3 Animals and Location
N. b.: While the previous chapter (section 2.3) provided information on disturbance-related information on behaviour and heart rate, this section focuses on the physiological basis of penguin
3.1.5.2 Penguin Heart Rate
“Measurement of heart rate can be a useful measure of the emotional response of an individual to short-term problems, provided that distinction is made between the metabolic and emotional effects, and that the measurement itself does not cause too much disturbance.” (BROOM & JOHNSON 2000, p. 92)
All vertebrates exhibit a similar electrocardiogram (ECG) with distinctly negative55 (P, R, T) and positive (Q, S) spikes56 (fig. 3-17), labelled with capital letters according to international nomenclature (PENZLIN 1980). An ECG represents the summation of the electrical activity in various parts of the heart (RANDALL & al. 2002). The major components of the ECG reflect atrial depolarisation (P), ventricular depolarisation (QRS), and ventricular repolarisation (T). Each PQRST-event in its entirety represents ‘one heartbeat’. Heart rate is usually reported in ‘beats per minute’ (bpm), a value derived from counting PQRST-events over a defined period of seconds (counting interval) and extrapolating the resulting figure to minute-values57.
54 Upon immersion, the monocular fields shrink due to loss of corneal refractionary power (caused by presence of the same medium on both sides of the cornea); they cease to overlap, and this results in loss of binocularity in water.
55 Upward deflection of the spike indicates negativity of the heart’s base relative to its tip. [Ausschlag nach oben bedeutet Negativwerden der Herzbasis gegenüber der Herzspitze. (PENZLIN 1980, p. 249)]
56 The ECG of fish and reptiles is characterised by an additional initial spike (V), representing depolarisation of the Sinus (PENZLIN 1980).
57 It is also possible to count a predefined number of heartbeats and subsequently extrapolate the seconds to 1 min.
Figure 3-17: Schematic Vertebrate ECG. All vertebrates exhibit a similar electrocardiogram (ECG) with distinctly negative (P, R, T) and positive (Q, S) spikes. From RANDALL & al. (2002)
As for penguin studies, counting intervals mentioned by different authors were found to vary quite widely: NIMON (1997), for instance, used counting intervals of 5 s, 10 s, and 15 s, respectively, in her study on heart rate in Gentoo penguins, Pygoscelis papua. For Royal penguins, Eudyptes
schlegeli, HOLMES & al. (2005) extrapolated from intervals of 5 s and 15 s, while ELLENBERG & al.
(2006, 2009) established intervals of 12 s for Humboldt, Spheniscus humboldti and Yellow-eyed penguins, Megadyptes antipodes, respectively. DEVILLIERS & al. (unpubl. data) as well as THISSTUDY
chose 20 s counting intervals for reasons outlined below.
A Brief Excursus on ECG Counting Intervals and Extrapolation Bias/ Error
Different counting intervals capture different aspects of the heart rate actually obtained: Brief to very brief changes in beat-to-beat variability are accentuated in shorter intervals, while longer intervals reflect a longer-lasting response in this parameter. Extrapolation to beats per minute values (bpm), however, creates a ‘common currency’ which may inadequately represent these different aspects. The following example illustrates the results of different counting intervals:
Figure 3-18 shows one minute of resting heart rate containing a total of 77 heartbeats (top), the number of heartbeats counted in successive counting intervals of five different durations, and the derived bpm-values for these counting intervals (bottom).
Differences between consecutive intervals of identical duration primarily arise from the fact that even during rest (no activity, no ‘emotional upheaval’), heartbeats do not strictly adhere to a second-by-second pattern and thus do not neatly fit into counting intervals. Rules for incorporation of ‘in-between intervals’ heartbeats are therefore set up, and these are used to unequivocally assign the respective beat. Mostly, this will lead to only minor differences from one interval to the next (fig. 3-18: ± 1 beat, as seen between most counting intervals regardless of duration). These
Figure 3.18: One Minute of Adélie Penguin Resting Heart Rate (top), and Heartbeats Counted in Successive Counting Intervals of Different Durations (bottom). Counting the entire 60 s, the sum of heartbeats totals 77 beats.
In the bottom part, successive counts and the resulting bpm-values are shown for interval durations of 5 s, 10 s, 12 s, 15 s, and 20 s, respectively.
differences, however, are artificially augmented by extrapolation, and for short intervals may suggest great fluctuations in heart rate when in reality only a gentle undulation occurs.
The size of the extrapolation bias increases with increasing shortness of counting interval chosen and equals the extrapolation factor (the factor the counted value is multiplied by; see tab. 3-2). The same applies to ‘truly misassigned’ beats, in that the extrapolation error increases with decreasing duration of counting interval/ increasing extrapolation factor.
