shallow dive profiles of emperor pen-guins (both at sea and at an isolated dive hole) and alldive profiles of free-ranging king and macaroni pen-guins, the ƒH profile pattern of emperor penguins indeep, long-duration dives differed in that the gradualdecline in ƒH during early descent culminated in asevere bradycardia to as low as 10 beats min−1 duringlate descent and during the bottom phase of the dive(Figs. 2C, 3, 8). Dives to intermediate depths had less-intense bradycardias than the deep dives, but rateswere lower than during shallow dives (Figs. 2B, 8).

The extremely low ƒH during late descent or nearthe greatest depth of deep dives may serve to limitpulmonary gas exchange as well as peripheral perfu-sion during this segment of the dive. In addition toconserving respiratory O2 for potential use later inthe dive, the extreme bradycardia should also limitnitrogen absorption at maximal depths of deep dives,

93

00:00 02:00 04:00 06:00 08:00 10:000

50

100

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250

300

350

400

450

500

550

600

EP 1EP 2EP 5EP 7

Tota

l div

e he

artb

eats

Dive duration (mm:ss)

0 50 100 150 200 250 300 350 400 4500

50

100

150

200

250

300

350

400

450

500

550

600

EP 1EP 2EP 5 EP 7

Tota

l div

e he

artb

eats

Maximum dive depth (m)

A

B

Fig. 6. Aptenodytes forsteri. Total dive heartbeats versus (A) maximum dive depth and (B) dive duration for emperor penguins (EP) at sea. Individual birds are denoted by color (see key; n = 4 birds, 344 dives)

Mar Ecol Prog Ser 496: 85–98, 2014

a potential advantage in avoidance of decompressionsickness. The decrease in cardiac output associatedwith a bradycardia of 10−20 beats min−1 would alsolimit perfusion of central organs and muscle, de -creasing the rate at which blood O2 is consumed andisolating muscle from the circulation. During this bot-tom phase of deep dives, stroke rates are highest(Williams et al. 2012), so the locomotory muscle, iso-lated from the circulation, is most probably depend-ent on myoglobin-bound O2 for maintenance of aero-bic metabolism.

Heart rate and the potential for muscle blood flowduring dives

In 27% of all dives, the dive ƒH was less than thelower limit of ƒH at rest (56 beats min−1). In 45% ofdives greater than the ADL and 18% of dives shorterthan the ADL, dive ƒH demonstrated a true brady -cardia across a range of dive depths at sea (Table 2).Additionally, the degree of bradycardia during divesincreased with dive duration (Fig. 4). Such low ƒH val-ues (even relative to surface ƒH or resting ƒH) have not

94

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Maximum dive depth (m)

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600 EP 1 Total dive heartbeats EP 1 Heartbeats to resting ƒH EP 2 Total dive heartbeats EP 2 Heartbeats to resting ƒH

EP 5 Total dive heartbeats EP 5 Heartbeats to resting ƒH EP 7 Total dive heartbeats EP 7 Heartbeats to resting ƒH

Hea

rtb

eats

Maximum dive depth (m)

A

B

Fig. 7. Aptenodytes forsteri. Total dive heartbeats (squares) and heartbeats to reach resting heart rate (ƒH; triangles); (A) 56beats min−1 (present study) and (B) 73 beats min−1 (Meir et al. 2008) versus maximum dive depth for emperor penguins (EP) at

sea. Individual birds are denoted by color (see key; n = 4 birds, 105 dives in A, 301 dives in B)

Wright et al.: Emperor penguin heart rates at sea

been reported in free-ranging macaroni and king pen-guins (Green et al. 2003, Froget et al. 2004). Lowerdive ƒH of emperor penguins at sea suggests relativelylower organ blood flow and lower muscle blood flowthan in other penguin species, with slow depletion ofblood O2 and greater dependence of aerobic musclemetabolism on the higher O2 content of muscle in em-peror penguins (Ponganis et al. 2010, 2011). The myo-globin concentration of emperor penguin locomotorymuscle is about 1.5 to 2 times greater than in otherpenguin species (Weber et al. 1974, Baldwin et al.1984, Ponganis et al. 1999b). Thus, while the distribu-tion of O2 stores is similar in emperor and king pen-guins, emperor penguins have higher muscle myoglobinconcentrations and greater muscle O2 stores (Ponganiset al. 2010, 2011). Consequently, in regard to musclemetabolism, emperor penguins would be more toler-ant of muscle ischemia and depressed ƒH than otherpenguin species. In addition, due to their large size,the locomotory effort of the emperor penguin is po-tentially less than that of other penguin species, lead-ing to a lower muscle metabolic rate and myoglobindesaturation rate (Sato et al. 2010). Thus, both largermuscle O2 stores and less locomotory effort in em -peror penguins probably make them more tolerantthan other penguin species of lower ƒH and lessmuscle perfusion during both shallow and deep dives.

