THE FORAGING ECOLOGY OF EMPEROR PENGUINS (APTENODYTES
FORSTERD AT TWO MAWSON COAST COLONIES, ANTARCTICA
by
Graham G. Robertson, Dipl. Agric., BSc, MSc
A thesis submitted in fulfilment of the requirements for the degree
of Doctor of Philosophy
UNIVERSITY OF TASMANIA
August 1994
xiii
STATEMENT OF ORIGINALITY
Except where otherwise stated, the work in this thesis is my own. The work
contains no material which has been accepted for the award of any other higher
degree at any tertiary institution.
Graham G. Robertson.
AUTHORITY OF ACCESS
This thesis may be made available for loan. Copying of any part of this thesis is
prohibited for two years from the date this statement was signed; after that time
limited copying is permitted in accordance with the Copyright Act 1968.
Graham G. Robertson
(5 March 1995)
Quintessential Antarctica: Auster emperor penguin colony in mid-winter, showing milky~blue grounded
ice bergs, pink twilight skies and 11,000 male emperor penguins (and a few
distracted individuals) huddling for shared warmth.
iii
ODE TO AN EMPEROR
(originally to a mouse)
I'm truly sorry man's dominion
has broken nature's social union
An' justifies the ill opinion
which makes thee startle
At me, thy poor earth-born companion
An' fellow mortal
- Robbie Burns (1785)
iv
ABSTRACf
1. The foraging ecology of emperor penguins was examined at two colonies on the
Mawson Coast of Antarctica during the winter, spring and summer of 1988. The
study sought to quantify the penguin's reproductive performances and chick
mortality schedules, chick diet composition, energy intake and food consumption of
adults and chicks, and adult hunting performance during the period of chick care.
2. Several techniques commonly used for conducting ecological research on
penguins were modified for use on emperors. These included techniques for:
capture and restraint, measuring body masses, marking individuals for
identification, sampling stomach contents, preventing liquid radio-isotopes from
freezing in sub zero temperatures, handling adults during incubation and brooding,
withdrawing blood samples and attaching dive recorders. The techniques are of
particular relevance to field research conducted during the Antarctic winter.
3. The population size and breeding success of emperor penguins at the Auster and
Taylor Glacier colonies was estimated from winter photographs of incubating males
and collections of abandoned eggs and dead chicks. At Auster a total of 10,963
pairs produced about 6,350 fledglings for a breeding success of 58%. At Taylor
Glacier about 2,900 pairs raised 1,774 fledglings for a breeding success of 61 %.
Fledglings left Taylor Glacier over a period of 33 days at a mean mass of 10.56 kg.
4. A validation study was conducted on the tritiated water (HTO) and sodium-22
(22Na) turnover methods as estimators of dietary water and sodium intake by freeranging emperor penguins. Penguins assimilated 76.2% and 81.8% of available
energy in squid and fish diets, respectively. Both isotopes had equilibrated with
body water and exchangeable sodium pools by 2 h after intramuscular injection.
The tritium method yielded reliable results after blood isotope levels had declined
by 35%. On average the tritium method underestimated water intake by 2.9%, with
a range of -10.3% to +11.1%. The 22Na method underestimated Na intake on
average by 15.9% with the errors among individuals ranging from -37.2% to -1.8%.
Discrepancies with 22Na turnover were significantly greater with the squid diet
than the fish diet. The results confirm the reliability of the tritium method as an
estimator of food consumption by free-living emperor penguins (provided sea water
and fresh water ingestion is known) and support the adoption of the 22Na method
v
to derive an approximation of sea water intake by tritiated emperor penguin chicks,
and by tritiated adults on foraging trips of short duration.