Table 3-2: Size of Extrapolation Bias for Different Counting Intervals.
METHODOLOGICAL CONSIDERATION: In THISTHESIS, heartbeats were counted for 20 s-intervals58 of heart rate obtained by continuous recording (see section 4.3.3.1.3 for details). To exclude extrapolation bias as well as to minimise extrapolation errors, however, values are presented ‘as counted’, i.e., as beats per 20 s. Comparison to other studies may be effected by tripling values reported here.
Table 3-3 provides maximum heart rates measured during various activities, while table 3-4 lists the resting heart rates obtained for a number of penguin species. As already mentioned (Theoretical Background, section 2. 3.1.3), the devices used to measure heart rate in penguins range from implants requiring surgery before and after the study (e.g., CULIK & al. 1990a, 1990b), via subcutaneous electrodes attached to an external recorder (e.g., CULIK & al. 1990b, GIESE 1998) to equipment the penguin has to make unrestrained contact with (e.g., NIMON 1997; GIESE & al. 1999).
Maximum heart rates were measured during or immediately after terrestrial exercise and upon resurfacing after or in-between dives (tab. 3-3), while during diving, heart rate as low as or even considerably lower than resting heart rate was recorded (minimum HR reported: MEIR & al.
2008: 3 bpm for an Emperor penguin, Aptenodytes forsteri, during a long dive).
Heart rate of (Adélie) penguin chicks is reported to be distinctly higher than that measured for adult penguins regardless of activity (CULIK & al. 1990a, 1990b). During capture of an adult Adélie, however, WILSON, R.P. & al. (1991) obtained heart rate elevations (from 76 bpm to 287 bpm) the absolute values of which came close to those measured in a chick subjected to the same procedure (from 225 bpm to 310 bpm). Moreover, the difference between resting heart rate and that measured during capture was greater for the adult (increase by 211 bpm) than for the chick (increase by 85 bpm).
In a study on Macaroni penguins, Eudyptes chrysolophus, GREEN & al. (2001) found that moulting females exhibited higher resting heart rates than breeding birds of either sex.
58 Given that in THISSTUDY resting heart rates obtained from focal animals were similar to those in humans, this interval length was opted for after consulting an ECG-trained nurse (B. PELESKA d.Ä., pers. comm.).
Counting Interval
n Heartbeats Counted à bpm
n + 1 Heartbeats Counted à bpm
Extrapolation Factor (effecting bpm)
=ˆ Extrapolation Bias (per beat assigned)
05 s 06 à 72 07 à 84 12
10 s 13 à 78 14 à 84 06
12 s 15 à 75 16 à 80 05
15 s 19 à 76 20 à 80 04
20 s 25 à 75 26 à 78 03
Table 3-3: Maximum Heart Rates of Several Penguin Species during Various Forms of Exercise. Device: Heart rate measuring apparatus; bpm = beats per minute; Specification = type of activity; N = number of animals examined; f.:
female, m.: male; poss.: possibly
Species Species (lat.) Device HR active (bpm) Specification N Authors Year 287 capture 1
implants
287
helicopter approach up to 25m
2
WILSON, R.P.
& al. 1991
127 ± 6
stand & preen/
manipulate nest/
rearrange eggs external ECG 11
recorder, externally attached electrodes
127 ± 10 human
disturbance 9
CULIK & al. 1989 Adélie Pygoscelis
adeliae
external ECG recorder, externally attached electrodes
145 (range:
139 - 150)
helicopter overflight at 20m
1 CULIK & al. 1990a implanted telemetric
heart rate transmitter 310 capture and
weighing 1 CULIK & al. 1990b Adélie
chick
Pygoscelis
adeliae a) safety pin electrodes and external ECG (N = 10) and b) implants (N = 4)
276 ± 6 treadmill
experiment 1 CULIK & al. 1990b up to 250 pre-dive 2
implants
218 ± 6 post-dive 2 CULIK 1992 Adélie Pygoscelis
adeliae implanted arterial catheter and external pressure transducer in watertight chamber
278
mean after vigorous running
3 MILLARD & al. 1973
Gentoo Pygoscelis papua
implanted arterial catheter and external pressure transducer in watertight chamber
386 (+ 267% resting
value)
surfacing
post-dive 1 MILLARD & al. 1973
245 ± 24 run 3
Humboldt Spheniscus
humboldti implant
231 ± 10 immediately post-dive 3
BUTLER &
WOAKES 1984
moulting females:
implants 193 ± 11 treadmill
moulting f. 6 breeding females:
external devices 166 ± 7 treadmill
breeding f. 9 Macaroni Eudyptes
chrysolophus
breeding males:
external devices 163 ± 5 treadmill
breeding m. 9
GREEN & al. 2001
standard ECG submersible recorder (external)
158 - 188
interdive HR;
poss. higher (counting programme limitations)
6 KOOYMAN & al. 1992 Emperor Aptenodytes
forsteri
subcutaneous electrodes and external ECG recorder
mean of means:
177 ± 3 (range of means:
97 - 256)
post-dive 9 MEIR & al. 2008
Table 3-4: Heart Rates of Several Penguin Species during Rest. Device: Heart rate measuring apparatus; bpm = beats per minute; N = number of animals examined; Specification: circumstances under which resting behaviour was observed, f.: female, m.: male; poss.: possibly.