It is also notable, in regard to potential restriction ofmuscle blood flow during dives at sea, that the totalnumber of heartbeats in dives of equivalent duration

were similar in emperor penguins at sea and at theisolated dive hole (Fig. 5). Given that the number ofwing strokes for dives of equivalent duration wasgreater at sea than at the isolated dive hole (Sato et al.2011), the similarity between total heartbeats for divesof equivalent duration at sea and at the isolated divehole suggests that the relationship of muscle work ef-fort and ƒH (i.e. muscle blood flow and O2 delivery) iseven more restricted at sea than at the isolated divehole, resulting in greater dependence on myoglobin-bound O2. Alternatively, one might propose that se-lective dilatation of the locomotory muscle vascularbed as demonstrated in diving ducks may also occurin penguins (Bevan & Butler 1992). Such dilatationduring dives at sea could then account for a greaterdistribution of cardiac output to muscle and, thus, al-low more muscle blood flow per heartbeat. However,this has not been investigated in diving penguins. Inaddition, ƒH of the diving duck is much higher, evenon a relative basis (Bevan & Butler 1992), than that ofdiving emperor penguins.

Comparison of the relationships of total number ofheartbeats and total number of wing strokes with diveduration offers additional support for a reduction inmuscle blood flow in prolonged dives of free-rangingemperor penguins. The total number of heartbeats ina dive leveled off at approximately 6 min duration(Fig. 6B); in addition, for dives be tween 6 and 10 minof individual birds, the total number of heartbeats iswithin the same range. In contrast, the total number of

95

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0 – 25 m >25 – 50 m >50 – 100 m >100 – 150 m >150 – 250 m >250 – 400 m >400 m

00:00 01:00 02:00 03:00 04:00 05:00 06:00 07:00 08:00 09:00 10:00

Fig. 8. Aptenodytes forsteri. Profiles of mean heart rate (ƒH) at 30 s intervals of dives for 7 depth categories (0−25, >25−50, >50−100, >100−150, >150−250, >250−400, and >400 m). Standard error bars shown (n = 4 birds, 344 dives)

Mar Ecol Prog Ser 496: 85–98, 2014

strokes during dives of emperor penguins at sea in-creased linearly with dive duration, with 10 min diveshaving nearly twice the number of strokes as 6 mindives (Sato et al. 2011). Despite a 2-fold increase inthe total number of strokes between 6 min and 10 mindives, there is no increase in the total number ofheartbeats, which again would suggest a greater re-liance on muscle myoglobin and less muscle bloodflow relative to stroke rate for longer dives.

Although myoglobin desaturation profiles of divingemperor penguins have demonstrated that muscleblood flow may occur during dives (Williams et al.2011), the findings of the present study do not offerany evidence that there is a coupling of stroke rate(muscle workload) and ƒH, as in a classic exercise ƒH

response or even as in the exercise-modified diveresponse suggested in other penguin species and,more recently, in dolphins and seals (Butler 1988,Green et al. 2003, Davis & Williams 2012). The lack ofcoupling of ƒH and stroke rate is reflected, especiallyin deeper dives, by the fact that the lowest ƒH valuesin the deepest dives of emperor penguins (Fig. 8) oc -curs at a time when previously measured stroke ratesare near maximal levels (Williams et al. 2012). Simi-larly, although muscle blood flow may be enhancedby increasing ƒH during ascent (Figs. 2, 3, 8), strokerate is declining during this period (Williams et al.2012). The same conclusion of a lack of coupling ofstroke rate and ƒH was also reached from ƒH andstroke rate analyses during dives of emperor pen-guins at an isolated dive hole (Meir et al. 2008).

In contrast, because ƒH and stroke rate during divesat sea are always highest during initial descent(Figs. 2 & 8) (Williams et al. 2012), it could be arguedthat muscle blood flow matches work effort at leastduring this period of the dive. However, during thistime, at least in dives at the isolated dive hole, venouspartial pressure of O2 (PO2) and hemoglobin satura-tion are usually increasing, sometimes to arterial lev-els (Meir & Ponganis 2009). With increasing venoussaturations it is un likely that there is muscle bloodflow and muscle O2 extraction; if there were suchflow to exercising muscle, venous saturation shoulddecrease. Indeed, it has been suggested that arterial-ized venous blood O2 levels early in the dive are con-sistent with flow-through peripheral arterio-venousshunts (Ponganis et al. 2009). Thus, the regulation ofmuscle blood flow during dives of emperor penguinsat sea still requires further investigation.

It should be noted that in shorter, shallower dives,emperor penguins exhibit a range of ƒH responses inrelation to resting ƒH limits, and therefore the muscleblood flow response may be variable during these

dives. For a large proportion of short, shallow dives,the ƒH response of emperor penguins resembles thatof other penguin species with a high potential formuscle blood flow and reduced dependence on myo-globin. However, when dive ƒH exceeds resting ƒH

in shallow dives, it is still unknown whether divingemperor penguins perfuse muscle or possibly utilizeperipheral arterio-venous shunts to enhance bloodO2 levels (Ponganis et al. 2009, Williams et al. 2011).