5. The diet composition of emperor penguin chicks was examined at Auster and
Taylor Glacier colonies by water-offloading adults serially between hatching in midwinter and fledging in mid-summer. Chicks at both colonies consumed a similar
suite of prey species. Crustaceans occurred in 82% of stomach samples at Auster
and 87% of stomachs at Taylor Glacier and were heavily digested; their
contribution to food mass could not be quantified. Fish, primarily bentho-pelagic
species, accounted for 52% by number and 55% by mass of chick diet at Auster
and squid formed the remainder. At Taylor Glacier the corresponding values were
27% by number and 31% by mass of fish and 73% by number and 69% by mass of
squid. Of the 33 species or taxa identified the fish Trematomus eulepidotus and the
squid Psychroteuthis glacialis and Alluroteuthis antarcticus accounted for 64% and
74% of the diets by mass at Auster and Taylor Glacier respectively. The sizes of
fish varied temporally but not in a linear manner from winter to summer. Adult
penguins captured fish ranging from 60 nun (Pleuragramma antarcticum) to 250 nun
(T. eulepidotus) in length and squid (P. glacialis) from 19 nun to 280 mm mantle
length. The length-frequency distribution of P. glacialis showed seasonal variation
with the size of squid increasing from winter to summer. The energy density of
chick diet mix increased significantly prior to fledging.
6. The energy requirements and food consumption of emperor penguin chicks during
their 150-day development was studied at Auster and Taylor Glacier colonies by
means of doubly labelled water (3H2180)-derived estimates of field metabolism
and measurement of tissue energy accumulation during growth. Growth rates to
asymptotic mass ranged from 19 g.d- 1 for brooded chicks to 74 g.d- 1 for chicks
mid-way through their development. Tritiated water derived feeding rates ranged
from 199 g.kg- 1 d- 1 for brooded chicks to 44 g.kg- 1.d- 1 for pre-departure fledglings,
which were fed a sub-maintenance ration following attainment of asymptotic mass.
Mass-specific field metabolic rates declined from 583 kJ.kg-1.d -1 for chicks
weighing about 1 kg to 323 kJ.kg- 1.d- 1 for chicks near to asymptotic mass (c 12 kg).
Field metabolism scaled on body mass was best described by FM = 0.446 MO.91 (r2
= 0.74; n = 32), where FM is field metabolism (MJ.d- 1) and M is chick mass (kg).
The relationship was statistically indistinguishable from tritiated water-derived
estimates of FM for chicks fed a ration suitable for maintenance (growth excluded)
only. An 'average' chick expended a total of 444 MJ metabolized energy during
development, which consisted of 125 MJ accumulated in new tissue and 319 MJ
VI
expended for maintenance. Food intake to satisfy total metabolized energy was 84
kg, which represents the amount of food required to produce an emperor penguin
chick from hatching to independence. Based on this estimate and knowledge of
chick diet composition, chicks at Auster and Taylor Glacier colonies consumed an
estimated 648 tonnes and 290 tonnes of food, respectively, during the 1988
breeding season.
7. The food and energy requirements of adult emperor penguins parenting chicks
were examined at Auster (about 11,000 pairs) and Taylor Glacier (about 2,900
pairs) colonies during the winter, spring and summer of 1988. Tritiated waterderived estimates of adult food consumption trebled during the five-month period
of chick care. For birds at sea, estimates ranged from 89 g.kg- 1 .d -1 (2.3 kg.d- 1) in
winter when chicks were < 5 % of adult mass, to 259 g.kg- 1 .d- 1 (6.3 kg.d- 1) in
summer, when chicks represented 40 - 50% of adult mass. These food consumption
rates were equivalent to the acquisition of 440 kJ.kg- 1 d- 1 (11.4 MJ.d- 1) and 1,380
kJ.kg- 1.d-1 (33.4 MJ.d-1) metabolizable energy in winter and summer respectively.
Chick provisioning was not accompanied by a major increase in food consumption
by adults. Adults assimilated 85-92% of their daily food intake themselves and
retained the remainder for the chick. The food ration of chicks for the three seasons
(648 tonnes at Auster) constituted only about 6% of the total food intake by the
adults during the same period. In spite of this, adults appeared to be operating
near their maximum food gathering capacity when raising chicks. Adults consumed
an estimated 482 kg of food (including the ration for the chick), which amounts to
about 10,615 tonnes and 2,800 tonnes of fish and squid consumed by the breeding
populations at Auster and Taylor Glacier, respectively.