Species Species (lat.) Device HR rest (bpm) Specification N Authors Year 76 not on nest 1
implants
83,4 incubating 2
WILSON, R.P.
& al. 1991 Adélie Pygoscelis
adeliae
external ECG recorder, externally attached electrodes
86 ± 5 (range: 83-91)
prone;
at zero windspeed
16 CULIK & al. 1989 220 sleeping 1
external ECG recorder, externally
attached electrodes 225 resting 1 CULIK & al. 1990b 182 ± 11 to 249 ± 5
inside respiration chamber
14 Adélie
chick
Pygoscelis
adeliae a) safety pin electrodes and external ECG (N = 10) and
b) implants (N = 4) 187 ± 5 to 245 ± 5 outside (in
cage or colony) 14
CULIK & al. 1990b
66.8 ± 1.4 incubating 1 implants
77.5 ± 1.6 incubating 1 CULIK 1992 implanted arterial
catheter and external pressure transducer in watertight chamber
mean: 122
(min.: 90) rest stand 3 (1) MILLARD & al. 1973
artificial egg
82.4 ± 8.1 (range of means:
69.5 - 91.7)
rest prone 10 Adélie Pygoscelis
adeliae
external ECG units 82.4 ± 11.7 rest prone 17
GIESE & al. 1999
implanted arterial catheter and external pressure transducer in watertight chamber
105 rest stand 1 MILLARD & al. 1973 Gentoo Pygoscelis
papua
artificial egg 79.5 to 105.8 rest prone 8 NIMON 1997 121 ± 5 stand on land 3
Humboldt Spheniscus
humboldti implant
139 ± 5 float on water 3
BUTLER &
WOAKES 1984 moulting females:
implants 125 ± 12 moulting
females 6 breeding females:
external devices 97 ± 2 breeding
females 9 Macaroni Eudyptes
chrysolophus
breeding males:
external devices 85 ± 4 breeding males 9
GREEN & al. 2001
standard ECG submersible recorder (external)
mean of means: 72 (range of means:
56 - 80)
stand on land 6 KOOYMAN &
al. 1992
Emperor Aptenodyte
forsteri subcutaneous electrodes and external ECG recorder
mean of means:
73 ± 2 (range of means:
63 - 84)
stand on land 9 MEIR & al. 2008
As mentioned in the previous chapter (Theoretical Background, section 2.3.1.3), CULIK & al. (1989), found Adélie penguin heart rate to increase linearly with wind speed (following the equation HR = 85.8 + 1.35w; with HR = heart rate in beats per minute; w = wind speed in meters per second), but to be unrelated to temperature, humidity, cloud cover and solar radiation. The same study reported that (after correcting for meteorological influences) heart rate did not show any diurnal periodicity.
Even after such corrections, however, individual variations in mean resting heart rate have been found by several authors (e.g., CULIK & al. 1989; GIESE & al. 1999). Furthermore, in those studies that reported the ‘range of means’ obtained instead of exclusively presenting a ‘mean of means’ (e.g., GIESE & al. 1999, KOOYMAN & al. 1992), variability in mean resting heart rate is seen to be quite extensive: The former authors mention 70-92 bpm for Adélie penguins resting prone, while the latter found mean values between 56-80 bpm for Emperor penguins standing on land.
METHODOLOGICAL CONSIDERATION: In THIS THESIS, heart rate was obtained from the same focal birds over a number of days. As even within-individual resting heart rate showed substantial differences on different days, no attempt was undertaken to ‘average’ heart rate prior to analyses.
The effect of wind speed was incorporated by using each animal as their own control (BALDOCK &
SIBLY 1990). Ranges will be provided to enable the reader to draw their own conclusions.