Heart rate and the potential for pulmonary bloodflow during dives

The higher ƒH values during short-duration, shallowdives imply more pulmonary blood flow, greaterpotential for gas exchange and more rapid utilizationof the respiratory O2 store than during deep dives.Although overall ƒH is slower in longer dives (Fig. 4),the total number of heartbeats is maximal during thesedeeper dives secondary to (1) the duration of the dive,(2) the greater number of beats during early descent,and (3) the gradual increase in ƒH during long ascents(Figs. 2, 3, 8). Thus, despite an overall low dive ƒH andextreme bradycardia during the late descent and bot-tom phases of the deepest dives, the cumulative poten-tial for pulmonary blood flow and gas exchange ismaximized during these dives, consistent with the in -creased diving air volumes determined in deeper divesof emperor penguins (Sato et al. 2011). Overall utiliza-tion of the respiratory O2 store should be slower undersuch circumstances, although gas exchange is proba-bly greatest early in the dive, when ƒH values are high(Figs. 2, 3, 6−8) and when air movement through theparabronchi of the lung is increased by high wingstroke rates (Boggs et al. 2001). Higher ƒH values and amaximal number of strokes during this phase of deepdives (Figs. 6−8) support this suggestion. As alreadydiscussed, the severe bradycardias during the latedescent and bottom phases of deep dives would limitgas exchange at great depths, a potential advantagefor limiting nitrogen absorption as well as conservingrespiratory O2 for utilization during the increased ƒH

periods during ascent, as recently proposed for deep-diving sea lions (McDonald & Ponganis 2012).

Heart rate variability: a multi-factored response

Although the greater part of this discussion hasbeen devoted to variations in ƒH and implicationsfor pulmonary gas exchange and muscle blood flow,individual dive ƒH variability is also likely influenced

96

Wright et al.: Emperor penguin heart rates at sea

by an assortment of endogenous and exogenous fac-tors. In short, shallow dives, physiological variabilityhas been documented not only in ƒH responses butalso in levels and rates of blood O2 depletion and indiving air volumes (Meir & Ponganis 2009, Sato etal. 2011). ƒH and other physiological responses areclearly dependent on the nature and circumstancesof individual dives (Furilla & Jones 1987, Jones et al.1988, Noren et al. 2012). For example, extremely lowdive ƒH (range = 9−17 beats min−1) in a few short-duration dives in this study corresponded to diveswith very short surface intervals (descent following alimited post-dive surface interval of ≤5 s). After suchshort surface intervals, low dive ƒH in the subsequentdive may function to conserve partially loaded O2

reserves resulting from the abbreviated surfaceinterval and may also reflect uncertainty about thetiming of the next surface period. Future ƒH studies offree-ranging emperor penguins should aid in theinterpretation of dive responses in relation to specificbehaviors and circumstances of individual dives (i.e.hunting, prey capture, travelling, and escape).

In summary, we have investigated the diving ƒH re-sponse of emperor penguins during foraging trips atsea. We confirmed that: (1) dive ƒH varies inverselywith dive duration; (2) a significant proportion of diveshave dive ƒH values that are less than the value at rest,and dive ƒH of dives greater than the ADL is lowerthan dive ƒH of dives less than the ADL; (3) the totalnumber of heartbeats in dives of equivalent durationat sea was similar to that of birds diving at an isolateddive hole, but dive profiles, especially in deeper dives,had different ƒH patterns; (4) a profound bradycardiaoccurs during deep dives; and (5) the total number ofheartbeats, and thus the cumulative cardiac output, ismaximized in deep dives due to (a) the duration of thedive, (b) higher instantaneous ƒH and a maximizednumber of heartbeats during early descent, and (c)the increase in ƒH during the long ascent.

ƒH values below resting rates during long-duration,deep dives at sea are consistent with conservation ofblood and respiratory O2 stores and with significantreliance on myoglobin-bound O2 for aerobic musclemetabolism. Our findings suggest that adjustments todiving ƒH preserve blood and pulmonary O2 storesduring deep dives by: (1) maintaining higher ƒH topromote gas exchange during early descent and, per-haps, ascent periods, (2) lowering ƒH to decrease gasexchange during deep portions of dives, and (3) limiting muscle blood flow. In contrast, ƒH values dur-ing short-duration, shallow dives are usually higher,implying a greater potential for muscle perfusion,and perhaps also arterio-venous shunting.

Acknowledgements. We thank G. L. Kooyman, G. Marshall,J. Goldbogen, M. Tift, and M. Fowler for assistance in thefield, and J. U. Meir for use of ƒH data from the isolated divehole study. We greatly appreciate the support of the UnitedStates Antarctic Program and McMurdo Station staff, and inparticular, the efforts of the Berg Field Center, Fixed WingOperations, and the pilots/crew of Ken Borek Air. Thiswork was supported by National Science Foundation grant09-44220. A.K.W. was supported by the NSF GraduateResearch Fellowship Program.

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Submitted: February 15, 2013; Accepted: October 9, 2013 Proofs received from author(s): January 21, 2014