8. The diving performance of adult emperor penguins was examined in winter,
early spring, late spring and summer. These seasons coincided with the brood,
creche, mid-growth and pre-fledging stages of chick development, respectively. The
distribution in the water column of modal depths did not appear to be affected by
season. Mean maximum dive depth (53-66 metres) was similar for all four seasons,
as was mean maximum dive duration (2.8-4.1 minutes). Maximum depths and
durations of individuals in the four groups ranged from 130-460 metres and from
6.2-22.0 minutes, respectively. Diving was restricted to daylight and twilight, and
dive rate increased as day length increased, from 64.1 ± 26.9 dives/ day in winter to
131 dives/day in summer (one individual). Deep dives occurred at any time of the
day, not only during periods of peak light intensity. The large proportion of
ben tho-pelagic prey in the emperors' diet, combined with knowledge of their dive
vii
patterns, suggests the emperors' hunted prey in the meso-pelagic region of the water
column, including on the sea bottom of the continental shelf. The penguins' prey
composition, prey habitat, marine topography, seasonal changes in the fast-ice and
the birds' diving performances are used to make some basic estimates of the
foraging locations and prey capture rates of emperor penguins.
I,
,!
!
,
.'",
,
\'
UTAS
'-.
.,.,
;t,
~
>
-'-j"
.- --- - _ . - ,
----~-.-
viii
ACKNOWLEDGEMENTS
This study would not have taken place without the initiative and foresight of Harry
Burton and the late Dr. Gavin Johnstone, both of the Australian Antarctic Division.
It was Harry and Gavin's idea that the Division commence a study on emperor
penguins and that it should be located on the Mawson Coast, one of the most ideal
places in Antarctica to conduct overwintering studies on emperors. I am grateful to
Harry and Gavin for giving me the freedom in the initial stages of the study to
rationalise the various themes to be addressed, and for the opportunity to conduct
the field program and compile this thesis.
The emperor penguin is the largest seabird and since it is the only species of bird to
breed through the severe Antarctic winter and spring it is arguably the most difficult
seabird to study. Although I had spent 14 years conducting field work in the
Australian arid zone before going to Mawson, the work on the emperors was
undoubtedly the most difficult field work I had ever conducted. The difficulties
that arose were mainly due to the logistical problems of conducting an extensive
ecological study on emperors in the dim light and cold of winter, and the newness
of some of the more intrusive aspects of the program. Within this context, it is
important to stress that the extent to which the program was successful was largely
a product of the unstinting support afforded by the 24 people with whom I
overwintered. These expeditioners are too numerous to mention by name, so I
thank them all collectively. A few, however, cannot remain nameless. Deserving of
special thanks are Phil Barnaart, Dave McCormack and Tony Everett for the
pivotal roles they played in the program. Phil, the station leader, not only assisted
in the field but did a great deal at the station, sight unseen by me, to ensure the field
program ran smoothly. Dave and Tony, both tradesmen, between them have spent
eight winters in Antarctica and their knowledge of the sea-ice and the weather, and
the interplay between the latter and the logistical side of the emperor work, reduced
my learning curve to a minimum and cut my mistake rate to a tolerable level.
I am grateful to Arthur Alexander, a diesel mechanic, for the 2.5 months he spent
helping in the field on this project and for his capacity to work a t any hour ofthe
day and in all weather conditions, no matter how atrocious. I also thank him for
his tolerance during the seven weeks we worked alone together at Taylor Glacier at
the end of the study, when for reasons unknown to both of us our capacity to
ix
maintain civil lines of communication fell dismally short of optimal levels. That the
data collection continued unabated testifies to Arthur's commitment to the emperor
program and his utility as an Antarctic expeditioner.
I am grateful to Brian Green and Keith Newgrain, both from the CSIROs Division of
Wildlife and Ecology, and to Roger Handsworth, of Platypus Engineering. Much of
what I know about isotope dilution work on seabirds I learnt from Brian and Keith
and I thank them both for their contributions during the formative stages of the
study and for their advice during the extensive laboratory work that resulted from
the field program. Roger, in consultation with Harry Burton and myself, designed
and built the electronic time-depth recorders used during the study and wrote the
software to analyse the penguin dive records. The winter deployment of timedepth recorders on emperors was pioneering work and carried considerable risk of
failure, given the likely effect of the cold on the microprocessors and power supply,
and the potential for the instruments to be damaged when the emperors dived in
dense pack-ice. Having neither seen an emperor nor experienced Antarctic
conditions, and with minimal time for testing during manufacture, Roger built
devices that functioned almost perfectly in all seasons. This 'strike rate' with the
emperor work attests to Roger's insightfulness and creativity in the engineering of
instruments for use under extreme conditions.
In the formative stages of this project my capacity to answer many of the research
questions about the emperors was shrouded in mystery, mainly because much of the
work was either new for the species or new for the winter period in which it was
conducted. The emperors large size and great strength were problems in theory
only, and in practise were mostly offset by the their phlegmatic disposition and
general approachability at the colony. Of greater concern was the emperors nonterritorial breeding habit, which made finding experimental birds particularly
difficult and often traumatic (for both penguin and researcher, due to the effect of
disturbance to non-experimental adults and chicks), and the penguins habit of
breeding in the darkness and cold of winter.
Emperors rear chicks in five months between mid-winter and mid-summer, and
most of the field work took place over this period. During this time emperors
conduct all the behaviours that characterise reproduction and care of the young in
wind-chill equivalent temperatures that may reach 90°C lower than the body
temperature of both the birds and the people studying them. To a person windchill equivalent temperatures of -50°C and lower seem incomprehensible, but to an
x
emperor they are a normal part of living and breeding in the cold. Our inability to
comprehend the capacity of emperors to cope in these temperatures reflects the
enormity of the gulf between the behavioural and physiological adaptations of
emperors and those of ourselves. Unlike the penguins the researcher possesses no
natural strategies for survival in the cold and in order to conduct productive field
work this gulf must be bridged by creative use of technology.
This is a long winded way of stressing the role played in the program of an apple
hut, a set of portable sheep yards, and a hagglunds oversnow vehicle. The apple
hut, a 3 metre diameter fibre glass dome, was indispensable for severe weather
work on the birds and for people to shelter in during blizzards. Rod Ledingham
bought the concept of an apple hut to my attention and made one available for the
study. The sheep yards were indispensable for temporarily restraining penguins, an
essential activity for most aspects of the study. Without the yards the integrity of
the isotope dilution work (Chapters 6 and 7), in particular, would have been
seriously compromised. The last serious work at Auster colony took place in the
1950s and relied on sledging dogs as a means of transport. I was fortunate to have
at my disposal a hagglunds oversnow vehicle, which was functional and reliable to
the point that nearly all one's time and energy could be devoted to the emperor
program, rather than to the logistical details of transportation and to devising ways
to cope during the next change in the weather.
It is customary in theses such as this to mention near the end of the list of
acknowledgements the contribution of one's immediate family, but it would
probably be more pertinent if they were listed first, such is the behind-the-scenes
contribution they usually make. I am grateful to my wife Debby for releasing me
from domestic duties to indulge myself with the emperors, and to daughters Anna
and Jacqui for enduring my 14-month absence in Antarctica and my mental
detachment from family life in the several intensive months it took to finish the
thesis.
I am also grateful to Jenny Cole for her assistance with various aspects of the typing
of this thesis, and to my supervisor, Dr David Ritz, for his administrative support
at the University, for his critical comments of drafts of each chapter and for his
tolerance with the time it took for me to bring this thesis to completion.
Finally, a word about the emperors. In my, moderately biased, opinion Auster
emperor penguin colony during winter lies at the epicentre of the experiences on
xi
offer by the Australian Antarctic Research Program. Very few people have the
opportunity to overwinter with the emperors and experience first-hand these
wonderful, phlegmatic birds at a time of year when they exhibit all the qualities that
enable them to thrive on the edge of existence. The experience is powerful enough to
puncture the soul of any mortal human, and behoves on those fortunate few, as a
kind of pay-back for the emperors tolerance and gocxl grace during
experimentation, the responsibility to look out for them in the future when the
volatile mix of human attitudes comes to bear on the management of the frozen
continent the emperors call home. I hope the particles of insight included in this
thesis will contribute to the well being and longevity of all emperor penguin
populations in Antarctica .
.~ .
~
- - - - - - - - - - - - - - - - - - - - - - - - - ---
.\,
.
'.,'
.'
Ii
UTAS
--~.-.. -
- --~ ----------
,
:i
d
'I
.,;
.. --.~- --- .- ----~. --"
xii
TABLE OF CONTENTS
Page
DECLARATION
ii
FRONTISPIECE
iii
ABSTRACT
iv
ACKNOWLEDGEMENTS
viii
CHAPTER 1: INTRODUCTION
1
1.1 Thesis presentation
7
CHAPTER 2: SOME FIELD TECHNIQUES FOR ECOLOGICAL
RESEARCH ON EMPEROR PENGUINS
8
2.1 INTRODUCTION
8
2.2 DESCRIPTION OF TECHNIQUES
9
2.2.1
Catching and restraining emperor penguins
9
2.2.2 Weighing emperor penguins
10
2.2.3
Marking emperor penguins for identification
11
2.2.4
Procuring stomach contents
12
2.2.5
Keeping radio-isotopes liquid in sub zero temperatures
14
2.2.6 Handling incubating males
15
2.2.7 Handling adults brooding chicks
16
2.2.8
Collecting blood samples
17
2.2.9
Attaching dive recorders to foraging birds
18
2.3 ACKNOWLEDGEMENTS
19
CHAPTER 3: POPULA nON SIZE AND BREEDING SUCCESS
OF EMPEROR PENGUINS AT AUSTER AND TAYLOR
GLACIER COLONIES
20
3.1 INTRODUCTION
20
3.2 STUDY COLONIES AND METHODS
21
3.2.1
Auster colony
21
xiii
3.2.2
Taylor Glacier colony
3.2.3 Counting emperor penguins
21
22
3.3 RESULTS
23
3.3.1
Population size
23
3.3.2
Breeding success
24
3.3.3
Pattern of chick mortality
25
3.3.4
Chronology of fledging
25
3.4 DISCUSSION
27
3.5 ACKNOWLEDGEMENTS
30
CHAPTER 4: EFFICACY OF THE TRITIATED WATER AND 22N A
TURNOVER METHODS FOR ESTIMA TING FOOD AND
ENERGY INTAKE BY EMPEROR PENGUINS
31
4.1 INTRODUCTION
31
4.2 MATERIALSANDMElHODS
32
4.2.1
General
32
4.2.2
Energy assimilation efficiency
33
4.2.3
Isotope administration and blood sampling
33
4.2.4
Isotope turnover rates
34
4.3 RESULTS
35
4.3.1
Energy assimilation efficiency
35
4.3.2
Isotope equilibration rates
35
4.3.3
Water turnover and food intake
36
4.3.4 Sodium turnover and food intake
37
4.4 DISCUSSION
37
4.5 ACKNOWLEDGEMENTS
41
CHAPTER 5: DIET COMPOSITION OF EMPEROR PENGUIN CHICKS
AT TWO MAWSON COAST COLONIES, ANTARCTICA
42
5.1 INTRODUCTION
42
5.2 METHODS
43
5.2.1
Penguin colonies and breeding pattern
43
5.2.2
Collecting stomach samples
43
xiv
5.2.3
Determining sex of adults
44
5.2.4 Sorting stomach samples
45
5.2.5
Identifying fish remains
46
5.2.6
Identifying cephalopod remains
47
5.2.7 Identifying crustacean remains
47
5.2.8
Data treatment
47
5.2.9
Determining food energy content
48
5.3 RESULTS
48
5.3.1
Stomach contents digestion and prey hard part erosion
48
5.3.2
Adult arrival mass and stomach content mass
49
5.3.3
General diet composition
49
5.3.4
Fish
50
5.3.5
Squid
51
5.3.6
Diet differences between colonies
51
5.3.7
Energy density of prey
52
5.38
Stones
52
5.4 DISCUSSION
53
5.4.1
Caveats on the data
53
5.4.2
Differences between colonies
54
5.4.3 Characteristics of prey and penguin foraging
55
5.4.4 Comparisons with other studies
57
5.5 ACKNOWLEDGEMENTS
57
CHAPTER 6: THE ECOLOGICAL ENERGETICS OF EMPEROR
PENGUIN CHICKS DURING THEIR DEVELOPMENT
58
6.1 INTRODUCTION
58
6.2 METHODS
59
6.2.1
Study colonies and environment
59
6.2.2
Salient features of the reproductive cycle
60
6.2.3 Selecting experimental chicks
60
6.2.4
62
Estimating water and sodium fluxes and field metabolic rates
6.2.5 Determining body composition
66
6.2.6
67
Estimating food consumption and energy budget
6.2.7 Estimating seawater consumption
68
6.2.8
69
Estimating snow consumption
xv
6.3 RESULTS
69
6.3.1
Recapture success
69
6.3.2
Seawater and snow consumption
69
6.3.3
Body composition
71
6.3.4 Growth
6.3.5
Water influx, food intake and energy expenditure
6.4 DISCUSSION
72
72
76
6.4.1
Caveats and explanations
75
6.4.2
Body composition
79
6.4.3
Growth
81
6.4.4
Energy expenditure
81
6.4.5
Energy budget
83
6.4.6
Energy intake and food consumption
84
6.5 ACKNOWLEDGEMENTS
87
6.6 POSTSCRIPT
88
APPENDIX 6.1
89
APPENDIX 6.2
90
CHAPTER 7: THE FORAGING ENERGETICS OF ADULT EMPEROR
PENGUINS DURING CHICK REARING
92
7.1 INTRODUCTION
92
7.2 METHODS
93
7.2.1 General
93
7.2.2 Colonies, timing and adult selection
93
7.2.3 Determining dietary water and food energy density
94
7.2.4 Estimating water influx and feeding rate
95
7.2.5 Correcting estimates of water influx
96
7.3 RESULTS
97
7.3.1
Recapture success
97
7.3.2
Seawater consumption
97
7.3.3
Body masses, mass gains and cycle times
98
7.3.4 Water influxes and feeding rates
7.4 DISCUSSION
99
100
xvi
7.4.1 Effects of experiments
100
7.4.2 Tritium method and energy balance
101
7.4.3 Feeding rates and energy expenditure
103
7.4.4 Population requirements
106
7.5 ACKNOWLEDGEMENTS
108
CHAPTER 8: DIVING PERFORMANCE OF EMPEROR PENGUINS
DURING CHICK REARING
109
8.1 INTRODUCTION
109
8.2 METHODS
110
8.2.1
110
Salient features 0 f the breeding cycle
8.2.2 Experimental design and dive recorders
110
8.2.3
111
Analysing dive records
8.3 RESULTS
112
8.3.1
Recapture success and data retrieval
112
8.3.2
Cycle times and mass gains
113
8.3.3
Dive depth and duration
113
8.3.4 Daily dive rate
114
8.3.5
115
Diurnal patterns
8.4 DISCUSSION
115
8.4.1 Dive patterns
115
8.4.2 Ecological considerations
116
8.5 ACKNOWLEDGEMENTS
121
CONCLUSIONS AND FUTURE RESEARCH
122
REFERENCES
127
1
CHAPTER 1: INTRODUCTION
With the purpose of setting the stage for the chapters that follow, this section
includes a brief description of the emperor penguin yearly cycle, a summary of the
present state of knowledge on emperor penguin biology (so the current work can be
placed in historical and biological perspective) and the overall aims of the study
and structure of the thesis. A systematic review of the literature has not been
included in this introduction because the literature on penguins in general, and
emperor penguins in particular, has been cited extensively in the appropriate
sections of the thesis and to review it again would be unnecessarily repetitive. For
this reason the themes of previous studies, rather than the details of their findings,
are mentioned below.
The breeding cycle of emperor penguins is only briefly described, because various
aspects of the cycle (but not the entire cycle) central to each chapter are summarised
in the appropriate sections of the chapters that follow. However, compared to other
bird species the annual cycle of emperors is extraordinary, and for the work that
follows to be placed in context with respect to the range of activities exhibited by
emperors during the course of the year, a description of the penguins' annual
calendar is included below.
Understanding of the annual cycle of emperor penguins relies mostly on
observations of birds at the Pointe Geologie colony (66°40'5; 140 0 01'E) as reported
by Prevost (1961), Mougin (1966) and Le Maho (1977). The breeding cycle lasts nine
months, but extends to a full year when adult pre- and post- breeding maintenance
requirements are included. The breeding period is inextricably linked to the annual
setting and breaking out of the fast sea-ice on which the penguins establish their
colonies, and this places time limits on the extent of the various stages in the annual
cycle. For simplicity the cycle can be divided into the summer maintenance period,
the autumn pre-nuptial period, the winter incubation period and the chick rearing
period.
For birds that bred successfully the previous year, the summer maintenance period
begins in late December or early January with a 30 day stint at sea when adults rebuild their energy reserves in preparation for the moult. Following the moult,
which lasts about 20 days, the birds fatten again at sea in preparation for the pre-